phototropism experiment conclusion

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Experiment: How do plants “see” light?

Can plants really “see” the light.

Scientists call a plant’s ability to bend toward light phototropism . Even as far back as ancient Greece it’s been a big puzzle about how plants are able to do it. People experimented with how plants accomplish this amazing feat, but no one really figured out how it worked—until Charles Darwin came along, that is.

Although Darwin is most well-known for his studies on evolution, he was also a prolific scientist in general. The questions about phototropism piqued his curiosity, and he thought of an ingenious experiment to test how plants are able to see light. In this experiment, we’ll recreate what he did, and at the end we’ll dive further into the science.

3 small cups full of soil Tape, a marker, and 3 sticky notes Medium-sized box (such as a shoebox or a storage cube) 12 corn seeds Aluminum foil Small cookie sheet that fits inside the box (or another sheet of aluminum foil) 1 Straw Water

• Plant four corn seeds in each of the soil cups. Make sure they’re evenly spaced, and plant them just a half inch under the dirt.
• Water the cups, and dump out any excess water (be careful not to tip the soil and seeds out). Place the cups on the cookie sheet or aluminum foil. This will prevent moisture and dirt from soaking through the box.
• Place the cups/cookie sheet setup inside of the box. Make sure it’s open on one side so that light is coming in from an angle. Place in a windowsill, with the open side facing the sun. (You might need to stack some books underneath it to support it, if your windowsill isn’t very wide.)
• Shoot cap: Cut a small 2″ x 3″ square of aluminum foil. Wrap it around the tip of a straw to create a small, closed-ended metal cap, and slide it off. This will be placed over the tip of the growing shoot to cover any light coming in to the tip.
• Base sleeve: Cut a small 1/2″ x 3″ square of aluminum foil. Wrap it around the middle of a straw so it creates a small open-ended 1/2″ tall tube, and slide it off. This will be placed around the growing shoot so that it can grow through it.
• Check the cups each day. Once they send up a shoot about half an inch high, place either a shoot cap (on Tip seedlings) or a base sleeve (on Base seedlings) around them, depending on which cup they’re in. The control cup will get neither of the light exclusion devices. The seedlings might grow at different rates, so be sure to check each day to put the caps/sleeves on as needed. They grow fast once they germinate!
• Continue to water the seedlings as needed.
• Check the seedlings after a week. What has happened? Compare the seedlings with the caps and the sleeves to the control seedlings. Are any of them growing in certain directions?

How did the seedlings “see” the light?

If the experiment worked correctly, you should have noticed that the seedlings that were covered with caps at the tip grew straight up, while the control seedlings and the seedlings with the bases covered bent towards the light. This is phototropism in action.

Darwin correctly concluded that plants are able to “see” light using the tips of the plant shoots, rather than through the stalks. It wasn’t until a bit later that scientists figured out exactly why that was, though.

It turns out that plants are able to grow by using hormones such as auxins and gibberellins . Auxin in particular tells individual cells to reach out and grow longer, like Stretch Armstrong. It’s one of the ways that plants grow taller. Normally, plants growing with an unshaded light source will grow straight up towards the sun because auxin is evenly distributed all around the shoot.

But when the light is heavily shaded and comes in from an angle, something interesting happens. Auxin starts to concentrate on the shaded side of the plant instead, and as a result, the cells on the sunny side stay the same size but the cells on the shaded side grow longer. This causes the plant to tip and grow towards the light.

Auxin is primarily produced in the tips of the plants. This is why the plant grew straight up when you covered the tip with a cap—it couldn’t “see” the light anymore! The tips of the control seedlings and the seedlings with the bases covered could still sense the light, so they grew towards the sunlight.

Thanks to Charles Darwin and modern science, the mystery of how plants grow towards light was finally solved.

Learn more about phototropism:

To understand plant tropisms, you first have to understand plant hormones. We created an excellent page about Plant Growth Hormones  here and here .

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Lindsay graduated with a master’s degree in wildlife biology and conservation from the University of Alaska Fairbanks. She also spent her time in Alaska racing sled dogs, and studying caribou and how well they are able to digest nutrients from their foods. Now, she enjoys sampling fine craft beers in Fort Collins, Colorado, knitting, and helping to inspire people to learn more about wildlife, nature, and science in general.

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Science project, plant phototropism experiment.

As plants grow, they move up toward the light. But what is a plant’s favorite color? Do plants move toward some colors more than others?

Do plants bend toward certain colors of light?

• 2 1-foot tall cardboard boxes with lids
• Piece of cardboard
• 2 small lamps
• 2 full spectrum light bulbs
• Box cutter knife
• Masking tape
• 1 3” x 3” piece of clear, red, green, and blue cellophane
• Spray bottle
• 8 bean seeds
• 8 small pots
• First, get your plants growing. Plant two of your bean seeds in two different pots, water them, and wait for them to poke out of the ground.
• While you’re waiting, get your boxes ready.  Cut a hole 2” in diameter about 3 inches from the bottom of each box. Place the clear cellophane over the hole. This will let all of the light into the box. Over the hole in the other box, place the red cellophane. This will only let red light into the box.
• Put one plant in the first box and one in the second. Use a ruler to position each bean plant two inches away from the cellophane window.  Take a photo of the plants, looking downward from the top of the box.
• Put the boxes on different sides of the same room.
• Now it’s time to light things up! Put the lamps next to the boxes on the side with the cellophane window. Take out your ruler again and measure to make sure that the lamps are the same distance from the hole.
• Put the lids on each box.
• Every morning, turn on each lamp. Every night, turn off the lamps before you go to bed. Leave the plants to grow for a week.
• After a week has passed, remove the lid and take a photo looking downward. Then remove the plants and take a photo from the front. Do the plants look different? Is one taller than the other? Is one twisted in a different direction?
• Do the same experiment with new bean plants, but change the color of cellophane to blue. Finally, repeat the experiment with green cellophane.
• Compare the photos of each bean plant after it had been growing for a week. Did the plants turn more toward a certain color? Was there a color they didn’t like?

The control plants will do better than the plants that are only exposed to one wavelength of light. The plants will grow better in red and blue light than in green light. The plants will grow toward red and blue light but will not move toward the green light.

Plants love the light, right? Yes and no. Plants do love the light, but they like some wavelengths of light more than others.

When you look at a rainbow, you can see that the visible spectrum of light actually has different colors or wavelengths inside it.  The visible spectrum is the light that we can see. Different objects reflect different types of light. A blue bowl reflects blue light. A green plant reflects green light.

Inside a plant are chloroplasts . Inside the chloroplasts are tiny molecules called photopigments . Photopigments help the plant absorb light. A plant has different types of photopigments so it can absorb different colors of light.

When natural light shines on a plant, that plant takes in the light from the different wavelengths and uses it to make food.  This natural light is called white light, and it contains all of the types of light. If there’s only one color of light shining on a plant, then only some of the photopigments work, and the plant doesn’t grow as well. This is why your plant under the full light spectrum grew better than the plants with the cellophane filters.

Plants also move toward the light. Seeds push little leaves up from the ground into the light. A house plant in a dark room will grow toward the light. This movement in response to light is called phototropism . When a plant moves toward the light, it’s called positive tropism . When a plant moves away from light, it’s called negative tropism .

How do plants move? They do so with the help of chemicals called auxins . Think of auxins as an elastic band for cells. They help cells get longer and move. Sunlight reduces auxin, so the areas of the plant that are exposed to sunlight will have less auxin. The areas on the dark side of the plant will have more auxin. That means that they will have long, stretchy cells. This allows the plant to move toward the light.

The plants in your experiment likely showed positive tropism, except when it came to the green light. Why did the plants not move toward the green light? Plants are green, which means that they reflect green light. It bounces off the leaves. This means that they can’t use green light very well, and the green light bounces off the plant instead of encouraging movement toward the light.

Digging Deeper

What would happen if you left plants for a long time in light that was only red or blue? Would they survive? 

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PHOTOTROPISM EXPERIMENTS

Branch botany (plants).

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Article Contents

What are the kinetic properties of higher plant phototropism, how does red light affect phototropism, auxin distribution and phototropism, what chromophore detects the blue light, finally, a photoreceptor protein for phototropism: a short summary, phototropin-mediated signal transduction pathways: fiercely independent, lov domains: chromophore domains with a unique photochemistry, some final thoughts, postscript: lov beyond the plant kingdom, acknowledgments, literature cited.

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Phototropism: Some History, Some Puzzles, and a Look Ahead

This work was supported by the National Science Foundation.

Address correspondence to [email protected] .

www.plantphysiol.org/cgi/doi/10.1104/pp.113.230573

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Winslow R. Briggs, Phototropism: Some History, Some Puzzles, and a Look Ahead, Plant Physiology , Volume 164, Issue 1, January 2014, Pages 13–23, https://doi.org/10.1104/pp.113.230573

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Though few and far between, phototropism studies through 1937 established a number of important principles. (1) Blue light is the active spectral region. (2) The phototropic stimulus is perceived by the coleoptile tip, and the consequences of the stimulation progress down into the growing region. (3) Lateral transport of auxin mediates the curvature response. (4) The reciprocity law holds for first positive curvature, whereas second positive curvature is time dependent. (5) Red light treatment had a major effect on phototropic sensitivity. Later studies established the following. (6) Seven blue light receptors (cryptochromes, phototropins, and three F-box proteins) were identified and characterized. (7) A flavin was established as the photoreceptor chromophore for all seven. (8) The chromophore domain, designated the LOV domain (for light, oxygen, or voltage), carries out a unique photochemistry. (9) LOV domains must be truly ancient chromophore domains. There remain some puzzles. The fluence-response threshold level for first positive curvature is far below that for phototropin photochemistry. Likewise, the fluence-response threshold level for the red light effect on coleoptile phototropism is far below those for phytochrome phototransformation. Cytological effects of red light are also very insensitive compared with the physiological effects of red light. What is the mechanism allowing for this extraordinary photosensitivity? How is phototropin specificity controlled? What are the functions of the phytochrome kinase substrate proteins in both phytochrome and phototropin responses? What mechanism leads to lateral auxin transport? Finally, are LOV domain proteins true photoreceptors in all of the bacteria in which they occur? If so, what is their biological function?

Even in the ancient world, astute observers noted that plants could turn to face the sunlight. What was originally designated heliotropism for plants that followed the sun eventually became divided into two distinct response categories: solar tracking (the real heliotropism), a repetitive and completely reversible turgor-driven process; and phototropism, an irreversible directional growth response determined by light direction. Over the past 200 years, a large number of brilliant biologists, including Julius Sachs (1864) , Charles Darwin (1881) , Frits Went (1928) , and Kenneth Thimann ( Went and Thimann, 1937 ) have applied their talents to examining and elucidating the mechanisms accounting for both of these responses. The entire history of phototropism and solar tracking parallels and is intertwined with that for a number of other blue light responses, found not just in higher plants but in bryophytes, ferns, algae, fungi, and, most recently bacteria. For a detailed account of this history, see Briggs (2006) .

Progress in research on blue light-activated processes over the last half century was severely hampered by a lack of knowledge of the relevant blue light receptors. By contrast, the discovery and initial characterization of a red/far-red-reversible phytochrome ( Butler et al., 1959 ) nurtured an enormous and sophisticated body of knowledge about these photoreceptors: their structure, their chromophores, their photophysics and photochemistry, and the extraordinary signal transduction networks that they rule. Meanwhile, although a huge and scattered body of knowledge on blue light responses in plants and fungi accumulated, there was scarcely a clue to what the photoreceptor(s) might be, and competing hypotheses abounded. Attention focused on the physical and physiological characterization of responses to blue light and, eventually, biochemical investigations of intriguing in vitro photochemistry. It was only with the advent of modern molecular genetics and its extraordinary capabilities that research on blue light photobiology finally began to catch up with phytochrome photobiology 20 years ago and the first blue light receptor, cryptochrome1 (cry1), became identified ( Ahmad and Cashmore, 1993 ).

This review will go back to some of the puzzles of earlier years, a few over 100 years old, and provide a glimpse of the status of these puzzles today. They arose from studies of response kinetics, action spectroscopy, interactions between blue and red regions of the visible spectrum, and discrepancies between in vivo and in vitro results. Although the focus will be on higher plant phototropism, several other blue light responses will contribute to the discussion. No effort will be made to be comprehensive. Any effort here would be redundant with that of three recent excellent reviews on phototropism ( Sakai and Haga, 2012 ; Christie and Murphy, 2013 ; Hohm et al., 2013 ) and on LOV (for light, oxygen, or voltage) domain photochemistry ( Losi and Gärtner, 2011 , 2012 ). The article concludes with a look at the unexpected role of LOV domains in prokaryotes.

Over a century ago, Fröschel (1908) and Blaauw (1909) first reported that the phototropic responses of Lepidium spp. seedlings and Avena spp. coleoptiles, respectively, obeyed the reciprocity law of Bunsen and Roscoe (1862) . The law states that as long as the light dose (fluence: intensity × time) is held constant, a given light response, in these two cases phototropism, will remain the same over a broad range of intensity × time combinations. In both cases, the authors were investigating threshold responses, something that later investigators tended to forget. Meanwhile, du Buy and Nuernbergk (1934) collected data from a number of authors and published the fluence-response curve shown in Figure 1 for the phototropic responses of Avena spp. coleoptiles over an immense range of fluences (8 orders of magnitude). The first maximum was designated first positive curvature, the immediately subsequent minimum first negative curvature, the second maximum second positive curvature, the next minimum a “zone of indifference,” and the final ascent third positive curvature. First positive curvature was usually located only a short distance below the coleoptile tip, whereas second positive curvature extended somewhat farther down the coleoptiles. For some reason, reciprocity tests were never carried out at any fluences above the threshold assays used by Fröschel (1908) and Blaauw (1909) , although their conclusions, unfortunately, became accepted and applied to higher plant phototropism in general. All of this early work was with white light from a variety of sources, and the unit of fluence at the time was the meter-candle second ( MCS ).

Fluence-response curve for the phototropic responses of Avena spp. coleoptiles assembled from the literature by du Buy and Nuernbergk (1934) . From Briggs (1960) .

Over 50 years ago, Briggs (1960) finally reinvestigated the reciprocity relationships of phototropism for maize ( Zea mays ) and oat ( Avena sativa ) coleoptiles over a wide range of fluences and demonstrated that the reciprocity law was valid only for first positive curvature but not for second. In all cases, for fluences above 10,000 MCS , maximum phototropic curvature for both species was attained after about 20 min of unilateral light stimulus irrespective of fluence. Indeed, a flashing-light experiment with a total fluence of just over 30,000 MCS showed that with increasing dark periods but constant flash duration, maximum curvature for maize coleoptiles was only achieved when the total exposure time, dark plus light, was 20 min or more.

Zimmerman and Briggs (1963a , 1963b ) then developed a kinetic model for the phototropic responses of oat coleoptiles, based on a detailed series of fluence-response curves, developing a set of differential equations to describe the various curves. The model for first positive phototropism involved an initial photoreceptor activation and its subsequent photoinactivation, a two-step photoresponse. The model they developed for second positive curvature involved the production of an activated photoreceptor followed by a dark reaction that led to the curvature response. The model, therefore, incorporated a thermal reaction and hence time dependence for the response, accounting for the lack of reciprocity. It also required a second photoreaction that reversed the first photoactivation.

By the early 1960s, it was well established that first positive curvature is responding strictly according to first-order photochemistry: the response is linear with respect to the log of the number of photoreceptor molecules activated. Like first positive curvature, blue light activation of phototropin1 (phot1) phosphorylation also obeys the Bunsen-Roscoe reciprocity law both in vivo and in vitro ( Briggs et al., 2001 ), consistent with this model. The descent of the response curve following the first positive maximum is then thought to involve a decrease in the difference between photoactivation of the photoreceptor on irradiated versus shaded sides of the coleoptiles. As fluences are increased, molecules of the photoreceptor on both sides of the coleoptiles all eventually become photoactivated and the differential disappears. This current hypothesis does not exactly match the model from Zimmerman and Briggs (1963b) for first positive phototropism. However, activation of photoreceptor molecules on the shaded side could replace the photoreceptor inactivation their model requires.

Let us examine the situation for second positive curvature. As exposure time increases, the activated phototropin molecules are postulated to relax gradually to their dark state and can now be reactivated. As there is a light gradient across the organ, reactivation is greater on the illuminated side than on the shaded side of the coleoptiles and a persistent differential becomes established, leading to second positive curvature, time dependent because it depends on the thermal decay rate for the activated photoreceptors. Again, the precise model of Zimmerman and Briggs (1963b) is not directly supported, but the differential reactivation of photoreceptors on the irradiated versus the shaded side of the responding organ could replace the reverse photoreaction they postulated.

Evidence for light-induced differential phosphorylation of phot1 across unilaterally illuminated oat coleoptiles ( Salomon et al., 1997 ) supports the hypothesis that a light gradient leads to a biochemical gradient in an activated photoreceptor, both for first and second positive curvature. Differential activation of auxin-induced gene expression in Brassica oleracea hypocotyls between irradiated and shaded sides by blue light, activity downstream from light-activated phototropin ( Esmon et al., 2006 ), likewise supports this hypothesis. Phototropin phosphorylation has been shown to be required for functional phototropism ( Inoue et al., 2008 , 2011 ). Thus, the time dependence for recovery of phosphorylated phototropin to its unphosphorylated (and physiologically inactive) dark state could account for the time dependence of second positive curvature. Indeed, the measured capacity of phot1 to undergo light-activated phosphorylation in vivo recovers over a period of minutes following a brief saturating light pulse ( Briggs et al., 2001 ). (A saturating pulse is one that is thought to activate all of the photoreceptor molecules at once on both irradiated and shaded sides of the responding organ, a pulse that fails to induce curvature, the first minimum in the fluence-response curve for phototropism [for details, see Briggs et al., 2001 ].) The recovery of phototropic sensitivity after such a pulse follows roughly the same time course ( Briggs, 1960 ).

Two features of the du Buy and Nuernbergk (1934) fluence-response curve remain unexplained: first negative curvature and third positive curvature. First negative curvature has only been demonstrated for oat coleoptiles, is lacking for maize coleoptiles, and has never been reported for dicot seedlings. It remains a puzzle, although Zimmerman and Briggs (1963b) developed a model, similar to that for first positive curvature, that provided a good fit to the data. Third positive curvature might be explained by the fact that the data sets leading to this response differed widely in fluence rate and exposure time used. These differing light conditions could easily have led to curious anomalies in response to yield an apparent “third positive curvature.” The longer exposure times required to achieve these fluences varied, as did the light sources. Indeed, since 1937, there has been no further evidence for a third positive curvature in any species investigated. However, first and second positive curvatures appear to be universal among monocot coleoptiles and dicot seedlings ( Fig. 2 ; Briggs, 1960 ; Zimmerman and Briggs 1963a ; Chon and Briggs, 1966 ; Baskin and Iino, 1987 ; Iino, 2001 ; Esmon et al., 2006 ), including Arabidopsis ( Arabidopsis thaliana ; Konjević et al., 1989 ).

Fluence-response curve for the phototropic responses of maize coleoptiles. From Briggs (1960) .

There is a distressing feature in attempts to correlate light-activated phototropin phosphorylation in vivo with phototropism: the threshold and saturation fluences for blue light activation of first positive curvature lie between 1 and 2 orders of magnitude below those for phosphorylation ( Briggs et al., 2001 ). The physiological response curve is simply not congruent with the photochemical response curve. This apparent paradox is currently unresolved.

Given that blue light activates phototropic curvature and red light normally does not (but see below), a majority of the early phototropism studies depended on red light as a safelight. However, Curry (1957) noted for the first time that small fluences of red light actually reduced the phototropic sensitivity of oat coleoptiles in the first positive curvature range by 1 order of magnitude. Zimmerman and Briggs (1963a , 1963b ) confirmed this dramatic effect both for first positive curvature (and for first negative curvature) of oat coleoptiles and demonstrated in addition that red light had the opposite effect on second positive curvature: it increased its sensitivity by a factor of 3. Chon and Briggs (1966) reported similar results with maize coleoptiles. Chon and Briggs (1966) also demonstrated that the maize response to red light was fully far-red reversible and appeared to be a classic phytochrome response.

There is a problem with a simple interpretation of the results based on phytochrome. Quantitative experiments with maize coleoptiles led to a surprising finding: Briggs and Chon (1966) measured fluence-response relationships for the red light effect on first positive phototropism and compared it with those relationships for phytochrome transformation in vivo for maize coleoptiles. Surprisingly, phototropism was altered by fluences of red light 3 orders of magnitude too low to cause measureable phototransformation of phytochrome ( Fig. 3 ). This discrepancy parallels the paradox in phototropism: blue light induces phototropic curvature at fluences far below those that induce detectable phototropin phosphorylation either in vitro or in vivo (see above). This result is all the more paradoxical in that the red light effect on phototropism is fully far-red reversible if the far-red light exposures are sufficiently short. (Longer far-red exposures themselves caused the same shift in phototropic sensitivity that red exposures did.) These highly sensitive responses were later designated “very low fluence” responses (see Mandoli and Briggs, 1981 , who used slightly different terminology). This apparent paradox is also currently unresolved.

Fluence-response curve for the phototropic curvature of maize coleoptiles (left) and for phytochrome phototransformation in vivo (right). From Briggs and Chon (1966) .

The situation in Arabidopsis is somewhat different. Red light actually sensitizes both first and second positive curvature. Janoudi and Poff (1991) first showed that red light treatment enhanced phototropic curvature in the first positive range, subsequently confirmed and shown to be mediated by phyA ( Hennig, 1996 ; Parks et al., 1996 ). Janoudi et al. (1992) showed that red light pretreatment actually shortened the lag period between the start of blue light irradiation and the onset of curvature, again an enhancement. Whippo and Hangarter (2004) demonstrated that the role of phytochromes was more complex and that phyB and phyD could also mediate the sensitization of Arabidopsis phototropism to higher blue light fluences (for further details, see Han et al., 2008 ). To date, there is no evidence for opposite effects of red light on first and second positive curvature in Arabidopsis.

Another effect of red light on etiolated coleoptiles might be related to red light-induced changes in phototropic sensitivity. Briggs (1963a) found that continuous red light treatment of etiolated maize coleoptiles reduced the amount of diffusible auxin that could be collected in agar blocks to roughly one-half of that from dark controls. The decrease was gradual, reaching a stable lower level after about 2 h. During a dark period after a 2-h red light pretreatment, the diffusible auxin yield gradually returned to the dark level, again over a recovery period of about 2 h. The time courses for these auxin changes were essentially parallel to the red light-induced decrease in phototropic sensitivity (2 h) and its subsequent recovery in the dark (2 h).

More recently, studies with phot1 tagged with GFP provided one possible mechanism for the red light-induced increase in phototropic sensitivity found in etiolated Arabidopsis hypocotyls. Sakamoto and Briggs (2002) first noted that blue light induced the movement of phot1-GFP from the plasma membrane into the cytoplasm, a response explored in detail by Wan et al. (2008) . The response required 10 to 15 min to go to completion. Subsequently, Kong et al. (2006) reported a similar movement of phot2-GFP from the plasma membrane in Arabidopsis hypocotyl cells. Han et al. (2008) then found that red light given prior to phototropic induction almost completely eliminated the blue light-induced movement of phot1. The photoreceptor remained closely associated with the plasma membrane. Given that lateral auxin transport is certain to be associated with plasma membrane proteins, retention of a blue light receptor following red light treatment could well account for the observed sensitization of phototropism in Arabidopsis. Interestingly, this red light effect could only be observed in the actively growing region of the hypocotyls.

While the above mechanism may be valid for the red light-induced sensitization observed for Arabidopsis, it can hardly be the whole story. First, red light dramatically desensitizes coleoptiles in the first positive curvature range, rather than sensitizing them. Second, while first positive curvature loses sensitivity, second positive curvature gains it. Third, the threshold for this red light effect in coleoptiles is far below that reported by Han et al. (2008) for inducing the changes in phot1 subcellular relocalization in Arabidopsis ( Briggs and Chon, 1966 ). Thus, the proposed mechanism, retention of phototropin at the plasma membrane, is clearly not the whole story. For the third time, an apparent discrepancy between physiology and photochemistry remains unresolved.

Newman and Briggs (1972) reported that red light treatment increased the electrical potential between the top 1 cm of etiolated oat coleoptiles by about 6 mV (with respect to a reference electrode in a 10 m m KCl solution containing the roots). The increase began about 10 s after the onset of red light and recovered to the dark level after about 6 min ( Fig. 4 ). At that time, a pulse of far-red light led after about 15 s to a decrease in potential of about 10 mV followed by dark recovery over several minutes. A second red light pulse had no effect if there had not been an intervening far-red light pulse. These electrophysiological changes are clearly phytochrome mediated and indicate some sort of rapid action at the plasma membrane. Haupt (1959 , 1960 ) some years earlier had done his classic experiments with the alga genus Mougeotia , demonstrating red/far-red-reversible effects on chloroplast movement that could only be explained by parallel-oriented phytochrome molecules in close proximity to the cell surface. Most recently, Jaedicke et al. (2012) have demonstrated an association of phytochrome with phototropin at the plasma membrane in protonemata of the moss Physcomitrella patens . They also used a split yellow fluorescent protein assay to demonstrate an association of Arabidopsis phytochrome with Arabidopsis phototropin when they were both injected into onion ( Allium cepa ) epidermal cells, although they failed to obtain evidence for such an association in a yeast two-hybrid test. Hughes (2013) has recently written a comprehensive review on cytoplasmic signaling mediated by phytochrome, covering the early history as well as recent developments. Work on the phytochromes and their signal transduction pathways has in recent years focused overwhelmingly on their effects on transcription ( Franklin and Quail, 2010 ; Quail, 2010 ; Leiver and Quail, 2011 ; Zhong et al., 2012 ). It is timely that attention is being returned to possible roles of phytochromes at the plasma membrane.

Red (R)/far-red (FR)-reversible changes in potential (mV) between the top 1 cm of an oat coleoptile and a reference electrode in a 10 m m solution around the roots. After Newman and Briggs (1972) .

In 2006, Lariguet et al. (2006) reported an important finding: the Arabidopsis PHYTOCHROME KINASE SUBSTRATE1 (PKS1) protein, strongly induced by blue light but phyA dependent, interacts both in vivo and in vitro with phot1 and NONPHOTOTROPIC HYPOCOTYL3 (NPH3). Like phot1 and NPH3, PKS1 is plasma membrane localized. PKS1 also was shown to regulate root phototropism and root gravitropism ( Boccalandro et al., 2008 ). A second family member, PKS2, was observed to regulate both leaf flattening and leaf positioning, two phototropin-dependent responses ( de Carbonnel et al., 2010 ). Finally, Kami et al. (2012) showed that some nuclear signaling involving phyA is needed for a maximal phototropic response. Thus, the two PKS proteins may well provide the missing link between phytochrome and phot1, a link that strongly impacts phototropism.

We are still left with the large discrepancy between physiology and photochemistry, regardless of mechanism. However, it is possible that the discrepancies observed between the photosensitivity of phytochrome phototransformation and both phototropic sensitivity changes and phototropin phosphorylation could be explained by some trigger mechanism at the plasma membrane, an amplification mechanism somehow already charged. This mechanism could be fired when only a very few photoreceptor molecules are activated. Such a mechanism might be analogous to the visual system where a very few photons are sufficient to activate signaling in a dark-adapted mammalian eye ( Pelli, 1990 ).

Frits Went (1928) originally proposed that the phototropism of coleoptiles was mediated by light-induced lateral transport of auxin, a conclusion based on measurements of diffusible auxin from irradiated and shaded sides of coleoptile tips. Because the total auxin recovered was less than that from dark controls, however, differential inactivation of auxin, higher on the irradiated side than on the shaded side, was not eliminated as a potential mechanism leading to curvature. The auxin mechanism in coleoptiles remained controversial until Briggs et al. (1957) demonstrated that an impermeable barrier (a coverslip) placed between shaded and irradiated halves of split maize coleoptile tips eliminated any auxin differential without affecting overall auxin yield, confirming Went’s result and conclusion. Briggs (1963b) and Pickard and Thimann (1964) , who used radiolabeled auxin, confirmed and extended these observations.

Several somewhat more recent studies have demonstrated that the growth differential between irradiated and shaded sides of phototropically curving organs is compensatory: a decrease in growth rate on the irradiated side is matched by an increase in growth rate on the shaded side. Iino and Briggs (1984) documented this response in maize coleoptiles, and Baskin et al. (1985) further resolved it with high-resolution time-course measurements of coleoptiles as curvature developed. Baskin (1986) then demonstrated a similar compensatory growth differential in phototropically stimulated epicotyls of pea ( Pisum sativum ). All three of these studies are consistent with a model that involves lateral transport of auxin without any net loss or gain of the hormone itself during the response.

As is well known, Darwin (1881) first demonstrated the importance of the grass coleoptile tip in perceiving the phototropic light stimulus. The coleoptile tip itself had to be irradiated in order for curvature of the lower regions of the coleoptile to develop curvature. Sierp and Seybold (1926) and Lange (1927) narrowed the photosensitive region to a fraction of 1 mm of the extreme coleoptile tip. Boysen-Jensen (1928) then demonstrated that physical contact between the illuminated and shaded sides of the oat coleoptile was also essential in order to obtain phototropic curvature. When he slit the coleoptile tip and inserted a piece of foil (opaque) or a chip of glass (transparent) into the slit prior to unilateral illumination at right angles to the slit, curvature development was blocked. If the slit was parallel to the direction of light, curvature developed even with the insertion of the barrier. Finally, if he split the tip and pushed the two halves back together without any barrier, he obtained curvature. Briggs (1963b) repeated the slit-tip experiment with maize coleoptiles using a glass barrier and obtained a similar result. When the barrier was oriented at right angles to the incident light, second positive curvature was significantly reduced and first positive curvature was completely eliminated. Briggs (1963b) then showed that with only 0.5 mm of 5-mm coleoptile tips intact, unilateral light still induced as great a differential in diffusible auxin between illuminated and shaded sides of 5-mm coleoptiles tips as when the apical 4 mm of the 5-mm coleoptile tips was intact. More recently, Palmer et al. (1993) showed that the apical 1 mm of maize coleoptiles showed the highest level of light-activated phosphorylation of what was subsequently identified as phot1.

All of these results indicate for phototropism (1) that photoperception in the coleoptile apex is essential, (2) that cell-cell lateral communication between lighted and shaded sides is essential, and (3) that a phototropin is likely the photoreceptor. These three conclusions appear to be unambiguous. Unfortunately, the large discrepancy between the fluence for threshold phototropism and the fluence for threshold blue light-driven phototropin phosphorylation casts something of a pall over the “unambiguous” conclusion implicating a phototropin in coleoptiles.

The growth measurements ( Baskin, 1986 ) demonstrating compensatory growth on irradiated and shaded sides of pea epicotyls clearly established that lateral transport of auxin could be functioning in dicots as well as monocots. In addition, as mentioned above, Esmon et al. (2006) demonstrated a difference in auxin-activated transcription between irradiated and shaded sides of B. oleracea hypocotyls. In the past decade, a great deal of information has accumulated about the several proteins involved in auxin transport ( Sakai and Haga, 2012 ; Christie and Murphy, 2013 ). However, an unanswered question remained: is the site of perception of the light signal in the responding tissue itself or, as in coleoptiles, is it perceived in the upper nonelongating tissues and transported basipitally, as in the case of coleoptiles? Christie et al. (2011) used dark-adapted deetiolated Arabidopsis carrying the DR5rev:GFP reporter protein, a system that responds visually to auxin, to address this question. They found that unilateral blue light induces, first, an inhibition of the flow of auxin from the cotyledons into the vascular tissue and epidermis below, accompanied by an inhibition of growth. Lateral displacement of auxin into the shaded epidermis above the elongation zone followed, and the auxin differential generated between epidermis on irradiated and shaded sides moved down into the elongation zone, accompanied by the development of curvature. Although blue light-induced inhibition of the auxin efflux transporter ABCB19 accounted for the initial growth inhibition, which auxin transporter(s) are involved in the actual lateral transport is not currently known. However, the model developed over a century ago by Darwin for coleoptiles is evidently also valid for Arabidopsis and likely for other dicots: light perception above the growing tissue and generation by lateral transport of an auxin gradient that moves down into the growing tissue.

At the beginning of the 19th century, Sebastiani Poggioli (1817) first asked what color of light was responsible for inducing plant movements. He noted that the leaves of Mimosa pudica favored violet light for inducing a change in leaf orientation to place the lamina at right angles to the light source (heliotropism or solar tracking), likely the first hint that there might be a specialized photoreceptor that required “violet” light for its activation and downstream signaling. Some years later, Payer (1842) demonstrated that true phototropism of watercress ( Nasturtium officinale ) seedlings was also maximally sensitive in the blue region of the spectrum. Other workers followed with more detailed studies ( Briggs, 2006 ), but it took until the middle of the 20th century for Shropshire and Withrow (1958) and Thimann and Curry (1960) to publish the first definitive action spectra for first positive curvature of oat coleoptile, covering the wavelength range 330 to 550 nm. Everett and Thimann (1968) then produced an action spectrum for second positive curvature that covered activity over the same wavelength range.

In subsequent years, action spectra for phenomena activated by blue light proliferated, with spectra for responses as diverse as phototropism in the two fungi Phycomyces blakesleeanus and Pilobulus kleinii , phototaxis in Euglena gracilis , stimulation of carotenoid synthesis by the fungi Neurospora crassa and Fusarium aqueductuum , chloroplast rearrangement in the moss Funaria hygrometrica , suppression of a circadian rhythm of conidiation in N. crassa ( Sargent and Briggs, 1967 ), and several other phenomena ( Presti and Delbrück, 1978 ). The general features of all of these action spectra were similar: a single broad band of activity in the UV-A near 360 nm, a more complex band in the blue with a maximum near 450 nm, and fine structure indicative of different vibrational modes of the photoreceptor.

Baskin and Iino (1987) , using the Okazaki Large Spectrograph, produced with alfalfa ( Medicago sativa ) seedlings what remains technically the best action spectrum by far for first positive phototropism. It extends from 530 nm well into the UV-B region of the spectrum (down to 260 nm) and documented for the first time a peak of activity around 280 to 290 nm, about one-third as high as the 450-nm maximum. Their action spectrum coincided almost exactly with that obtained by Thimann and Curry (1960) for oat coleoptiles over the entire wavelength range covered by both studies.

Conventional wisdom for many decades was that there was a single blue light receptor common to all of these responses. The overriding controversy was whether the chromophore was a carotene, a flavin, or something entirely different. It was only in 1993 that the first blue light receptor was identified, cry1 in Arabidopsis ( Ahmad and Cashmore, 1993 ). Lin et al. (1995) soon identified a second cryptochrome (cry2). The cryptochromes are structurally related to DNA photolyases, two-chromophore proteins involved in DNA repair and binding both a flavin and either a pterin (methenyltetrahydrofolate) or a deazaflavin as chromophores ( Sancar, 2003 ). Cryptochromes were found to bind a flavin and most likely methenyltetrahydrofolate as the second chromophore ( Lin et al., 1995 ; Malhotra et al., 1995 ), an initial win for flavins.

After the discovery of the cryptochromes, identification of the photoreceptor chromophore for phototropism remained controversial. Quiñlones and Zeiger (1994) proposed that the carotinoid zeaxanthin, an important component of the photoprotective xanthophyll cycle for photosynthesis, might be the functioning chromophore for phototropism in maize coleoptiles. However, Palmer et al. (1996) found that the coleoptiles of maize seedlings grown on the inhibitor of carotenoid biosynthesis norflurazon showed normal phototropism in the absence of any detectable carotenoids. Ahmad et al. (1998) then presented evidence that cryptochromes themselves might be carrying out the photoreceptor function for phototropism. Lascève et al. (1999) then investigated the stomatal opening responses to both blue light and phototropism in Arabidopsis mutants in cryptochromes ( cry1 , cry2 , and a cry1 cry2 double mutant), a blocked xanthophyll cycle mutant ( npq1 ), and the recently discovered phot1 mutants nph1 , nph3 , and nph4 ( Liscum and Briggs, 1995 , 1996 ). As only the nph mutants suppressed first positive phototropism in response to blue light ( Liscum and Briggs, 1996 ; Lascève et al., 1999 ), the authors ruled out members of the xanthophyll cycle and both cryptochromes for phototropism.

Lascève et al. (1999) also eliminated phot1 as mediating stomatal opening because the phot1 ( nph1 ) mutants showed significant stomatal opening in the absence of a phototropic response. Thus, they concluded that there must be a minimum of four different blue light receptors in this model species: two cryptochromes, phot1, and an unknown photoreceptor that functioned for stomatal opening but not phototropism. The source of this error is now obvious. The less sensitive phot2 ( Jarillo et al., 1998 ; Kagawa et al., 2001 ) had not been identified at the time. Lascève et al. (1999) had used a fluence rate in the stomatal studies that was high enough to activate phot2, whereas the fluence they used for the phototropic studies was much too low to activate phot2 ( Sakai et al., 2001 ). Hence, they missed phot2’s contribution to phototropism but detected it for stomatal opening. Thus, the fourth blue light receptor has turned out to be another phototropin, phot2, and not a completely different molecule.

Currently unanswered is what the photoreceptor is for the UV-B peak described by Baskin and Iino (1987) . It could be the consequence of photoexcitation of the UV-B-absorbing peak of the flavin chromophore of one or both phototropins or of one or more aromatic residues in a currently unknown photoreceptor protein. It could also be the consequence of the photoexcitation of UVR8, a recently described UV-B photoreceptor in Arabidopsis ( Rizzini et al., 2011 ). Time will tell.

Finally, there have been two reports of phytochrome-mediated phototropism. Iino et al. (1984) reported very weak phototropic curvatures of maize mesocotyls. It could be significantly enhanced by placing the seedlings horizontally on a clinostat to eliminate curvature elicited by gravitropism. Red light from above prior to unilateral red light completely eliminated the phototropic response, leading the authors to conclude that the photoreceptor was a phytochrome. Likewise, Parker et al. (1989) observed a weak phototropic response to unilateral red light from etiolated pea epicotyls that had developed in complete darkness. They reported a sharp decrease in overall growth rate about 15 min after the onset of red light and hypothesized that the curvature was the consequence of differential growth inhibition across the mesocotyl. Red light from above also eliminated the response, leading the authors to the same conclusion. It appears that a phytochromobilin chromophore functions for a photoreceptor for phototropism, although phototropism is hardly its major assignment.

Identification of the phototropins finally became feasible with the use of Arabidopsis mutants that were deficient in phototropism ( Khurana and Poff, 1989 ). Reymond et al. (1992) found that one of the mutants of Khurana and Poff (1989) , JK224, was severely impaired in its light-inducible phosphorylation. Liscum and Briggs (1995) then isolated a phototropism mutant designated nph1 that failed to respond to unilateral light in the first positive curvature range and lacked the light-activated phosphorylation reaction. Huala et al. (1997) then used this mutant to identify and sequence the gene encoding the protein that was the substrate for light-induced phosphorylation of a membrane protein. It contained two domains about 100 amino acids long with very similar amino acid sequences, which they designated LOV domains (as they were similar to domains in other proteins that were sensitive to light, oxygen, or voltage). Downstream was a protein kinase domain, a member of the AGC-VIIIb protein kinase subfamily ( Bögre et al., 2003 ). A year later, Christie et al. (1998) expressed the gene in insect cells and demonstrated (1) that it bound a flavin and (2) that light activated its phosphorylation in the absence of any other plant proteins. These authors thus concluded that it was a photoreceptor for phototropism. Christie et al. (1999) then demonstrated that the LOV domains were both binding sites for FMN. It was not long before a second phototropin, phot2, was identified ( Jarillo et al., 1998 ; Kagawa et al., 2001 ).

As we now know (see below), there is a third family of blue light receptors in Arabidopsis, the Zeitlupe family (ZTL [ Somers et al., 2000 ], LKP2 [ Schultz et al., 2001 ], and FKF1 [ Nelson et al., 2000 ]). Rather than playing a role in phototropism, they are involved in modulating circadian rhythms and flowering through posttranslational regulation ( Fujiwara, 2008 ). These proteins are all F-box proteins that use the same unique LOV domain photochemistry now elucidated for the phototropins and many bacterial blue light receptors ( Losi and Gärtner, 2012 ). As both cryptochromes, both phototropins, and all three F-box proteins use a flavin as chromophore, the long, drawn-out carotenoid versus flavin controversy has been settled unanimously in favor of flavins. Furthermore, a putative single blue light receptor has now disintegrated into seven demonstrable blue light receptors: two cryptochromes (possibly a third), two phototropins, and three F-box proteins.

There is a surprising disconnect between the elements identified for one phototropin-activated signal transduction pathway and another. For example, the protein phosphatase PP2A A1 is required to dephosphorylate (and hence deactivate) phot2 but evidently plays no role in the dephosphorylation of phot1 ( Tseng and Briggs, 2010 ). The 14-3-3 λ protein isoform is required for optimal stomatal opening mediated by phot2 but has no effect on stomatal opening mediated by phot1. Furthermore, a mutation at the 14-3-3 λ site fails to affect phot2-mediated phototropism, leaf flattening, or chloroplast movement ( Tseng et al., 2012 ). Only phot1 mediates the rapid inhibition of stem growth of etiolated seedlings ( Folta and Spalding, 2001 ). Both the chloroplast-avoidance response and nuclear positioning are regulated only by phot2 ( Demarsy and Fankhauser, 2009 ). Thus, although many responses can be activated by either phototropin, perhaps with different sensitivities, many others depend exclusively on only one of the two photoreceptors. Furthermore, even for a single phototropin, signal transduction pathways for different responses must actually differ at the level of the photoreceptor. A phototropin-interacting protein required for one response is completely dispensable for another response. For discussion of these and several other examples, see Demarsy and Fankhauser (2009) .

Purified LOV domains have provided a rich new source of material for investigating chromophore structure and photophysics. Salomon et al. (2000) demonstrated that they carried out a unique photoreaction: the formation of a covalent bond between a highly conserved Cys and the C-4a carbon of the FMN to form a cysteinyl adduct. Swartz et al. (2001) first reported that the LOV domain photocycle involved the formation of a flavin triplet intermediate prior to cysteinyl adduct formation. Swartz et al. (2002) also reported protein and chromophore structural changes induced by light using Fourier-transform infrared spectroscopy. Corchnoy et al. (2003) showed next that LOV domain photoactivation led to about a 30% decrease in α-helicity, based on circular dichroism measurements. Harper et al. (2003) then showed that adduct formation led to an unfolding of an amphipathic α-helix just C terminal from the downstream LOV domain, likely the step necessary to activate the C-terminal kinase domain (likely accounting for the α-helicity loss reported by Corchnoy et al. [2003] ). A number of LOV domain structures have now been solved by x-ray crystallography. Readers should consult the reviews by Möglich et al. (2010) and Losi and Gärtner (2011 , 2012 ) for a summary of progress in this active area.

Although incredible progress has been made in the past two decades in understanding plant blue light receptors and the processes they regulate, there remain a few puzzles that have stubbornly resisted solving to date or have been almost totally ignored. The huge discrepancy between the amount of light that activates a particular physiological response and the amount that it takes to activate the responsible photoreceptor is still unexplained. Indeed, even when a great deal is known about the activation and relaxation of a photoreceptor, be it a phototropin or a phytochrome, the discrepancy persists unexplained. Is there a specialized trigger mechanism? (The phytochrome community is actually worse off than the phototropin community. Their discrepancy has the physiology and photochemistry separated by about 3 orders of magnitude, whereas the phototropin community must only cope with a discrepancy of somewhere between 1 and 2 orders of magnitude.) How is phototropin specificity regulated? What determines why a given response is mediated by phot1 alone, phot2 alone, or both phototropins? What determines whether a protein plays a role in one signaling pathway but not another? Do different sites or patterns of phototropin phosphorylation play a role? Are there other posttranslational modifications that lend specificity? How does unilateral light really activate the lateral transport of auxin? What auxin transporters are involved? These fascinating questions should keep inquisitive plant biologists busy for a long time.

Since the original discovery of flavin-binding LOV domains in phototropins ( Christie et al., 1999 ) and of their unique photochemistry, light-activated formation of a flavin-cysteinyl adduct ( Salomon et al., 2000 ), putative LOV domains have been identified in proteins not only from fungi ( Idnurm et al., 2010 ) but in proteins from over 10% of all bacteria thus far sequenced ( Losi and Gärtner, 2012 ; Pathak et al., 2012 ). The first functional fungal photoreceptor to be characterized was White collar1 (Wc1) from N. crassa ( Froehlich et al., 2002 ), and homologs of Wc1 are now known from all major groups of fungi ( Idnurm et al., 2010 ), including P. blakesleeanus ( Idnurm et al., 2006 ), the sporangiophores of which were the subject of decades of phototropism research. Wc1 binds the promoters and regulates the transcription of a number of light-regulated genes in a blue light-dependent fashion.

The first bacterial protein reported to have a LOV domain was a LOV -STAS protein, YtvA, from Bacillus subtilis ( Losi et al., 2002 ). Putative LOV domains are found upstream from a large number of His kinases ( LOV -HK), the commonest LOV proteins, cyclic-di-GMP domains (GGDEF; EAL domains), STAS domains, DNA-binding domains, and phosphatase domains. There are also many short LOV proteins with no known function ( Krauss et al., 2009 ). Recent metagenome-based screening, largely from the Sargasso Sea but also from the open ocean, resulted in the assignment of 578 putative LOV domains on the basis of a highly conserved core region, a minimum of 14 amino acids thought to be essential for photoactivity, and a minimal length of 80 amino acids ( Pathak et al., 2012 ).

There is a vast reservoir of proteins harboring LOV domains in nonphotosynthetic as well as photosynthetic bacteria. (In addition to proteins containing LOV domains, there are many that contain putative phytochromes or BLUF [for blue light sensing using FAD] domain proteins. Indeed, some bacteria carry two different types of putative photoreceptors and some even carry three [ Gomelsky and Hoff, 2011 ].) Whenever it has been possible to express either the LOV domain itself or the entire LOV protein, they all show normal LOV domain photochemistry: cysteinyl adduct formation on photoexcitation. However, a major question remains: what are the functions of these many putative LOV domain photoreceptors? Finding a phenotype has been a challenging task. However, in a number of recent cases, the efforts have been successful. Light activation of a LOV domain HK in the animal pathogen Brucella abortus increases its virulence 10-fold in a macrophage assay ( Swartz et al., 2007 ). Light induces the activity of a cyclic di-GMP phosphodiesterase activity in the cyanobacterium Synechococcus elongatus ( Cao et al., 2010 ). Light activates a general stress response through the LOV -STAS protein YtvA in B. subtilis ( Avila-Pérez et al., 2006 ). A LOV -HK mediates host colonization by the plant pathogen Xanthomonas axonopodis pv citri ( Kraiselburd et al., 2012 ). Likewise, a LOV -HK enzyme mediates light-activated cell attachment for Caulobacter crescentum ( Purcell et al., 2007 ). A LOV -HK mediates exopolysaccharade production, attachment, and nodulation in Rhizobium leguminosarum ( Bonomi et al., 2012 ). Light plays an important role in regulating swarming motility in Pseudomonas syringae through a LOV -HK, a response that also involves a bacterial phytochrome ( Wu et al., 2013 ). Finally a LOV -STAS protein confers light-dependent transcription, swimming motility, and invasiveness to the animal pathogen Listeria monocytogenes ( Ondrusch and Kreft, 2011 ). This list will no doubt increase.

While information on the signal transduction pathways that these LOV proteins activate is still scant, it is clear that there is a whole rich world of bacterial photophysiology wide open for investigation. Thus, basic research on plant photoreceptors not only still poses tantalizing questions about plant photoreceptors themselves but has uncovered an exciting new field for microbiologists.

I thank Drs. Tong-Seung Tseng and Rajnish Khanna for their careful review of the manuscript and Dr. Tseng for help in scanning and improving the quality of published figures. I also thank Michael R. Blatt for providing the motive farce for this article.

light, oxygen, or voltage

meter-candle second

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Phototropism: Mechanism and Outcomes

Ullas v. pedmale.

a Division of Biological Sciences and Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211

R. Brandon Celaya

c Department of Molecular, Cellular and Developmental Biology, University of California — Los Angeles, 3206 Life Science Bldg, 621 Charles E Young Dr, Los Angeles, CA 90095

Emmanuel Liscum

Plants have evolved a wide variety of responses that allow them to adapt to the variable environmental conditions in which they find themselves growing. One such response is the phototropic response - the bending of a plant organ toward (stems and leaves) or away from (roots) a directional blue light source. Phototropism is one of several photoresponses of plants that afford mechanisms to alter their growth and development to changes in light intensity, quality and direction. Over recent decades much has been learned about the genetic, molecular and cell biological components involved in sensing and responding to phototropic stimuli. Many of these advances have been made through the utilization of Arabidopsis as a model for phototropic studies. Here we discuss such advances, as well as studies in other plant species where appropriate to the discussion of work in Arabidopsis.

INTRODUCTION

Light, apart from being an essential source of energy for plants, also provides a multitude of cues for proper growth and development. Phototropism, or the directional curvature of organs in response to lateral differences in light intensity and/or quality, represents one of the most rapid and visually obvious of these responses ( Darwin, 1880 ; Sachs, 1887 ; lino, 1990 ). Although a number of plant organs appear to be responsive to phototropic stimuli ( lino, 1990 ; Koller, 1990 ), a vast majority of the experimental data related to phototropism deals with the responses observed in seedling stems and primary roots. In particular, stems have been shown to exhibit positive phototropism, or curvature towards the light ( Figure 1 ), while roots show negative phototropism, or curvature away from the light. Stem phototropism is thought to provide plants with an effective means for increasing foraging potential (maximizing photosynthetic light capture) and is therefore likely to have appreciable adaptive significance ( lino, 1990 ; Stowe-Evans et al., 2001 ). Less is known about the phototropic response of roots, yet it is clear that cooperative interaction between a negative phototropic response and a positive gravitropic response could help to ensure proper growth of the root into the soil where water and nutrients are most abundant and available for absorption ( Galen et al., 2004 ; Galen et al., 2007b ). The adaptive advantage provided by stem and root phototropic responses may be particularly important during the early stages of growth and establishment of seedlings ( lino, 1990 ; Galen et al., 2004 ; Galen et al., 2007b ) and during gap filling situations in dense canopy conditions ( Ballare, 1999 ).

Phototropism in Arabidopsis induced by low fluence rate blue light. Photographs show 3-d-old etiolated seedlings 0 (A) , 100 (B) , 200 (C) , and 300 min (D) after the blue light was turned on. Incident light (coming from the left at a fluence rate of 0.002 µmol m -2 s -1 ) was obtained from one blue light emitting diode (λ max = 440 nm, 30 nm half-band). Note that the slight backwards bend in the upper hypocotyls region is an artifact that results from the seedlings being grown along an agar surface such that the cotyledons contain the positive phototropic response because they often lodge in the agar.

Phototropic responses are distinguished from other types of directional growth responses, such as nastic ( Satter and Galston, 1981 ; Forterre et al., 2005 ) and circadian-regulated ( McClung, 2001 ; Moshelion et al., 2002 ; Ueda and Nakamura, 2007 ) leaf movements, by two criteria. First, the direction of phototropic curvatures is determined by the direction of the light stimulus, while the directions of circadian-regulated movements are not ( Salisbury and Ross, 1992 ). Second, many leaf movement responses occur as a result of reversible swelling/shrinking of specialized motor, or pulvinar, cells ( Hart, 1988 ; Koller, 1990 ; Moran, 2007 ) whereas all stem and root phototropic responses are driven by changes in cell elongation rates across the bending organ. With respect to phototropic responses, unidirectional irradiation of seedlings with UV-A/blue light (BL) results in enhanced growth of the stem within the flank away from the light (“shaded side”) and generally represses growth in the flank facing the incident light (“lit side”) ( Baskin et al., 1985 ; Briggs and Baskin, 1988 ; Orbovic and Poff, 1993 ; Esmon et al., 2006 ), causing it to bend towards the light ( lino, 1990 ). An essentially opposite response is observed in roots, where growth is enhanced in the “lit side” and repressed in the “shaded side”, causing the root to bend away from the light ( Okada and Shimura, 1992 ; Kiss et al., 2002 ; Kiss et al., 2003b ). The differential growth rates driving the development of phototropic curvatures appear to be established as a result of differential accumulation of ( Went and Thimann, 1937 ), and subsequent responsiveness to, the plant hormone auxin ( Went and Thimann, 1937 ; lino, 1990 ; Liscum and Stowe-Evans, 2000 ; Esmon et al., 2006 ).

One feature shared between stem/root phototropic responses and nastic leaf movement responses is co-localization of photoperception and growth response, namely that the cells exhibiting the “growth response”, however mechanistically different, are the same ones perceiving the light signals ( Briggs, 1963b ; Koller, 1990 ). This is not necessarily the case with either circadian-dependent or true phototropic movements of leaves, where cells in the leaf blade perceive the signal, and pulvinar cells at the base of the leaf or petiole exhibit the growth response ( Schwartz and Koller, 1978 ; Engelmann and Johnsson, 1998 ; Moran, 2007 ). In nastic leaf movements the movements resulting from asymmetrical turgor pressure changes, also referred to as an “osmotic motor”, are driven by plasma membrane ATPase affecting KCl flux and thus water movement, into or out off the cells. Light, circadian and exogenous mechanical signals are known to feed into this osmotic motor to regulate leaf movements ( Moshelion et al., 2002 ; Moran, 2007 ).

“The Weed of Enlightenment”

The phototropic response has been utilized for over 100 years as a system for studying two basic cellular processes in plants - signal transduction and cell elongation. In the past couple of decades, significant leaps have been made in our understanding of the biochemical and molecular events mediating phototropism. Although not solely responsible for these advances, the utilization, since the mid 1980's, of Arabidopsis as a model organism for studies of phototropism has played an important role. In fact, it is fair to say that like many other aspects of plant biology, “we would not be where we are today without Arabidopsis.” This chapter will attempt to summarize these advances, with attention being given to both mechanism (e.g., the photoreceptor molecules and signal-response elements associated with various components of phototropic responses) and outcome (e.g., ecological and evolutionary significance of phototropism). While most of the discussion presented here will revolve around studies in Arabidopsis, reference will be made to studies in other organisms where contextually or historically important. For a more broad perspective on phototropism the reader is referred to a number of other sources ( Darwin, 1880 ; Sachs, 1887 ; Banbury, 1959 ; Thimann and Curry, 1961 ; Briggs, 1963b ; Firn and Digby, 1980 ; Dennison, 1984 ; Hart, 1988 ; lino, 1990 ; Firn, 1994 ; Whippo and Hangarter, 2006 ; Christie, 2007 ; Holland et al., 2009 ).

PERCEPTION OF DIRECTIONAL LIGHT CUES

Evidence for two distinct blue-light (bl) photoreceptors for phototropism: a historical perspective.

Most studies of higher plant phototropism, including those with Arabidopsis, have been done using etiolated (dark-grown) seedlings and low fluence rate (<0.5 µmol m -2 s -1 ) BL ( Dennison, 1984 ; Hart, 1988 ; lino, 1990 ; Galland, 1992 ; Firn, 1994 ). Although the total fluence (number of photons per unit area; e.g., µmol m -2 ) to which seedlings were exposed varied as much as six orders of magnitude from one experiment to the next, results from such studies suggested that a single photoreceptor mediates phototropic responsiveness under low fluence rate conditions ( Poff et al., 1994 ; Liscum and Stowe-Evans, 2000 ). This conclusion holds independent of whether pulses (seconds or fractions of seconds) or extended irradiations (minutes to a few hours) are used. While the function of a single receptor over such a broad fluence response range might seem unlikely, similar broad fluence-responsive properties have long been recognized for the red (RL)/far-red (FR) light-absorbing phytochromes (phys) ( Mancinelli, 1994 ).

In contrast to the single photoreceptor prediction from studies employing low fluence rate conditions, the function of at least two distinct photoreceptor molecules has been suggested for phototropic curvatures induced by high fluence rate BL ( Konjevic et al., 1989b ; Konjevic et al., 1989a ). In an elegant series of studies in Arabidopsis, Konjevic and colleagues ( Konjevic et al., 1989a ) obtained several pieces of physiological evidence in support of a two-receptor model. First, while irradiation with a single pulse of low fluence rate (e.g., 0.1 µmol m -2 s -1 ) BL (450 nm) led to a singlepeak biphasic fluence-response curve for phototropism ( Figure 2A ), use of higher fluence rate (e.g., 0.7 µmol m -2 s -1 ) BL resulted in a clear dual-peak response curve ( Figure 2B ). Second, this curious alteration in fluence responsiveness was also dependent upon wavelength. For example, irradiation with 490 nm light resulted in a single peak fluence-response curve with a distinct lower-fluence shoulder ( Figure 2C ), while use of 510 nm light gave rise to only a single peak curve with no shoulder ( Figure 2D ). Such wavelength-and fluence rate-dependent changes in fluence-responsiveness are not expected for the action of a single photoreceptor. Third, the second higher-fluence peak of the 450 nm fluence-response curve ( Figure 2B ) could be eliminated by a pre-irradiation with a saturating pulse of 510 nm light (25 µmol m -2 ), a unexpected phenomenon if a single receptor were responsible for both fluence-response peaks. Fourth, sequential irradiation with 510 and 450 nm light at a fluence and fluence rate that gives rise to maximal single-peak responses ( Figure 2A and D ), resulted in a phototropic response that was nearly additive. As discussed below the action of two photoreceptors in high fluence rate-induced phototropism has now been confirmed through molecular genetic studies in Arabidopsis, though all of the photophysiological properties described by Poff and colleagues have not been fully explained by the two identified receptors. While the genetic identification and basic biochemical properties of these photoreceptors will be addressed here, we refer the reader to other sources for more detailed discussion of these receptors and their roles in non-phototropic processes ( Christie and Briggs, 2001 ; Celaya and Liscum, 2005 ; Stone et al., 2005 ; Briggs, 2007 ; Christie, 2007 ).

Fluence rate and wavelength dependence of pulsed light-induced phototropism in Arabidopsis (adapted from (Konjevic et al., 1989)

(A) Phototropism induced by a single pulse of blue light (λ max = 450 nm, 10 nm half-band) at a “low” fluence rate (0.1 µmol m -2 s -1 ).

(B) Phototropism induced by a single pulse of blue light (λ max = 450 nm, 10 nm half-band) at a “high” fluence rate (0.7 µmol m -2 s -1 ).

(C) Phototropism induced by a single pulse of blue/green light (λ max = 490 nm, 10 nm half-band; at a fluence rate of 0.9 µmol m -2 s -1 ).

(D) Phototropism induced by a single pulse of green light (λ max = 510 nm, 10 nm half-band; at a fluence rate of 0.4 µmol m -2 s -1 ).

Phototropin 1 (phot1): A Broad Fluence Rate-Responsive Phototropic Receptor

The first significant progress towards the identification of an apoprotein for a low fluence rate phototropic receptor came in 1988 with a report of a BL-activated phosphorylation of a plasma membrane-localized protein in etiolated pea seedlings ( Gallagher et al., 1988 ). As discussed in a review by Short and Briggs ( Short and Briggs, 1994 ), the phosphorylation of a single plasma membrane protein (114 to 130 kDa, depending upon the species) appears to be a ubiquitous response of higher plants to BL irradiation. Many of the photophysiological properties of this light-dependent phosphorylation reaction, as determined in a number of species (most notably maize, oat, pea, and later Arabidopsis), suggested it was important for phototropic responses. For example, the phosphorylation reaction occurs in the most phototropically sensitive tissues, it is strongest in the tissue closest to the light and decreases in strength moving away from the lit side, it is fast enough to precede the development of curvature, its action spectrum matches that for phototropism, and it shows similar dark-recovery kinetics as phototropism after a saturating irradiation ( Short and Briggs, 1994 ; Briggs and Huala, 1999 ).

A genetic connection between the aforementioned phosphorylation reaction and phototropism came in 1992, when Reymond and colleagues ( Reymond et al., 1992b ) showed that a phototropic mutant of Arabidopsis, strain JK224 ( Khurana and Poff, 1989 ), exhibited little, if any, BL-induced phosphorylation. Strain JK224 was originally described as a mutant that exhibited a shift in its fluence threshold (10 to 30-fold higher) for pulse light-induced BL-dependent phototropism ( Khurana and Poff, 1989 ). It was subsequently proposed, based on responsiveness to BL and green light (GL) at low and high fluence rates, that strain JK224 contains a lesion in a photoreceptor ( Konjevic et al., 1992 ), in particular the low fluence rate receptor system described by Konjevic and colleagues ( Konjevic et al., 1989a ). Liscum and Briggs (Liscum and Briggs) demonstrated that null mutations in the NONPHOTOTROPIC HYPOCOTYL 1 ( NPH1 ) locus, of which the mutation in strain JK224 is an allele ( nph1–2 ), fail to show BL-dependent phosphorylation because they in fact lack the target protein. Hence, it was hypothesized that the NPH1 locus encodes the apoprotein for a phototropic receptor and that the observed BL-induced phosphorylation represents an autophosphorylation response ( Liscum and Briggs, 1995 ).

Cloning of the NPH1 gene ( Table 1 ) showed that the encoded protein is of the proper size (120 kD in Arabidopsis; ( Reymond et al., 1992a )) to be the substrate of the phosphorylation reaction ( Huala et al., 1997 ). The predicted NPH1 protein was also shown to contain the eleven signature domains of Ser/Thr protein kinases ( Figure 3 ), making autophosphorylation a formal possibility. On the other hand, nothing was found in the primary sequence that indicated an obvious inherent photoreceptor activity for NPH1. However, a repeated sequence motif within the amino-terminal portion of NPH1 was identified ( Figure 3 ) that exhibits homology to a subfamily of PAS domains that are found within sensor-proteins ( Huala et al., 1997 ; Zhulin et al., 1997 ; Taylor and Zhulin, 1999 ). Both of these PAS-like domains of NPH1, designated LOV1 and LOV2 (for their relationship to l ight, o xygen, and v oltage-regulated PAS domains), were subsequently shown to bind one FMN molecule ( Christie et al., 1998 ), a finding consistent with the hypotheses that NPH1 represents a BL-absorbing phototropic receptor ( Khurana and Poff, 1989 ; Konjevic et al., 1992 ; Liscum and Briggs, 1995 ). Soluble nph1 (NPH1 apoprotein with associated FMN cofactors; see Table 2 for nomenclature) isolated from a heterologous insect cell expression system was shown to exhibit BL-dependent autophosphorylation with kinetic, fluence-response, and action spectrum characteristics essentially like those obtained with native Arabidopsis nph1, and for phototropism itself ( Christie et al., 1998 ). Hence, in the absence of all other plant proteins nph1 can function as a photoreceptive molecule with the properties consistent with its function as a phototropic receptor in plants.

Genes shown to be definitively involved in phototropic signal perception, transduction, and response

Domain structures of the phot1 and phot2 receptors. The aminoterminal photosensory LOV domains are shown in blue with their associated FMN co-factor (above each LOV domain). The carboxyl-terminal protein kinase domain of each phot is shown in red.

phototropin nomenclature 1

As discussed above, genetic studies in Arabidopsis have demonstrated that nph1 is necessary for normal phototropic response to directional low fluence rate UV-A, BL, and GL, and it is presumed that the light-activation of nph1's kinase domain is critical to its signaling properties. Biochemical and structural studies suggest that the kinase domain of nph1 is activated in response to a light-dependent formation of a self-contained FMN- C(4a)-cysteinyl adduct ( Salomon et al., 2000 ; Crosson and Moffat, 2001 ). The nph1 holoprotein has been given the trivial name, phototropin 1 (phot1), in order to reflect its physiological and biochemical properties ( Christie et al., 1999 ; Briggs et al., 2001 ); see Tables 1 and ​ and2 2 ).

A second phototropin gene, PHOT2 (previously designated NPL1 , for NPH1-like ; see Tables 1 and ​ and2), 2 ), has been identified in the Arabidopsis genome ( Jarillo et al., 1998 ; Initiative, 2000), and the function of its encoded protein as a second phototropic receptor will be discussed in the following section.

Phototropin 2 (phot2): A Second High Fluence Rate Phototropic Receptor

As discussed earlier, pulse-irradiation experiments suggested that two photoreceptors are capable of modulating response to directional BL, in a fluence rate-dependent fashion ( Konjevic et al., 1989a ; Konjevic et al., 1992 ). Additional physiological and genetic support for this two-photoreceptor hypothesis came from studies of etiolated nph1 ( phot1 )-null mutants under long-term irradiation conditions ( Liscum and Stowe-Evans, 2000 ; Sakai et al., 2000 ). For example, Sakai and colleagues ( Sakai et al., 2000 ) found that while phot1-101 lacks hypocotyl and root phototropism at fluence rates < 1.0 µmol m -2 s -1 , it retains a phototropic response at fluence rates of BL above ∼1.0 µmol m -2 s -1 and is essentially like wild-type at 100 µmol m -2 s -1 . Similar results have been observed with the phot1–5 null mutant under greenhouse conditions (T. Campbell and E. Liscum, unpublished). Thus, while there is ample genetic, biochemical, and physiological evidence to conclude that phot1 is a phototropic receptor under low fluence rate (< 1.0 µmol m -2 s -1 ) conditions ( Liscum and Stowe-Evans, 2000 ), the aforementioned results clearly indicate that a second phototropic receptor functions under high fluence rate (1 µmol m -2 s -1 ) conditions ( Table 2 ).

The most obvious candidate for a second phototropic receptor apoprotein is the PHOT1 paralog PHOT2 ( Jarillo et al., 1998 ). Although PHOT2 is slightly smaller than PHOT1 (110 kD versus 124 kD), sequence and structural motifs are highly conserved. In particular, PHOT2, like PHOT1, contains a Ser/Thr protein kinase domain in its carboxyl terminal region and two LOV domains in its amino terminal half ( Jarillo et al., 1998 ); ( Figure 3 ). Moreover, the light-dependent autophosphorylation and photocycling properties of baculovirus/insect cell-expressed phot2 are similar to those of phot1 ( Sakai et al., 2001 ), suggesting that phot2 functions as a BL receptor by a mechanism analogous to that of phot1.

While no alterations in phototropic responsiveness have been observed in phot2 single mutants ( Sakai et al., 2000 ; Jarillo et al., 2001 ; Sakai et al., 2001 ), phot1phot2 double mutants fail to exhibit seedling phototropic responses at both low and high fluence rates ( Sakai et al., 2001 ). The fact that phot2 single mutants retain a phototropic response indistinguishable from wild-type under all fluence rates tested ( Jarillo et al., 2001 ; Sakai et al., 2001 ) while the phot1phot2 double mutant is essentially blind ( Sakai et al., 2001 ), demonstrates that phot1 functions to some extent under all fluence rate conditions. while phot2 has redundant function for phot1 specifically under high fluence rate conditions ( Table 3 ). If the phot1 and phot2 holoproteins have similar photochemical and biochemical properties, as cited above, how can we explain these overlapping yet distinct functions in the perception of phototropic stimuli?

Role of phototropins and associated signaling components in mediating responses in Arabidopsis

In a study by Aihara and coworkers ( Aihara et al., 2008 ), chimeric proteins were constructed between amino-terminal LOV domains and with the carboxy-terminal kinase domains of both phot1 and phot2 to understand the fluence rate-dependent sensitivities of these photoreceptors. Chimeric proteins containing the combination of phot1 LOV domains with the protein kinase domain of phot2 were as sensitive as phot1 indicating that fluence rate sensitivity of a phototropin resides in the amino-terminal photosensory LOV domains. Moreover, combination of LOV domains of phot2 with the protein kinase domain of phot1 was less sensitive, akin to phot2. However, both these chimeras were able to promote chloroplast avoidance response that is specific to phot2 suggesting that the fluence sensitivity is more complex for other phototropin-dependent responses ( Aihara et al., 2008 ).

Beyond the structural-functional divergences between phot1 and phot2, simple differences in expression patterns of the two genes/proteins likely also contribute to the conditional differences in functions of the two receptors. It is clear that steady-state levels of PHOT1 and PHOT2 mRNAs exhibit light-dependent differences ( Table 3 ). While the abundance of PHOT1 mRNA does appear to be under the control of the circadian oscillator — with highest levels being observed at midday ( Harmer et al., 2000 ), acute light-dependent regulation of PHOT1 expression has not been observed. In contrast, PHOT2 mRNA levels increase upon exposure to UV-A, BL, RL, or white light ( Jarillo et al., 2001 ; Sakai et al., 2001 ), apparently through the action of phyA ( Tepperman et al., 2001 ). Strikingly, a two-fold increase in PHOT2 steady-state message levels was observed at fluence rates of BL (∼10 µmol m -2 s -1 ) where the redundant function of phot2 is most obvious ( Sakai et al., 2001 ). Light-dependent increase in PHOT2 message level may, in addition to structural-functional differences between the two phototropin proteins, contribute to the high fluence rate-specific phototropic function of phot2. It is also worth noting that a more rapid dark-recovery time required by phot2, which is more than 10 times faster than that of phot1 ( Kasahara et al., 2002 ; Kagawa et al., 2004 ), has also been proposed as a contributor to the higher fluence-rate threshold for phot2 activity ( Sakai et al., 2001 ; Takemiya et al., 2005 ).

LOV Domain Functionality

Independent of exactly how different fluence rate dependencies for phot1 and phot2 responses arise, the protein kinase domain of phot2 alone has been found to be sufficient to trigger constitutive light-independent phot2 specific responses, such as stomatal opening and the chloroplast avoidance response ( Kong et al., 2007 ). This would prompt one to ask the question, what role do LOV photosensory domains play in photoperception? It has been demonstrated that the LOV2 domain regulates the protein kinase activity of phot2 in vitro ( Matsuoka and Tokutomi, 2005 ), and that LOV2 photoactivity is required for in vivo autophosphorylation of phot1 and subsequent phototropism in response to BL exposure ( Christie et al., 2002 ; Cho et al., 2007 ). Similarly, the LOV2 domain is sufficient to stimulate phot2 protein kinase activity for phototropism in Arabidopsis ( Cho et al., 2007 ) and for chloroplast movement in Adiantum ( Kagawa et al., 2004 ). LOV1 alone is unable to stimulate autophosphorylation of phot1 in response to BL, or to promote phototropism, suggesting that the LOV2 domain plays a major role in photoperception and subsequent activation of the protein kinase domain to promote phototropism ( Christie et al., 2002 ; Harper et al., 2003 ; Cho et al., 2007 ).

At this juncture, a precise role played by LOV1 domain is not entirely clear. While LOV1 undergoes an FMN-dependent photocycle like that of LOV2 ( Kasahara et al., 2002 ; Christie, 2007 ), it has been reported that LOV1 may promote dimerization of the phots. This proposal is based on studies of amino-terminal Avena sativa phot1 polypeptides expressed in E. coli and studied in solution via gel-chromatography ( Salomon et al., 2004 ). Xray crystallographic studies on the LOV1 domain of phot1 and phot2 also support the homo-dimerization thesis ( Nakasako et al., 2008 ). In this latter study the authors reported that homodimers were formed in crystal through face-to-face association of the beta-sheets of respective LOV1 domains. Surprisingly, the critical residues apparently mediating dimerization of LOV1 domains differ between phot1 and phot2 ( Nakasako et al., 2008 ). Although further studies are required to determine if full-length phototropins are capable of forming dimers in planta , a recent study demonstrated that a fully active version of phot1 can trans-phosphorylate a kinase-dead version of phot1 in planta, suggesting that homodimerization is likely ( Kaiserli et al., 2009 ). Heterodimerization between phot1 and phot2 also cannot be ruled out at this moment as phot2 is capable of cross-phosphorylating kinasedead phot1 mutant in vitro ( Cho et al., 2007 ).

Light-Dependent Intracellular Relocalization of phot1 and phot2: Receptor Desensitization, Foundation for Phototropic Signaling, or Both?

Although phot1 and phot2 holoproteins lack obvious plasma membrane targeting signals or post-translational lipid/fatty-acids modification signatures, both are associated with the plasma membrane, as observed in various plant species ( Christie et al., 1998 ; Sakamoto and Briggs, 2002 ; Knieb et al., 2004 ; Kong et al., 2006 ; Zienkiewicz et al., 2008 ). While the exact mechanism by which phototropins are associated with the plasma membrane remains unknown, ionic interactions are not likely the basis as extensive washing of microsomal membranes with high salt buffer fails to release phot1 into solution ( Knieb et al., 2004 ). Recent serial-deletion analyses in Arabidopsis have however demonstrated that the protein kinase domain of phot2 is sufficient for its plasma membrane localization ( Kong et al., 2006 ; Kong et al., 2007 ).

A study by Sakamoto and Briggs ( Sakamoto and Briggs, 2002 ) observed movement of a phot1-GFP fusion protein from plasma membrane into the cytosol upon BL irradiation. Consistent with these observations, appreciable amounts of phot1 protein have been detected by immunoblot analysis in soluble protein fractions prepared from in vivo BL irradiated Arabidopsis seedlings ( Sakamoto and Briggs, 2002 ; Knieb et al., 2004 ). Downregulation of phot1 protein levels were also observed after prolonged treatment with BL, in a fluence and time dependent manner ( Sakamoto and Briggs, 2002 ; Kong et al., 2006 ). It has been estimated that in etiolated mustard seedlings upon BL irradiation, cytoplasmic phot1 ([phot1] cyt ) constitutes approximately 20% of the total cellular phot1 ( Knieb et al., 2004 ). It is currently unknown whether [phot1] cyt is part of an endosomal vesicle or other sub-cellular component ( Sakamoto and Briggs, 2002 ; Wan et al., 2008 ). Treatment of seedlings with protein synthesis inhibitor cycloheximide fails to disrupt the production of [phot1] cyt , indicating that [phot1] cyt is derived de novo from the plasma membrane associated phot1 ( Wan et al., 2008 ). Moreover, it has recently been shown that phot1 movement from the plasma membrane apparently represents a clathrin-dependent endocytosis event ( Kaiserli et al., 2009 ). Though [phot1] cyt disappears gradually over time, it is presently unclear whether it cycles back to the plasma membrane or undergoes degradation.

Unexpectedly, upon BL treatment phot2 translocates from the plasma membrane to cytoplasmic vesicles which co-localize with a Golgi marker K.AM1/MUR3 in Arabidopsis ( Kong et al., 2006 ). In contrast to phot1, no phot2 was detected in soluble proteins extracts prepared from in vivo BL irradiated seedlings, nor did total phot2 protein levels change appreciably ( Kong et al., 2006 ). It is intriguing to note that in spite of having similar overlapping photosensory function in phototropism and other responses, phot1 and phot2 relocalize to apparently distinct cellular compartments in response to BL ( Kong et al., 2006 ; Kong et al., 2007 ).

What is the functional role of BL induced relocalization of phots? It has been hypothesized that relocalization of phots modulates their activity ( Kong et al., 2006 ; Wan et al., 2008 ). It is attractive to speculate that different sub-cellular localizations of a phot might elicit different responses. In this context it is worth noting that in guard cells, [phot1] cyt was not detected, indicating that phot1 movement does not occur in all cell types, and is not prerequisite for all responses ( Wan et al., 2008 ). In addition, Kong and colleagues ( Kong et al., 2006 ) have shown that phot2 is able to mediate chloroplast movement in cells treated with brefeldin A (BFA), an inhibitor of vesicular endomembrane recycling ( Nebenführ et al., 2002 ). This latter observation indicates that presumed vesicular trafficking of phot2 to Golgi is not required for chloroplast movement responses ( Kong et al., 2006 ). Yet, a potential signaling role of phots from internalized membrane vesicles should probably not be discounted offhand since such potential vesicle-based signaling mechanisms are not unknown in plants. For example, BRI1 (BRASSINOSTEROID INSENSITIVE 1), the brassinosteroid hormone receptor-like kinase ( Wang et al., 2006 ), localizes to both the plasma membrane and endosomes, and enhancement of brassinosteroid signaling is observed after treatment with BFA, suggesting that signaling occurs from endosomal-localized BRI1 ( Geldner et al., 2007 ).

If the active site of phot signaling were to be exclusively at the plasma membrane rather than some internalized compartment, what then is the role of phot relocalization from the plasma membrane to cytoplasmic locations? One obvious possibility is that such internalization could serve to attenuate signaling by removing the receptor from the site of action. Such a mechanism is not uncommon in mammals, where cell surface and plasma membrane-associated receptors are regularly internalized by various mechanisms to desensitize receptor activity ( Vieira et al., 1996 ; von Zastrow and Sorkin, 2007 ). Various receptor internalization pathways have been documented, and of them clathrin-dependent receptor endocytosis is by far the most well studied ( Holstein, 2002 ), making the findings of Kaiserli and colleagues that phot1 is apparently endocytosed in a clathrin-dependent fashion ( Kaiserli et al., 2009 ) particularly intriguing. Many receptors, upon binding their respective ligand, trigger their own internalization to modulate signaling ( Mellman, 1996 ). An example of such a mechanism in plants is the receptor-like kinase FLAGELLIN-SENSING 2 (FLS2). Upon binding of its ligand, flagellin or its derivative flg22 peptide, FLS2 undergoes ligand-mediated endocytosis ( Robatzek et al., 2006 ). It thus seems plausible that a phot, upon perceiving its ligand — BL, could induce its own internalization to reduce the number of signal-active receptors present on the plasma membrane, thus desensitizing the overall cellular responsiveness to light. It is intriguing to note phyA activation with RL can inhibit the BL-induced movement of phot1 from the plasma membrane ( Han et al., 2008 ). These results are consistent with phot1 functioning at the plasma membrane and internalization representing a desensitization process since RL absorbed by phyA is known to result in enhanced phototropic responsiveness ( Parks et al., 1996 ; Janoudi et al., 1997b ; Stowe-Evans et al., 2001 ; Whippo and Hangarter, 2004 ). The influences of phyA on the modulation of phototropism will be discussed in detail later.

Are There Additional Directional Light Sensors?

As discussed above and later, there is overwhelming evidence to conclude that phot1 and phot2 are phototropic receptors. However, in plants, twelve photoreceptors are known to exist in addition to phot1 and phot2 - five phys, three cryptochromes (crys), one chimeric phot/phy called neochrome ( Adiantum PHY3) and three ZEITLUPE/ADAGIO (ZTL/ADO) family members ( Briggs and Olney, 2001 ; Chen et al., 2004 ; Banerjee and Batschauer, 2005 ; Franklin et al., 2005 ; Lin and Todo, 2005 ; Wang, 2005 ; Christie, 2007 ). The ZTL/ADO proteins have been shown to participate in BL-dependent targeting of components of the circadian clock for ubiquitylation and proteasomal degradation ( Imaizumi et al., 2003 ; Banerjee and Batschauer, 2005 ; Briggs, 2007 ; Christie, 2007 ; Kim et al., 2007 ; Sawa et al., 2007 ). Three members of the ZTL/ADO family have been identified in Arabidopsis: ZTL/ADO ( Somers et al., 2000 ); FLAVIN-BINDING, KELCH REPEAT, F-BOX (FKF1) (FKF1; Nelson et al., 2000 ); and LOV KELCH REPEAT PROTEIN 2 (LKP2) (LKP2; Schultz et al., 2001 ). Each of the ZTL/ADO family members contains a single LOV domain that utilizes FMN as its BL-absorbing chromophore. Moreover, it appears that the photocycle of ZTL/ADO LOV domain-FMN interactions is conserved with that of the phots ( Imaizumi et al., 2003 ; Kim et al., 2007 ; Sawa et al., 2007 ). The wide selection of photoreceptors available to plants poses the question of whether any of these, apart from phot 1 and phot 2, function as primary receptors of directional BL cues? In etiolated seedlings the short answer to this question is apparently no. However, to be fair the potential role(s) of the phot-related ZTL/ADO proteins in phototropism has yet to be extensively examined.

Crys Appear Not to Function as Directional Sensors

In 1998, Ahmad and colleagues proposed that the cry BL receptors, cry1 and cry2 ( Batschauer, 1999 ; Briggs and Huala, 1999 ; Cashmore et al., 1999 ; Christie and Briggs, 2001 ), represent redundant primary phototropic receptors in etiolated Arabidopsis seedlings ( Ahmad et al., 1998b ). This conclusion was based upon the observations that while cry1 and cry2 single mutants (containing equivalent G to E substitutions within the FAD-binding domain) retained a normal phototropic response, the cry1cry2 double mutant lacked response, and cry1 and cry2 overexpressing lines were hypersensitive to unilateral BL. Moreover, it was suggested that cry1 and cry2 function upstream of phot1 in phototropic signaling since BL-dependent autophosphorylation of phot1 appeared impaired in the cry1cry2 double mutant.

A subsequent study by Lascève and colleagues ( Lascève et al., 1999 ) found that two independent cry1cry2 double mutant lines ( hy4-B104cry2-1 and cry1-304cry2-1 ) which lack detectable cry1 and cry2 proteins altogether ( Guo et al., 1998 ; Mockler et al., 1999 ) retained both BL-induced phototropism and phot1 autophosphorylation — in stark contrast to the results obtained for the substitution mutants in the study by Ahmad and colleagues ( Ahmad et al., 1998b ). Although a slight reduction in the magnitude of maximal pulse-induced phototropism was observed in the cry1cry2 double mutants, no change in the threshold or peak-response fluence dependencies was observed ( Lascève et al., 1999 ). In contrast, the phot1–2 mutant (originally designated strain JK224) retains a phototropic response of equal magnitude to wildtype, but exhibits a 20 to 30-fold shift in fluence responsiveness ( Khurana and Poff, 1989 ; Konjevic et al., 1992 ), as would be expected for a photoreceptor mutant that retains a response. Lascève and colleagues concluded that neither cry1 nor cry2 function as primary phototropic receptors, or as photoreceptors that mediate BL-induced phosphorylation of phot1. A subsequent study of phototropism in phot1, phot2, cry1 and cry2 , as single and multiple mutants, at fluence rates of BL ≤100 µmol m -2 s -1 , provided additional support for the conclusion that the only primary phototropic photoreceptors are the phototropins ( Ohgishi et al., 2004 ).

Based on results from a study employing a sensitive mathematical approach to measure phototropic curvatures from timelapse images of etiolated Arabidopsis seedlings exposed to unidirectional BL, Whippo and Hangarter proposed that proper phototropism represents a balance between the differential growth response induced by phot action and the hypocotyl growth inhibition response mediated by crys in a fluence rate-dependent fashion ( Whippo and Hangarter, 2003 ). Recently it has been reported that crys have a negative effect on the phot1 transcript and protein accumulation in light grown seedlings when compared with etiolated seedlings ( Kang et al., 2008 ), which could provide a more direct connection between the two pathways. While it is quite clear that crys do not act as primary phototropic receptors, future studies will be required to determine how much influence crys are having on phototropism via general effects (e.g., growth inhibition) versus those on phot signal-response more directly (e.g., modulation of phot1 protein levels).

Phys Appear to Sense Directional R/FR Cues and Contribute to Phototropism in De-etiolated But Not Etiolated Plants

Even before the molecular identification of the phots, the phytotochrome (phy) family of RL/FR receptors ( Casal, 2000 ; Fankhauser, 2001 ; Bae and Choi, 2008 ) had been proposed to function as mediators of phototropic responses in de-etiolated (light-grown) seedlings of a number of species ( Atkins, 1936 ; Shuttleworth and Black, 1977 ; Ballare et al., 1992 ). As one example, cucumber seedlings exhibit phyB-dependent negative phototropism in response to perception of FR reflected from canopy plants ( Ballare et al., 1992 ; Ballare et al., 1995 ). Pretreatment of etiolated seedlings with RL prior to phototropic stimulation with unilateral BL is known to modulate phototropic responsiveness ( Briggs, 1963a ; Chon and Briggs, 1966 ; Stowe-Evans et al., 2001 ). RL-induced enhancement of hypocotyl phototropism under low fluence rate BL conditions (0.01 µmol m -2 s -1 ) appears to be controlled primarily by phyA, whereas phyB and phyD redundantly influence phototropism at higher fluence rates of BL (e.g., 1.0 µmol m -2 s -1 ) ( Whippo and Hangarter, 2004 ). Interestingly, RL promotes positive phototropism in Arabidopsis roots, while BL promotes negative root phototropism ( Ruppel et al., 2001 ; Esmon et al., 2005 ). The positive root phototropic response to RL is not very apparent, as it is significantly weaker than BL-dependent negative phototropism and strong gravitropic responses. By employing mutants defective in gravitropism it has been demonstrated that phyA and phyB promote positive phototropism in roots ( Kiss et al., 2003a ). It is however unclear at this time precisely how phys are sensing directional light cues to promote photo-movements.

Despite their influences on positive root phototropism, experimental evidence argues against a role for a phy as a primary receptor of directional BL cues in hypocotyls of etiolated Arabidopsis seedlings. First, RL (or FR) does not induce shoot phototropism in etiolated seedlings of most species, including Arabidopsis ( Steinitz et al., 1985 ; Liscum and Briggs, 1996 ). Because phy function is coupled to its photocycling between the Pr (RL-absorbing) and Pfr (FR-absorbing) forms which can occur in response to irradiation with RL/FR or UV-A/BL ( Shinomura et al., 2000 ; Fankhauser, 2001 ), it is unlikely that phy can function as a primary phototropic receptor in BL if it is not doing so in RL or FR. Second, while the magnitude of phototropism is reduced in phyA and phyB mutants, the fluence dependencies of the responses are unchanged ( Parks et al., 1996 ; Janoudi et al., 1997a ; Janoudi et al., 1997b ; Lascève et al., 1999 ), indicating that phyA and phyB are not likely to function as primary phototropic receptors. Thus, phys, like the crys, have been proposed to act as modulators of phot1/phot2-dependent phototropic responses ( Liscum and Stowe-Evans, 2000 ; Stowe-Evans et al., 2001 ; Whippo and Hangarter, 2004 ). This modulatory activity will be discussed later in more detail.

Chloroplastic Zeaxanthin as a Phototropic Sensor: Enigma or Red Herring?

Historically there has been considerable debate over the identity of the chromophore mediating absorption of UV-A and BL cues, with two camps split between flavins and carotenoids ( Shropshire, 1908 ; Galston, 1977 ; DeFabo, 1980 ; Briggs and lino, 1983 ; Quinlones and Zeiger, 1994 ; Palmer et al., 1996 ; Quinones et al., 1996 ; Lascève et al., 1999 ). With the identification and characterization of the phots, which are clearly flavin-binding proteins capable of mediating primary perception of direction UV-A, BL, and GL cues in Arabidopsis, one would think the controversy over “flavins versus carotenoids” with respect to phototropism would be over. Not quite! In 2001, Jin and colleagues ( Jin et al., 2001 ) found that hypocotyl phototropism in Arabidopsis appears to require mature chloroplasts and suggested the need for a functional xanthophyll cycle. Much of their conclusions are based upon a simple observation that mature chloroplasts are present within the bending region of the hypocotyl, and that RL pretreatments that increase BL-dependent phototropism also broaden the “zone of chloroplast maturation” within the hypocotyl.

While a causal relationship between chloroplast maturation and phototropism is impossible to derive from these correlative phenotypic data, the authors provided preliminary genetic evidence to support their hypothesis. First, the phytoene-accumulating pds2 mutant that lacks all derivative carotenoid pigments ( Norris et al., 1995 ) exhibited neither chlorophyll autofluorescence associated with mature functional chloroplasts, nor detectable hypocotyl phototropism. Second, a previously uncharacterized mutant designated star , that apparently exhibits delayed greening, failed to exhibit either phototropism or autofluorescent chloroplasts after a 2 hr exposure to low fluence rate unilateral BL (0.3 µmol m -2 s -1 ), but exhibited both responses if pretreated with 4 hr of RL (4 µmol m -2 s -1 ) prior to BL exposure. The story is not likely to end here however since wild-type Arabidopsis seedlings grown on norflurazon (an inhibitor of phytoene desaturase; ( Bartels and McCullough, 1972 ; Britton, 1979 ), while exhibiting a dampened response, retain normal phototropic sensitivity ( Orbovic and Poff, 1991 ). Norflurazon-treated seedlings phenocopy the chloroplast but not the phototropic defects of the pds2 , similar to what has been observed for maize seedlings deficient in phytoene desaturase activity ( Palmer et al., 1996 ).

What's the next chapter in this saga? While nearly overwhelming evidence indicates that carotenoids are not primary receptors of phototropic stimuli, it is equally clear that carotenoid deficiency reduces the magnitude of phototropic curvatures. One plausible explanation for these observations that is also consistent with the apparent relationship between chloroplast development and phototropism is that some function(s) of the chloroplast is important for full phototropic competence, directly or indirectly, and that carotenoid deficiency simply impairs normal chloroplast development/function. Although this particular hypothesis has not been tested, it is interesting to note that the biosynthesis of the phytochromobilin (PφB), the phy chromophore, is entirely plastid localized ( Terry et al., 1993 ; Kohchi et al., 2001 ), and that the activity of PφB synthase, which converts biliverdin to PφB ( Kohchi et al., 2001 ), is stimulated by light in intact plastids, likely through production of NADPH (and ATP) via photosynthetic activity ( Terry and Lagarias, 1991 ). Phys, as already mentioned and to be discussed later in detail, appear to modulate the output(s) from the phot-dependent pathways that lead to phototropism in etiolated Arabidopsis seedlings. Hence, if PφB is limiting in etiolated seedlings, as appears to be the case at least in the hook region ( Murphy and Lagarias, 1997 ), and its plastid-localized synthesis is directly related to the amounts of active holophy (apophy plus PφB), defective chloroplast function might depress phototropic responses through reductions in the levels of photoactive phys that are capable of enhancing phot-mediated signaling. At this point it is important to keep an open mind relative to the role of the chloroplast and/or carotenoids in phototropism, and to develop new strategies to ask more directed questions like the one just proposed.

PHOTOTROPIC SIGNALING COMPONENTS

Phosphorylation: an output signal from phots, a cue for sensor adaptation, both, or neither.

As discussed above, the only photoreceptors that can clearly be assigned a role in primary perception of phototropic stimuli associated with etiolated seedling responses are phot1 and phot2 ( Liscum and Briggs, 1995 ; Christie et al., 1998 ; Sakai et al., 2001 ). Given that both phot1 and phot2 are light-activated Ser/Thr protein kinases ( Christie et al., 1998 ; Sakai et al., 2001 ; Matsuoka and Tokutomi, 2005 ) it is quite reasonable to hypothesize that phototropic signal transduction might involve phot-activated phosphorelays ( Briggs and Huala, 1999 ; Fankhauser and Chory, 1999 ; Liscum and Stowe-Evans, 2000 ; Briggs and Olney, 2001 ; Christie and Briggs, 2001 ). If this hypothesis is correct the phots might be expected to associate with protein kinases or phosphatases; however, no such interactions have yet been described. In fact the only known in planta phosphorylation substrates for the phots are the phots themselves, with autophosphorylation being described for both phot1 ( Christie et al., 1998 ) and phot2 ( Sakai et al., 2001 ). However, the phot2 protein kinase domain has the ability to phosphorylate casein in vitro ( Matsuoka and Tokutomi, 2005 ).

While the role of phot autophosphorylation is not entirely understood, at least one property of the reaction in maize, oat, and Arabidopsis indicates that the bulk of the phosphorylation of phot1 is not required for the induction of phototropism. Specifically, the fluence thresholds for low fluence rate-induced phototropism and bulk autophosphorylation differ by several orders of magnitude — phototropism being 2–3 orders more sensitive to BL than the autophosphorylation response ( Palmer et al., 1993 ; Salomon et al., 1997 ; Christie et al., 1998 ). Generation of a protein kinase dead mutant of phot1, through substitution of Asp 806 with Asn within the kinase domain that prevents binding of Mg 2+ for phosphate transfer ( Hanks and Hunter, 1995 ), results in the complete abolition of phot1 autophosphorylation and mediated responses ( Christie et al., 2002 ; Inoue et al., 2008 ). This finding indicates that phot1 protein kinase activity is absolutely required for both autophosphorylation and subsequent phot1-dependent responses, although how the two are connected remains unknown. One possibility may be reflected by the hierarchical nature of the auto-phosphorylation response, where some sites exhibit BL-induced phosphorylation at lower fluences than others ( Salomon et al., 2003 ). Thus it is plausible that while bulk phosphorylation may not be necessary for phototropism, phosphorylation at specific sites under lower fluence conditions may be prerequisite for phototropic signal transduction.

Additional insights have been made on phot1 autophosphorylation by comparison of phot1 phosphorylation sites between dark and in vivo BL-irradiated seedlings using gas chromatography-mass spectrometric techniques ( Inoue et al., 2008 ; Sullivan et al., 2008 ). Multiple Ser and Thr phosphorylation sites have been identified throughout the phot1 polypeptide and among them Ser 851 in the activation loop of phot1 kinase domain appears to be important for both proper phot1 localization ( Kaiserli et al., 2009 ) and various phot1-mediated responses. For example, transgenic Arabidopsis seedlings carrying a Ser 851 to Ala substitution fail to exhibit normal BL-induced phototropic, stomatal opening or chloroplast accumulation responses ( Inoue et al., 2008 ). However, substitution of other phosphorylatable Ser residues with Ala, such as Ser 849 in the activation loop, had little or no effect on phototropism ( Inoue et al., 2008 ), suggesting that different sites have different biochemical roles in the modulation of phot activity. At present it is not known whether Ser 851 represents a low or high fluence-responsive site as the corresponding site was not identified in the oat study discussed above ( Salomon et al., 2003 ).

PROTEINS INVOLVED IN EARLY POST-PERCEOPTION SIGNALING

Nph3: a modular adaptor protein and regulator of phot signaling.

Despite extensive screening for loss-of-function phototropism mutants, only one mutant locus, nph3, has been described that appears to alter a protein that functions close to, but downstream of, the phot1 photoperception event ( Liscum and Briggs, 1995 , 1996 ; Motchoulski and Liscum, 1999 ). In particular, nph3 mutations have been shown to disrupt phototropism in etiolated seedlings under low fluence rate conditions (<1 µmol m -2 s -1 ) ( Liscum and Briggs, 1996 ; Motchoulski and Liscum, 1999 ), as well as high fluence conditions (>1 µmol m -2 s -1 ) ( Inada et al., 2004 ) without affecting BL-induced autophosphorylation of phot1 ( Liscum and Briggs, 1995 ). By means of combinatorial mutant analysis NPH3 has been demonstrated to function in both phot1 and phot2 phototropic signaling ( Inada et al., 2004 ).

The NPH3 gene ( Table 1 ) was isolated by a map-based cloning approach and found to encode a member of a novel family of plant-specific proteins ( Motchoulski and Liscum, 1999 ). Not surprisingly, given the similarity of phenotypes and the genetic interaction between phot and nph3 mutants, the NPH3 transcript is expressed highly in dark-grown seedlings in all the tissues and remains unaffected by light (A. Motchoulski and E. Liscum, unpublished; ( Inada et al., 2004 ), similar to what was discussed already for PHOT1. In rice, COLEOPTILE PHOTOTROPISM1 (CPT1), was identified as an ortholog of NPH3, and nph3 and cpt1 mutants were found to have similar phenotypes implying that NPH3 and its orthologs have conserved functional roles across plant taxa ( Haga et al., 2005 ).

As shown in Figure 4B , NPH3 belongs to a 33-member protein family in Arabidopsis, designated NRL ( N PH3/ R PT2- L ike) after the founding members of the family — NPH3 ( Motchoulski and Liscum, 1999 ) and ROOT PHOTOTROPISM 2 (RPT2) ( Sakai et al., 2000 ). Primary amino acid sequence conservation between members of the NRL protein family is found in five discrete, positionally conserved, regions designated DIa, DIb, DII, DIII, and DIV ( Figure 4A ). Within domain DIV there is a consensus metazoan Tyr phosphorylation site ([RK]-x(2,3)-[DE]-x(2,3)-Y; ( Patschinsky et al., 1982 ) that is conserved in 29 of the 33 members of the family, including NPH3 (RTCDDGLY 545 ) ( Motchoulski and Liscum, 1999 ). Although it is not known whether phosphorylation can occur on Tyr 545 of NPH3, it is worth noting that the nph3-2 mutant that carries in an in-frame deletion of this residue is phenotypically indistinguishable from a null mutant (nph3-6) that contains a stop codon at the Trp 2 position ( Motchoulski and Liscum, 1999 ). It remains to be determined whether Tyr 545 is important for function of NPH3 (e.g., is it differentially phosphorylated in ‘signaling’ and ‘non-signaling’ NPH3 isoforms?) or as a structural motif that regulates protein stability/abundance.

Consensus domain structure of the NPH3/RPT2 (NRL) protein family.

(A) The DIa, DIb, DII, DIII, and DIV regions (black bars) represent areas of sequence conservation among members of the NPH3/RPT2 protein family. The BTB/POZ (red region) and coiled-coil (blue region) domains represent structurally conserved motifs. While not all members of the family contain all of these domains (see cladogram in Figure 4B ), each domain is present in both NPH3 and RPT2 ( Motchoulski and Liscum, 1999 ; Sakai et al., 2000 ). Inter-domain regions (grey) while not sequence conserved exhibit moderate structural similarities from member to member (see http://www.biosci.missouri.edu/liscum/nph3-rpt2figs.html ).

(B) Cladogram of the NRL protein family based on amino acid sequence obtained from Arabidopsis genome annotation (TAIR8) at TAIR. NRL protein sequences were aligned by ClustalW and the resulting ClustalW alignment was used to generate a rooted phylogenetic tree (Cladogram). Corresponding AGI numbers for a given NRL member is given in parenthesis.

At present no general functional role for various members of NRL family in plants is easily predictable. Yet, recent reports by various groups suggest that the physiological roles played by various NRL members may be quite diverse. First, mutations of NRL20 , known as mab4/enp/npy1 (macchi-bou4/enhancer of pinoid/naked pins in yuc mutants 1), were isolated separately as enhancers of pinoid ( pid ) and yucca ( yuc ) phenotypes ( Cheng et al., 2007 ; Furutani et al., 2007 ). Interestingly PID is a protein kinase whose catalytic domain clusters in the same phylogenetic clade as the phot kinase catalytic domain ( Christensen et al., 2000 ; Benjamins et al., 2001 ; Galvan-Ampudia and Offringa, 2007 ). Moreover, PID appears to regulate the activity/function of PIN-FORMED (PIN) proteins, a class of auxin efflux carriers, to modulate asymmetric and polar auxin transport ( Christensen et al., 2000 ; Benjamins et al., 2001 ; Friml et al., 2004 ; Galvan-Ampudia and Offringa, 2007 ; Michniewicz et al., 2007 ; Robert and Offringa, 2008 ; Sukumar et al., 2009 ). In a phenotypic class quite distinct from the nph3 and mab4/enp/npy1 mutants, the seth6 mutants (containing lesions in NRL18) exhibit a block in pollen germination and tube growth ( Lalanne et al., 2004 ), suggesting that NRL functions are quite diverse indeed.

Members of the NRL protein family, in addition to displaying modular sequence conservation, exhibit modular structural features that are positionally conserved while sequence diverged ( Figure 4A ). Two of these structurally-conserved regions represent known protein-protein interaction motifs; a BTB (broad complex, tramtrack, bric à brac)/POZ (pox virus and zinc finger) domain ( Albagli et al., 1995 ; Aravind and Koonin, 1999 ; Stogios et al., 2005 ) in the amino-terminal region, and a coiled-coil domain ( Cohen and Parry, 1990 ; Lupas, 1996 ) in the carboxyl-terminal region ( Motchoulski and Liscum, 1999 ; Sakai et al., 2000 ; Stogios et al., 2005 ). While no particular function can be inferred from the presence of a BTB/POZ (hereafter referred to simply as BTB) or a coiled-coil domain, the fact that most of the NRL family members contain one or both (21 of 33 members, including NPH3 which contains both; Figure 4B ) suggests that protein-protein interactions are an important feature of the biochemical function of this family.

While the subcellular localization of most members of the NRL family is currently unknown, NPH3, like phot1 ( Briggs and Huala, 1999 ; Inada et al., 2004 ), has been shown to be associated with the plasma membrane ( Motchoulski and Liscum, 1999 ; Lariguet et al., 2006 ; Pedmale and Liscum, 2007 ). In dark-grown wild-type seedlings NPH3 exists in a phosphorylated form (hereafter referred to as NPH3 DS ; DS, dark state) that is rapidly converted into a dephosphorylated form in response to BL irradiation (NPH3 LS ; LS, lit state) in a time dependent manner, but independent of fluence rate ( Pedmale and Liscum, 2007 ; Tsuchida-Mayama et al., 2008 ). Moreover, NPH3 LS is rapidly converted back into NPH3 DS by merely placing the light-treated seedlings in darkness ( Pedmale and Liscum, 2007 ; Tsuchida-Mayama et al., 2008 ). Since NPH3 and phot1 share the same sub-cellular space, it seemed possible that NPH3 might be a substrate for phot protein kinase activity. However, Pedmale and Liscum ( Pedmale and Liscum, 2007 ) demonstrated that NPH3 DS is formed in phot1phot2 double mutants, indicating that neither phot1 nor phot2 is required for dark-dependent phosphorylation of NPH3. Interestingly, conversion of NPH3 DS to NPH3 LS in BL is phot1 dependent, while phot2 does not appear to play a role ( Pedmale and Liscum, 2007 ; Tsuchida-Mayama et al., 2008 ). This suggests that the protein phosphatase dephosphorylating NPH3 DS might function immediately downstream of phot1, and that phot1 might well be regulating the unknown phosphatase.

Pedmale and Liscum ( Pedmale and Liscum, 2007 ) showed that dephosphorylation of NPH3 might be necessary for phototropism, since conversion of NPH3 DS to NPH3 LS was shown to be correlated with BL dependent phototropism. In a more recent study Tsuchida-Mayama and colleagues ( Tsuchida-Mayama et al., 2008 ) came to the conclusion that conversion of NPH3 DS to NPH3 LS is not required for phototropic signaling. This latter conclusion was based largely on the observations that NPH3 phosphorylation incompetent mutants fail to rescue aphophototropism in a null-mutant background. However, closer examination of these results reveal that it may be premature to throw out the model proposed by Pedmale and Liscum ( Pedmale and Liscum, 2007 ). For example, all of the potential phosphorylation sites examined by Tsuchida-Mayama and colleagues ( Tsuchida-Mayama et al., 2008 ) were identified entirely through computational methods, and no report of in vivo confirmation currently exists. Even more importantly, the finding that mutation of a Ser/Thr to Ala results in apparently phototropically competent NPH3 protein ( Tsuchida-Mayama et al., 2008 ) is entirely consistent with a model in which NPH3 LS (dephosphorylated NPH3) is the active signaling state ( Pedmale and Liscum, 2007 ) since those mutations would be expected to result in a constitutively active signaling state. The true test of the alternative model proposed by Tsuchida-Mayama and colleagues ( Tsuchida-Mayama et al., 2008 ) would be to generate phosphorylation mimic mutants that lock NPH3 in a pseudo-phosphorylated state (NPH3 DS -like). Such mutations would prevent conversion of NPH3 DS to NPH3 LS , thus directly testing the validity of the two opposing models.

Emergent Model: NPH3 as a Component of a CULLIN3-based Ubiquitin Ligase

Recent reports have demonstrated that BTB-domain containing proteins can participate as a substrate-specific adaptors in CULLIN3 (CUL3)-based E3 ubiquitin ligases, also known as CRL3s (CUL3-RING-ligase) ( Geyer et al., 2003 ; Krek, 2003 ; Pintard et al., 2003 ; Xu et al., 2003 ; Willems et al., 2004 ; Dieterle et al., 2005 ; Figueroa et al., 2005 ; Gingerich et al., 2005 ; Petroski and Deshaies, 2005 ; Stogios et al., 2005 ; Weber et al., 2005 ). Interestingly, the activity of E3 ubiquitin ligases can be influenced by phosphorylation of its core components ( Spanu et al., 1994 ; Glickman and Ciechanover, 2002 ; Schwechheimer and Calderon Villalobos, 2004 ), and the phosphorylation status of the substrates themselves can influence the ability of the E3 ligase to target those substrates ( Spanu et al., 1994 ; Wang et al., 2004 ). Hence it seems plausible that NPH3, based on its sequence and structural properties ( Motchoulski and Liscum, 1999 ; Inada et al., 2004 ; Celaya and Liscum, 2005 ; Pedmale and Liscum, 2007 ) represents a substrate adapter component of a CRL3, and that the conversion of NPH3 DS and NPH3 LS might constitute the ‘on/off switch for the activity of CRL3 NPH3 ( Celaya and Liscum, 2005 ; Pedmale and Liscum, 2007 ). Given that BTB-containing proteins normally function as dimers/multimers ( Stogios et al., 2005 ) and that NPH3 is a member of the larger NRL family, it seems appropriate to hypothesize that NPH3 can homodimerize with itself, or heterodimerize with other NRL family members, allowing a CRL-3 NPH3/NRL to target numerous substrates. Such an arrangement appears to be common with mammalian and fungal BTB-containing proteins. For example, homo- and heterodimerization of the mammalian BTB protein Keap1 allows for targeting of multiple target proteins for ubiquitination by CRL3 Keap1 ( Lo and Hannink, 2006 ). Future studies on the biochemical function of NPH3 and identification of substrate(s) of CRL3 NPH3 will provide a wealth of new insights in how early phototropic signal transduction proceeds and the role that protein ubiquitination plays in these processes.

RPT2: A Modular Adapter for phot Signaling?

RPT2 ( Table 1 and Figure 4B ), the other founding member of the NRL family, was originally identified via a mutant allele that conditions reduced phototropism ( Okada and Shimura, 1992 ). However, in the case of the rpt2 mutant a phototropic defect is only obvious under high fluence rate BL (≥ 10µmol m -2 s -1 ) ( Sakai et al., 2000 ; Inada et al., 2004 ). It thus appears that RPT2 functions over a fluence rate range similar to that in which phot2 functions ( Sakai et al., 2000 ; Sakai et al., 2001 ) ( Table 3 ). A parallel between RPT2 and PHOT2 is also observed at the level of transcript abundance, with both transcripts being detectable at only very low levels in etiolated seedlings but increasing in abundance in response to light with similar fluence rate and wavelength dependencies ( Sakai et al., 2000 ; Sakai et al., 2001 ) ( Table 3 ).

RPT2, like NPH3 ( Motchoulski and Liscum, 1999 ; Lariguet et al., 2006 ), is a plasma membrane-localized protein that has been found to co-immunoprecipitate with phot1 in extracts from etiolated Arabidopsis seedlings ( Inada et al., 2004 ). It also appears that RPT2 and NPH3 can heterodimerize through their amino-terminal BTB-domains ( Inada et al., 2004 ), though this may not be particularly surprising as BTB containing domains are known to mediate protein-protein interaction for homo- or heterodimerization ( Ahmad et al., 1998a ; Stogios et al., 2005 ). While Inada and colleagues proposed that RPT2 directly interacts with phot1 — largely based on weak interaction in yeast ( Inada et al., 2004 ), the finding that RPT2 and NPH3 strongly interact in yeast suggests that RPT2 may co-immunoprecipitate in plant extracts with phot1 via interaction with NPH3, which interacts strongly and directly with phot1 in vitro , in yeast and in planta ( Motchoulski and Liscum, 1999 ; Lariguet et al., 2006 ). The conditional phototropic phenotype of the rpt2 mutant in comparison to the apparent complete aphototropic phenotype of the nph3 mutants, along with the sequence and structural homologies between the RPT2 and NPH3 proteins ( Motchoulski and Liscum, 1999 ; Sakai et al., 2000 ; Inada et al., 2004 ), suggest that RPT2 may have partial overlapping function with NPH3 in phototropic signaling but only under high fluence rate conditions. While it seems appropriate to speculate that RPT2 also participates in function of a CRL3 complex, either as a homodimer or as a heterodimer with NPH3, this has yet to be tested.

PKS1: A Bridge Between phot and phy Signaling?

PHYTOCHROME KINASE SUBSTRATE 1 (PKS1), while identified in a yeast-two-hybrid screen that utilized the carboxylterminus of phyA as a bait, is the first protein known to interact with both phyA and phyB in the cytosol ( Fankhauser et al., 1999 ; Lariguet et al., 2003 ). Phys readily phosphorylate PKS1 both in vitro and in vivo in a light-dependent fashion, and it has been hypothesized that phosphorylated PKS1 negatively regulates phy function ( Fankhauser et al., 1999 ; Schepens et al., 2008 ). PKS1 is a member of a small gene family in Arabidopsis ( PKS1 to PKS4 ) with no predictable functional sequence motifs ( Lariguet et al., 2003 ; Lariguet et al., 2006 ). Interestingly, BL stimulates the expression of PKS1 ( Lariquet, 2006 ), suggesting that PKS1 may also function in BL responses such as phototropism. In line with this possibility Lariquet and colleagues ( Lariguet et al., 2006 ) have shown that pks1pks2pks4 triple mutant seedlings exhibit reduced phototropism in low fluence rate BL, conditions under which phot1 operates as the primary phototropic photoreceptor ( Celaya and Liscum, 2005 ; Holland et al., 2009 ). In the same study it was demonstrated that PKS1 is a plasma membrane-associated protein and that it physically interacts with both phot1 and NPH3 in vitro and in planta ( Lariguet et al., 2006 ). It has recently been shown that PKS1 also positively regulates phot1-dependent BL-induced negative root phototropism in Arabidopsis by negatively regulating gravitropism ( Boccalandro et al., 2008 ), and that it modulates phy-dependent positive root phototropism induced by RL ( Molas and Kiss, 2008 ). A common theme emerging from such studies is that PKS proteins appear to regulate directional orientation of organs to various stimuli by influencing asymmetric growth ( Lariguet and Fankhauser, 2004 ; Lariguet et al., 2006 ; Boccalandro et al., 2008 ; Schepens et al., 2008 ). How exactly the PKS proteins function biochemically is currently unknown, although it does appear that these proteins can function in both phy- and phot-dependent signaling pathways.

Other phot-Interacting Proteins: A 14-3-3 and a Dynein Light Chain-like Protein (VfPIP)

As discussed in the previous sections, three phot1-interacting proteins have been characterized that play roles in phototropic signaling. Two additional phot1-interacting proteins, a 14-3-3 and a dynein light chain-like protein (VfPIP, for phot1-interacting protein) have been identified in Vicia faba ( Kinoshita et al., 2003 ; Emi et al., 2005 ), but their roles in phototropism have yet to be examined. The 14-3-3 protein was found through its reversible binding to Vfphot1a and Vfphot1b (paralogs of Arabidopsis phot1); binding that is dependent upon specific BL-induced autophosphorylation of the phot1 isoforms ( Kinoshita et al., 2003 ; Inoue et al., 2008 ). Recently, it has been found that phot1 interacts with non-epsilon type 14-3-3 proteins in Arabidopsis as well, though no interactions have been observed as yet between phot2 and 14-3-3 proteins ( Sullivan et al., 2009 ). Although it is presently not known how 14-3-3 proteins might influence phot1 signaling several possibilities exist: for example, 14-3-3 proteins are known to interact with a target protein to generate a scaffold so that other proteins can dock, to inhibit a target protein's activity, to change in subcellular localization of the target protein or to tag a protein for post-translational modification ( Kinoshita et al., 2003 ; Ferl, 2004 ; Gampala et al., 2007 ). Emi and colleagues ( Emi et al., 2005 ) proposed that VfPIP, identified by virtue of its ability to interact with Vfphot1a and found to localize to the cortical microtubules in guard cells, functions as a motor-proteins to mediate phot1-dependent stomatal opening in response to BL.

Ca 2+ As a Second Messenger

It may not be too surprising given its pervasive role in intracellular signaling ( Bush, 1993 ) to find that Ca 2+ may play a role in the transduction of phototropic stimuli in higher plants ( Gehring et al., 1990 ; Ma and Sun, 1997 ; Harada and Shimazaki, 2007 ). A study by Baum and colleagues ( Baum et al., 1999 ) reported that a transient increase in cytoplasmic Ca 2+ ([Ca 2+ ] cyt ) is observed in wild-type Arabidopsis seedlings exposed to BL, and that this response is severely impaired in the phot1 mutant background. It was also shown that Ca 2+ was moving into the cytosol across the plasma membrane, thus placing the necessary channel activity in the same intracellular compartment as phot1 - the plasma membrane. Use of a noninvasive ion-selective microelectrode ion flux measurement (MIFE) technique allowed Babourina and colleagues ( Babourina et al., 2002 ) to measure the net Ca 2+ ion flux across the plasma membrane and cell wall in Arabidopsis seedlings. It was found that in phot1 and phot1phot2 mutants BL did not initiate the immediate influx of Ca 2+ in to the cytoplasm, while Ca 2+ influx in phot2 mutant seedlings was comparable to wild-type seedlings. These findings indicate that BL-induced influx of Ca 2+ from the apoplastic space occurs primarily through the action of phot1 ( Babourina et al., 2002 ).

BL dependent opening of plasma membrane calcium channels characteristic of Ca 2+ influx is reported to be dependent on phot1 in mesophyll cells of Arabidopsis leaves but independent of photosynthetic activity ( Stoelzle et al., 2003 ). In addition to phot1, phot2 is also capable in eliciting rapid Ca 2+ influx at higher fluence rates ( Harada et al., 2003 ). The investigators used the bioluminescent Ca 2+ indicator aequorin in Arabidopsis phot1, phot2 and phot1phot2 mutant plants to demonstrate that phot1 and phot2 contributed additively in elevation of free [Ca 2+ ] cyt . Given the differences in photosensitivities of phot1 and phot2, it is not surprising that phot2 efficiently mediates the influx of Ca 2+ at fluence rates of BL between 1 and 250 µmol m -2 s -1 , whereas phot1 is effective in the 0.1 to 50 µmol m -2 s -1 range. At this point it is unclear if phot2 is able to mediate Ca 2+ influx from the apoplast independent of phot1 since the two studies had conflicting results ( Babourina et al., 2002 ; Harada et al., 2003 ). Moreover, given the overlapping but distinct roles of phot1 and phot2 in mediating BL responses, it is possible that an individual phot might trigger the release of free [Ca 2+ ] cyt from different stores for specific responses. It is interesting to note that the rapid transient BL-induced increase in [Ca 2+ ] cyt is observed in both cry1 and cry2 mutants ( Baum et al., 1999 ; Stoelzle et al., 2003 ), suggesting that phots are the only class of BL receptors responsible for this plasma membrane-localized response.

BL is also known to induce the rapid phosphorylation and activation of plasma membrane H + -ATPase in a phot1- and phot2-dependent manner ( Kinoshita and Shimazaki, 1999 ; Kinoshita et al., 2001 ). Harada and Shimazaki ( Harada and Shimazaki, 2009 ) have shown that H + -ATPase activation is prerequisite to the phot-dependent BL-induced [Ca 2+ ] cyt increase. Another possible regulatory mechanism has also been reported by Chen and colleagues ( Chen et al., 2008 ) who found that BL, acting through phots, suppresses steady-state transcript levels of INOSITOL POLYPHOSPHATE 5-PHOSPHATASE 13 (5PTase13), a gene encoding an enzyme that dephosphorylates inositol polyphosphates (Ins (1,4,5) P3, Ins (1,3,4,5) P4 or PtdIns (4,5) P2). The authors proposed that in darkness 5PTase13 enzyme activity is high due to a higher level of protein and that the reduced levels of inositol polyphosphates keep plasma membrane Ca 2+ channel activity low, thus keeping the [Ca 2+ ] cyt low. In contrast, in BL 5PTase13 enzyme levels are suppressed thereby leading to increased levels of inositol polyphosphates, Ca 2+ channel activity, and an increase in free [Ca 2+ ] cyt . At present it is not known how well, if at all, the temporal and photobiological properties of 5PTase13 enzyme and Ca 2+ levels correlate.

While the role of BL-induced changes in [Ca 2+ ] cyt in phototropic signaling remains to be determined it is worth noting that Ca 2+ has also been proposed as a possible second messenger for gravitropic signaling ( Trewavas and Knight, 1994 ; Sinclair and Trewavas, 1997; Chen et al., 1999 ). Moreover, identification of calmodulin-like TOUCH3 (TCH3) protein and the calcium binding motif containing PINOID-BINDING PROTEIN 1 (PBP1) as PID-interacting proteins provides evidence for the existence of cross-talk between calcium and auxin movement ( Benjamins et al., 2003 ). Though PID action in phototropic signaling has yet to be described, PID has been shown to be required for the lateral relocalization of PIN1 ( Friml et al., 2004 ) and to function in gravitropism ( Benjamins et al., 2001 ). Interestingly, PIN1 has also been shown to be relocalized in response to phototropic stimulation in a phot1-dependent manner ( Blakeslee et al., 2004 ). As will be discussed in the following section auxin relocalization represents a common link between various tropic responses ( Firn and Digby, 1980 ; Poff et al., 1994 ; Kaufman et al., 1995 ; Estelle, 1996 ). It is therefore attractive to speculate that the regulation of PIN1 localization and auxin movement by both PID and phot1, members of the same subclade of protein kinases, the AGCVIII kinases ( Galvan-Ampudia and Offringa, 2007 ; Robert and Offringa, 2008 ), may utilize Ca 2+ and Ca 2+ -binding proteins as common signaling elements.

Differential Auxin Localization and Changes In Gene Expression

Regulation of auxin transport and accumulation.

Auxins have long been implicated as regulators of tropic growth responses ( lino, 1990 ; Kaufman et al., 1995 ). In fact, auxin is a linchpin in most mechanistic models of phototropism (and gravitropism) ( Estelle, 1996 ; Chen et al., 1999 ; Liscum and Stowe-Evans, 2000 ; Hoshino et al., 2007 ). The Cholodny-Went theory ( Went and Thimann, 1937 ) provides much of the basis for the proposed central role of auxin in tropic responses. In brief, this theory holds that tropic stimuli induce differential lateral auxin transport that leads to the unequal distribution of auxin, and hence growth, in the two sides of a curving organ. While differential auxin transport, or accumulation, has been difficult to demonstrate in many cases ( Trewavas et al., 1992 ), it has become clear through the use of Arabidopsis mutants that transport of, and response to, auxin is prerequisite for the development of tropic curvatures ( Bennett et al., 1996 ; Estelle, 1996 ; Watahiki and Yamamoto, 1997 ; Chen et al., 1998 ; Luschnig et al., 1998 ; Muller et al., 1998 ; Rouse et al., 1998 ; Stowe-Evans et al., 1998 ; Utsuno et al., 1998 ; Chen et al., 1999 ; Marchant et al., 1999 ; Palme and Galweiler, 1999 ; Rosen et al., 1999 ; Yamamoto and Yamamoto, 1999 ; Harper et al., 2000 ; Rashotte et al., 2000 ; Geldner et al., 2001 ; Swarup et al., 2001 ; Friml et al., 2002 ; Tanaka et al., 2006 ). Numerous studies have shown that auxin efflux processes, which are necessary for the establishment of a lateral gradient of auxin ( Lomax et al., 1995 ; Friml et al., 2002 ), may be regulated via reversible protein phosphorylation ( Bernasconi, 1996 ; Garbers et al., 1996 ; Delbarre et al., 1998 ; Christensen et al., 2000 ; Rashotte et al., 2001 ; Michniewicz et al., 2007 ). These findings provide a compelling potential connection between the phots, which are light-activated protein kinases ( Christie et al., 1998 ; Sakai et al., 2001 ), and the differential auxin gradients that have been observed in seedlings irradiated with unilateral BL ( lino, 1990 ; Esmon et al., 2006 ).

Several possible biochemical pathways from phot activation to changes in auxin transport can be postulated. First, a direct phot1/phot2-dependent phosphorelay involving currently unidentified protein kinases, or via PID, might lead to an altered auxin transport activity. Alternatively, phots might activate/modulate auxin transport through an indirect pathway that utilizes Ca 2+ as a second messenger. In this latter scenario phot1 (phot2)-dependent increases in cytoplasmic Ca 2+ levels might lead to activation of a Ca 2+ -dependent protein kinase (CDPK) ( Satterlee and Sussman, 1998 ; Harmon et al., 2000 ) or PID kinase via the action of Ca 2+ -binding PBP1 or TCH3, which would in turn phosphorylate an auxin transport complex and thus alter its activity. A third possible outcome of phototropin activation is the modulation of auxin transporter localization, rather than the activity of single molecules. For example, relocalization of auxin efflux carriers from a basal to lateral region of a cell would result in a shift from basipetal to lateral auxin transport. Geldner and colleagues ( Geldner et al., 2001 ) have shown that the apparent static asymmetric localization of PIN1, one member of a family of auxin efflux carriers ( Chen et al., 1998 ; Luschnig et al., 1998 ; Muller et al., 1998 ; Utsuno et al., 1998 ; Palme and Galweiler, 1999 ; Titapiwatanakun et al., 2009 ), actually results from a rapid actin-dependent cycling of PIN1 between the plasma membrane and endosomal compartments. Interestingly, though the mechanism has yet to be resolved, phot1 has been shown to be genetically required for the redistribution of PIN1 in the shaded flank of a phototropically-stimulated seedling ( Blakeslee et al., 2004 ). It is also worth noting that it has been found that PID can directly phosphorylate the PIN1 auxin efflux carrier to alter its endocytotic cycling ( Skirpan et al., 2009 ; Huang et al., 2010 ; Zhang et al., 2010 ), suggesting that phot1 protein kinase activity could be linked to this process. Another auxin efflux carrier, PIN3, has been shown to localize to all faces of the plasma membrane in non-tropically stimulated cells, but relocalize to the lateral faces following gravitropic stimulation ( Friml et al., 2002 ). Though no phototropic stimulation-dependent relocalization of PIN3 has been demonstrated ( Blakeslee et al., 2004 ), pin3 mutations render seedlings defective in both gravitropic and phototropic responses ( Friml et al., 2002 ), indicating that PIN3 function is important for phototropism.

As second class of auxin transporters, the ABCB subgroup of ABC transporter superfamily ( Verrier et al., 2008 ), has also been associated with tropic responsiveness. For example, mutations in ABCB19 (also known as PGP19 ) result in enhanced phototropic and gravitropic responses in Arabidopsis seedlings ( Noh et al., 2003 ; Blakeslee et al., 2004 ). In addition, PIN1 is mislocalized in abcb19 mutants in manner similar to that observed when wild-type seedlings are exposed to BL ( Noh et al., 2003 ; Blakeslee et al., 2004 ). Interestingly, steady-state levels of ABCB19 mRNA are suppressed through the action of phys and crys ( Nagashima et al., 2008 ), suggesting yet another mechanism by which these other photoreceptors might influence phot-dependent phototropism.

Given the overlapping localization of phot, PIN and ABCB proteins in the plasma membrane of elongating cells is seems plausible that phots may influence auxin transport by directly interacting with and modulating the activity/localization of the latter proteins. Alternatively, phot activation could also lead indirectly to changes in the activity/localization of auxin transporters, possibly through phosphorylation or Ca 2+ -dependent changes in the activity of a variety of regulator proteins, such as the NPA (naphthylphthalamic acid)-binding protein ( Muday et al., 1993 ), 3-phosphoinositide dependent kinase 1 (PDK1) ( Zegzouti et al., 2006 ) and the calossin-like protein BIG ( Gil et al., 2001 ). Determining exactly how phot activation leads to changes in auxin transporter activity/localization will be one of the most active areas of phototropic research over the next few years.

Changes in auxin-dependent transcription

In recent years significant advances have been made in understanding how differential auxin gradients established in response to tropic stimulation are interpreted at a molecular level to give rise to differential growth patterns. Critical to these advances was the identification and characterization of semi-dominant mutations in the NON-PHOTOTROPIC HYPOCOTYL 4/MASSUGU 1/TRANSPORT INHIBITOR RESISTANT 5 (NPH4/MSG1/TIR5) locus (hereafter referred to as NPH4 ) ( Table 1 ) of Arabidopsis that disrupt multiple differential growth responses in aerial tissues, including phototropism and gravitropism, without altering overall growth and development of the plant ( Liscum and Briggs, 1995 , 1996 ; Ruegger et al., 1997 ; Watahiki and Yamamoto, 1997 ; Stowe-Evans et al., 1998 ; Watahiki et al., 1999 ). These phenotypes, together with the findings that the nph4 mutants exhibit severely impaired auxin-induced stem bending ( Watahiki and Yamamoto, 1997 ), stem growth inhibition ( Watahiki and Yamamoto, 1997 ; Stowe-Evans et al., 1998 ), and gene expression responses ( Stowe-Evans et al., 1998 ). suggested that the NPH4 protein functions as a modulator of auxin-dependent differential growth. Map-based cloning of the NPH4 gene revealed that it encodes the auxin response factor ARF7 ( Harper et al., 2000 ), a member of a large family of transcription factors whose activities are regulated by auxin ( Guilfoyle et al., 1998 ; Liscum and Reed, 2002 ). NPH4/ARF7 functions as a transcriptional activator in transient expression assays ( Ulmasov et al., 1999 ), consistent with the impaired auxin-induced gene expression profiles observed in the nph4/arf7 mutants ( Stowe-Evans et al., 1998 ). It therefore appears that localized changes in gene expression are at least one of the likely consequences of a differential auxin gradient established in response to phototropic stimulation ( Harper et al., 2000 ; Stowe-Evans et al., 2001 ).

NPH4/ARF7 has been shown to interact with numerous members of the Aux/IAA family of auxin-induced proteins that function as dominant repressors of ARF activity ( Tiwari et al., 2001 ; Tiwari et al., 2004 ; Li et al., 2009 ). Of particular interest in the context of tropic growth regulation are the MASSUGU2 (MSG2/IAA19) and AUXIN RESISTANT5 (AXR5/IAA1) proteins, in which dominant gain-of-function mutations condition severely impaired phototropic and gravitropic responses ( Park et al., 2002 ; Tatematsu et al., 2004 ; Yang et al., 2004 ). These findings, together with a developing and sophisticated understanding of how auxin regulates changes in gene expression, have allowed the development of a relatively simple model for tropic growth can occur in response to auxin-responsive transcription ( Tatematsu et al., 2004 ; Holland et al., 2009 ). In brief, elevated levels of free auxin, like those induced differentially across a phototropically-induced stem ( Esmon et al., 2006 ; Haga and lino, 2006 ), promote the 26S proteasome-dependent degradation of Aux/IAA proteins, such as MSG2/IAA19 and AXR5/IAA1, through a targeting mechanism mediated by the CRL1 TIR1 (also known as SCF TIR1 ) complex that contains the auxin receptor TIR1 ( Tan et al., 2007 ). Given that MSG2/IAA19 and AXR5/IAA1 would be found as heterodimers with NPH4/ARF7 under low auxin conditions thus repressing activity of the latter, their auxin-induced degradation would therefore allow homodimerization of NPH4/ARF7 and subsequent transcriptional upregulation of ‘auxin-responsive genes’ ( Tatematsu et al., 2004 ; Celaya and Liscum, 2005 ; Holland et al., 2009 ). In an interesting twist to this model, it is likely that MSG2/IAA19 and AXR5/IAA1 themselves represent target genes for NPH4/ARF7 regulation ( Stowe-Evans et al., 1998 ; Tatematsu et al., 2004 ), with the transcription and translation of these genes providing a feed-back mechanism to rapidly dampen the auxin response ( Liscum and Reed, 2002 ).

A microarray approach was utilized to identify potential transcriptional targets of NPH4/ARF7 under tropically-responsive conditions. Several, tropic stimulus-responsive (TSI) transcripts were identified by comparing expression profiles between opposing flanks of phototropically- and gravitropically-stimulated hypocotyls of Brassica oleracea ( Esmon et al., 2006 ). Among the TSI transcripts identified were EXPANSIN (EXP) 1 and 8 , whose steady-state mRNA levels were shown to be up-regulated in a tropic stimulation and auxin-dependent fashion in the flank farthest from the tropic stimulation- prior to the development of a differential growth response ( Esmon et al., 2006 ). These genes are particularly interesting because they encode proteins that are thought to break H-bonds between cellulose microfibrils and hemicellulose in the cell wall to increase wall extensibility, allowing for increased turgor-driven cell elongation ( Cosgrove, 2005 ; Yennawar et al., 2006 ; Durachko and Cosgrove, 2009 ). Two GH3 genes ( GH3.5 and GH3.6/DFL1 ), known to encode enzymes that catalyze the conjugation of free IAA to amino acids ( Staswick et al., 2005 ), were also identified in this study. While the steady-state levels of these genes increased in the same spatial region and with similar tropic stimulation- and auxin-dependencies as the EXP genes, the timing of expression was considerably delayed in comparison to the latter genes, consistent with the notion that the proteins encoded by the GH3 genes would act to suppress auxin responsiveness by decreasing the free auxin pool ( Esmon et al., 2006 ). Not surprisingly, given the auxin-dependencies of the TSI genes, the promotor regions of each of these genes contain at least one auxin responsive element (AuxRE) ( Esmon et al., 2006 ) known to provide a binding site for ARF proteins, like NPH4/ARF7 ( Hagen and Guilfoyle, 2002 ; Liscum and Reed, 2002 ). Consistent with this finding it was also found that auxin-induced expression of the TSI genes in Arabidopsis is dependent upon the presence of NPH4/ARF7 ( Esmon et al., 2006 ). With the functional genomics tools now at our disposal, additional targets for NPH4/ARF7 regulation should not remain elusive for long.

RESPONSE MODULATION VIA SECONDARY PHOTOSENSORY EVENTS

Plants utilize a process known as photosensory adaptation to modify their sensitivity and responsiveness to changes in their light environment that occur throughout diurnal and seasonal cycles ( Galland, 1989 , 1991 ). Photosensory adaptation can be separated into two types of phenomena: 1) sensor adaptation, and 2) effector adaptation. Sensor adaptation was introduced earlier in the context of a potential role for phot1 and phot2 light-induced phosphorylation and the phototropic desensitization process. In this section we will discuss what is known about the molecular properties of effector adaptation processes as they relate to phototropism in Arabidopsis. In particular we will focus on the amplification of signal outputs from the phot1-dependent transduction pathway that lead to enhancement of a basal phototropic response in etiolated seedlings.

By definition photosensory adaptation responses include rapid desensitization components (discussed earlier), as well as slower recovery and responsiveness modulation (enhancement) components ( Galland, 1989 , 1991 ). Recovery of phototropic sensitivity occurs within a few minutes of onset of irradiation, while enhancement takes place over a period of hours ( Zimmerman and Briggs, 1963 ; lino, 1990 ; Poff et al., 1994 ). For example, preirradiation results in a decrease in the lag times for recovery of phototropic sensitivity ( Zimmerman and Briggs, 1963 ; Janoudi et al., 1992 ; Liu and Lino, 1996 ) and enhancement of curvature ( Chon and Briggs, 1966 ; Janoudi and Poff, 1991 ; Liu and lino, 1996 ). Recovery of phototropic sensitivity and response enhancement appear to be mechanistically related and reflect effector rather than sensor adaptation processes ( lino, 1990 ; Poff et al., 1994 ).

phyA Is the Major Effector of phot1-Dependent Phototropism

Although BL can induce phototropic enhancement in monocot ( Blaauw and Blaauw-Jansen, 1970 ; lino, 1988 ) and dicot ( Janoudi and Poff, 1991 ) seedlings, RL can also induce phototropic enhancement ( Figure 5 ) implicating a RL-absorbing receptor in the enhancement response ( lino, 1990 ; Poff et al., 1994 ). Action spectroscopy and partial RL/FR reversibility ( Janoudi and Poff, 1992 ; Liu and lino, 1996 ), together with the absorptive properties of phys ( Butler, 1964 ; Pratt and Briggs, 1966 ; Vierstra, 1983 ), have suggested that one or more phy can mediate phototropic enhancement under both BL alone and BL plus RL conditions ( Liscum and Stowe-Evans, 2000 ; Whippo and Hangarter, 2004 ). Analyses of phy-deficient mutants of Arabidopsis provide compelling support for this hypothesis and indicate that both phyA and phyB ( Table 1 ) function as regulators of phototropic enhancement. In particular, phyA appears to act as the major receptor in low fluence conditions, while phyB dominates under high fluences ( Parks et al., 1996 ; Janoudi et al., 1997a ; Janoudi et al., 1997b ). As already discussed, Han and colleagues have found that phyA activation by RL can inhibit BL-induced internalization of phot1 ( Han et al., 2008 ). This finding, together with the aforementioned photobiological properties, suggest that phyA-dependent enhancement of phototropism could result from more phot1 being retained at the plasma membrane to allow more signal transduction, without actually altering phot1 sensitivity.

Phytochrome-induced enhancement of phot1-dependent phototropism in Arabidopsis.

(A) Three-d-old etiolated seedlings mock-irradiated for 8 h.

(B) Three-d-old etiolated seedlings mock-irradiated for 4 h, then exposed to 4 h of unilateral blue light (λ max = 436 nm, 30 nm half-band; at a fluence rate of 0.1 µmol m -2 s -1 ) from the left.

(C) Three-d-old etiolated seedlings exposed to 4 h of red light (λ max = 660 nm, 30 nm half-band; at a fluence rate of 0.3 µmol m -2 s -1 ) from above, then 4 h of unilateral blue light (λ max = 436 nm, 30 nm half-band; at a fluence rate of 0.1 µmol m -2 s -1 ) from the left.

Phys have also been implicated as upstream modulators of both auxin transport ( Eliezer and Morris, 1980 ; Behringer and Davies, 1992 ; Jensen et al., 1998 ; Shinkle et al., 1998 ) and auxin-regulated gene expression ( Oyama et al., 1997 ; Soh et al., 1999 ; Steindler et al., 1999 ; Tian and Reed, 1999 ; Nagpal et al., 2000 ). While one can certainly imagine how phys could influence auxin transport or response via alteration in phot1 localization, it is worth noting that the transcription of a large subset of genes, in the range of ∼10% of the genome, appears to be regulated by phyA ( Tepperman et al., 2001 ). Direct phyA-dependent transcriptional regulation could provide an additional means to modulate auxin levels in the plant, quite independent from phot function, which does not appear to directly regulate transcription ( Ohgishi et al., 2004 ). By the ability to tightly control the expression of a suite of genes, phyA is able to rapidly deploy genes leading to a cascade in signaling. Given the apparent role of lateral auxin gradients in the establishment and maintenance of phototropic responses ( Went and Thimann, 1937 ; lino, 1990 ; Kaufman et al., 1995 ), and the transcriptional responses likely to result from such gradients ( Stowe-Evans et al., 1998 ; Harper et al., 2000 ; Esmon et al., 2006 ), a phy-dependent increase in auxin responsiveness represents an ideal mechanism by which phototropic enhancement could occur ( Liscum and Stowe-Evans, 2000 ).

Compelling support for this contention has been obtained through studies of the nph4/arf7 mutants. In particular, while nph4/arf7 null mutants are aphototropic in low fluence rate BL ( Liscum and Briggs, 1995 , 1996 ), they retain a strong phototropic response in high fluence rate BL (T. Campbell, E.L. Stowe-Evans, and E. Liscum, unpublished), or other irradiation conditions (e.g., low fluence rate BL plus RL) that stimulate both phot1 activity and significant phy Pr to Pfr photoconversion ( Liscum and Briggs, 1996 ; Stowe-Evans et al., 2001 ). Not only does the action of phyA predominate in the phototropic enhancement response of etiolated wild-type seedlings ( Parks et al., 1996 ; Janoudi et al., 1997a ; Janoudi et al., 1997b ; Stowe-Evans et al., 2001 ), but it also appears to be the major modulatory photoreceptor for recovery of response in the nph4/arf7 background ( Stowe-Evans et al., 2001 ). Together these results indicate that phyA action is able to suppress the deficiency in auxin-dependent gene expression conditioned by the loss of NPH4/ARF7. The simplest hypothesis to explain this phyA-dependent phototropic response in the complete absence of NPH4/ARF7 activity is that another ARF may respond to phyA signaling by activating the expression of genes that NPH4/ARF7 would otherwise activate ( Figure 6 ). Given that NPH4/ARF7 activity appears genetically limiting ( Liscum and Briggs, 1996 ; Stowe-Evans et al., 1998 ), this hypothesis is also consistent with the phyA-dependent phototropic enhancement response in wild-type where the second ARF would stimulate additional gene expression beyond that stimulated by the activity of NPH4/ARF7.

Working models to explain the photochrome A-induced enhancement of phototropin-dependent phototropism in wild-type Arabidopsis seedlings and the recover of response in nph4 mutants lacking the auxin response factor ARF7.

From studies of the nph4/arf7 mutants it appears that phyA-dependent increases in the phototropic response of etiolated hypocotyls occur because of a partial activation of a second ARF ( Stowe-Evans et al., 2001 ). Two obvious models can be developed. Both models assume that when multiple ARFs are expressed in the same cell any one ARF can specifically regulate the expression of auxin-responsive genes involved in a distinct biological phenomenon because of differences in the auxin sensitivities of the different ARFs (Liscum and Reed, 2001). First (A) phyA activation could lead to changes in auxin transport and/or metabolism leading to increases in auxin concentration on the side away from light (red block), above that induced by phot1 activation alone (blue block). Whereas the auxin concentration induced by phot1 action alone would result only in the activation of NPH4/ARF7, the auxin concentration established under both phot1 and phyA activating conditions would lead to the activation of both NPH4/ARF7 and ARFy. Alternatively (B) phyA action could lead to changes in the auxin sensitivity of ARFy. Note shift of ARFy response curve (red line) to lower auxin concentration range as compared to panel A. These models are not mutually exclusive, but each can account for the increase in phototropic response of wild-type seedlings, as well as the partial recovery of response in the nph4/arf7 null mutants.

Models for phyA-Dependent Changes in ARF Activity

Two mechanistic explanations for the aforementioned hypothesis seem most probable. First, phyA action might lead to increased auxin content within the hypocotyl as a result of alterations in auxin transport (basipetal, lateral, or some combination thereof) or metabolism. Hence, any differential auxin accumulation in a phototropically-stimulated hypocotyl induced via a phot1-dependent response pathway would be enhanced, potentially resulting in partial activation of an ARF with a lower sensitivity to auxin ( Figure 6a ). Alternatively, phyA signaling might condition increased auxin sensitivity of a redundant ARF system via changes in expression or activity of that ARF protein ( Figure 6b ).

Relative to the first model it is worth noting that Stone and colleagues ( Stone et al., 2008 ) employed a second-site enhancer screen to identify mutations in a nph4/arf7 -null mutant background that would lead to complete loss of phototropic responsiveness in RL plus BL conditions where phyA activity normally suppresses the aphototropic phenotype observed in BL alone. Of the three enhancer mutations identified the m odifer of a rf7 p henotypes 1 (map1) mutation was shown to be allelic to AUX1 ( Stone et al., 2008 ), a member of a small family of high-affinity auxin influx carriers ( Swarup et al., 2004 ; Yang et al., 2006 ; Kerr and Bennett, 2007 ). The map1/aux1-201 mutation was shown to be a missense allele converting Ala 94 to Val within the second transmembrane span of AUX1 ( Stone et al., 2008 ). While map1/aux1-201 was identified as an enhancer of nph4/arf7 phototropic defects, this aux1 allele, as well as several previously identified missense alleles were shown to also condition subtle but significant reductions in phot1-dependent BL-induced phototropism even in the presence of normal NPH4/ARF7 activity ( Stone et al., 2008 ). These and other results led to the proposal that phyA influences AUX1 activity (and possibly AUX1 mRNA expression) to increase local symplastic auxin concentrations within the elongation zone of the hypocotyl/stem such that activation of another ARF(s) with lower auxin sensitivity leads to enhanced phototropic responsiveness in the presence of NPH4/ARF7 activity and to partial recovery of responsiveness in the absence of NPH4/ARF7 ( Stone et al., 2008 ).

While to date there is no direct experimental evidence in support of the model in which phyA activity increases auxin sensitivity through changes in ARF activity or expression, recent findings with respect to another conditional phototropic phenotype of nph4/arf7 -null mutants suggest this model has merit. It had previously been shown that exposure to ethylene prior to, or concomitant with, exposure to directional BL could, like phyA activation ( Stowe-Evans et al., 2001 ), partially suppress the aphototropic phenotype of nph4/arf7 -null mutants observed in BL alone ( Harper et al., 2000 ). Stone and colleagues ( Stone et al., 2008 ) were able to demonstrate that the combination of a nph4/arf7 mutation with loss-of-function mutations in ARF19 , the most closely related ARF to NPH4/ARF7 ( Remington et al., 2004 ), renders Arabidopsis seedlings incapable of exhibiting BL-induced phot1-dependent phototropism with or without ethylene exposure. Interestingly, nph4/arf7arf19 double mutants still recover BL-induced phototropism when phyA is activated ( Stone et al., 2008 ). These findings demonstrate that ARF19 is sufficient for the ethylene-dependent suppression of nph4/arf7 aphototropism but not the phyA-dependent response. What makes this finding particularly interesting within the context of the model introduced above is the finding that ARF19 mRNA expression is up-regulated in response to ethylene exposure ( Li et al., 2006 ), thus providing an obvious explanation for the ARF19-dependent phenotype ( Stone et al., 2008 ). While genetic support for a similar model of increased ARF activity does not currently exist for the phyA-dependent response, it is intriguing that the map3 mutation (currently uncloned) influences the phyA-response specifically in much the same way the arf19 mutations are specific to the ethylene response ( Stone et al., 2008 ).

Redundant ARF function could also be influenced by phyA through promotion of Aux/IAA degradation. It is now well established that Aux/IAA proteins are targeted for 26S proteasome-dependent degradation by the CRL1/SCF TIR1 E3 ubiquitinligase complex ( Gray and Estelle, 2000 ; Ramos et al., 2001 ; Schwechheimer et al., 2001 ; Dharmasiri et al., 2005 ; Kepinski and Leyser, 2005 ; Quint and Gray, 2006 ; Dos Santos Maraschin et al., 2009 ). In yeast and flies, many proteins targeted by a CRL1/SCF complex are first phosphorylated ( Patton et al., 1998 ; Maniatis, 1999 ; Koepp et al., 2001 ). Interestingly it has been shown that phyA can interact with and phosphorylate Aux/IAA proteins in vitro ( Colon-Carmona et al., 2000 ). Thus it seems plausible that phyA could influence the auxin sensitivity of a redundant ARF(s) by promoting, through phosphorylation, ubiquitylation and subsequent degradation of an Aux/IAA protein(s) that normally inhibits the activity of the redundant ARF(s). Although this possibility remains untested at present, protein turnover does appear to be at least one of the components of phyA-dependent recovery of phototropism in nph4/arf7 mutants since nph4/arf7axr1 double mutant seedlings fail to exhibit any phototropic response (E. L. Stowe-Evans, R. M. Harper, and E. Liscum, unpublished). AXR1 ( Table 1 ) encodes one of the two components (the other being ECR1) of a heterodimeric ubiquitin-E1-like enzyme that functions upstream of the CRL1/SCF TIR1 complex ( del Pozo and Estelle, 1999 ; Gray and Estelle, 2000 ). Not surprisingly, axr1 single mutants also exhibit impaired phototropic responses ( Watahiki et al., 1999 ; Yang et al., 2004 ).

ECOLOGICAL AND EVOLUTIONARY SIGNIFICANCE OF PHOTOTROPISM

In contrast to the controlled and relatively simply environmental conditions plants find themselves in under laboratory or growth chamber conditions, growth in natural habitats results in exposure to large variations in all sorts of environmental stimuli on temporal and spatial scales. One of the challenges that plants have toadapt to is the fluctuation in light quality and quantity through the course of the day, as well as by surrounding vegetation. Given the ubiquitous nature of phototropism within the plant kingdom, and its potential to dramatically increase the photosynthetic foraging capacity of a plant, it seems obvious to expect that the genes controlling this response have been under positive selective pressure during the evolution of different land plants. Yet, despite the potential ecological and evolutionary significance of phototropism, until recently no one had even asked: If two plants are growing in a shaded or light-limited environment, would the one exhibiting a stronger phototropic response have an adaptive advantage over the one with a weaker response? Why hadn't such a study been done until recently; could it be that such a test sounds easy but in fact has been quite difficult to design and execute? Just by the way the aforementioned question is posed - “if…the one exhibiting a stronger phototropic response has an adaptive advantage over the one with a weaker response?” - it is clear that this question has been extremely difficult to ask since it requires that one has access to two plants, presumably within the same species, with dramatically different phototropic potentials. With the identification of mutants in Arabidopsis that exhibit altered phototropic response the aforementioned question could finally be addressed.

Galen and colleagues ( Galen et al., 2004 ) examined the fitness of phot1 , phot2 and nph3 mutants in comparison to wild-type plants and found that each of these loci imparts a significant fitness advantage to young Arabidopsis seedlings that are germinated under simulated and natural canopy litter conditions. In particular, it was observed that phot1, phot2 and nph3 mutants had reduced lifetime fitness compared to wild-type, with phot1 and NPH3 contributing most prominently to fitness during seedling germination and emergence, and phot2 contributing post emergence of the seedling from the soil ( Galen et al., 2004 ). Given the known fluence rate sensitiveness of phot1 and phot2 these observations were not, in hindsight, that surprising. Consistent with these findings under natural environmental conditions, Takemiya and colleagues ( Takemiya et al., 2005 ) found that phot1 and phot2 promote at least three-fold higher biomass production in growth chamber-grown plants given RL sufficient to saturate the photosynthetic response but supplemented with low fluence rate BL conditions, as compared to plants grown in RL alone. Both of these studies indicate that phots provide adaptive value with respect to establishment and growth of plants, yet they do not address how phot activity impacts physiology to derive this adaptive value.

Negative phototropism and positive gravitropism direct directional growth of plant roots deeper in the soil for water and nutrients. A plants water status reflects the balance between absorption of water through the roots and transpiration through the stomatal pores in the leaves. Interestingly, both negative root phototropism (leading to increased access to soil-borne water) and stomatal opening (leading to water loss) are mediated by phots. How these two BL-induced spatially separated processes are coordinated is largely a mystery. However, it appears that phot1 function confers an adaptive advantage to plants growing under water-limited conditions ( Galen et al., 2004 ). While the role of phot1-mediated stomatal opening was not specifically addressed, the investigators showed that roots of phot1 -null mutants exhibited largely random growth patterns compared to wild-type or PHOT1 transgene-complemented phot1 mutant plants, leading to very shallow root growth relative to soil depth. Thus in dry soil conditions roots of phot1 mutant plants simply do not penetrate the soil deep enough to access the limited water ( Galen et al., 2007b ; Galen et al., 2007a ). Interestingly the aberrant root phenotypes of the phot1 mutant are accentuated in dry versus wet conditions suggesting that there is interplay between drought and phot1 sensing-response systems ( Galen et al., 2007b ; Galen et al., 2007a ).

The potential fitness advantages of maintaining phototropic responsiveness may be further increased by the co-opting of multiple photoreceptor systems in the modulation of phototropic response. For example, if phototropism was an all-or-nothing response, controlled solely by the differential activation of phot1 or phot2 a seedling could be “misled” into bending towards an unsuitable source of light. It makes intuitive sense that the action of phys and crys as modulators of the phot signal-output could be beneficial for a plant, allowing it to select forage areas with the highest photosynthetic light quality. One clear example of the interdependency, as well as complexity, of receptor systems regulating phototropism is illustrated by the responses of phyA phyB double mutants of Arabidopsis to unidirectional narrow-band BL. Under low to moderate fluences of BL etiolated phyAphyB seedlings exhibit < 5° total curvature, demonstrating that the magnitude of phototropic curvature under such conditions is almost completely determined by phy ( Janoudi et al., 1997b ), although phot1 is absolutely required for perception of the directional stimulus ( Liscum and Briggs, 1995 ; Sakai et al., 2000 ). The story is complicated further under high fluence conditions, because phyAphyB seedlings retain a phototropic response largely equivalent in magnitude to that of wild-type ( Janoudi et al., 1997b ). Hence, under low fluence conditions phot1-activated processes dictate the direction of growth, while phyA and phyB determine the magnitude of the curvature response. In contrast, under high fluence conditions phot2 likely functions as the directional BL sensor ( Sakai et al., 2001 ) and its activity, or that of another unidentified secondary receptor(s), determines the magnitude of the response. One can envision utilizing the natural variation that exists within the Arabidopsis germplasm as a tool to address this, as well as additional unresolved questions about phototropism.

The work done to date in Arabidopsis, and availability of mutants that disrupt various components of the phototropic response, provides an ideal system in which to examine the relationship between phototropism and fitness under natural, as well as experimentally modified, growth conditions. It is clear that many of the advances in our understanding of phototropism in the coming decade will require not only continued genetic, biochemical, and molecular approaches, but also their coupling to approaches aimed at addressing larger ecological and evolutionary questions — questions undoubtedly now more easily addressed because of the tools provided by genetic studies of phototropism in Arabidopsis.

Acknowledgements

The authors would like to thank National Science Foundation for funding the research being conducted in the Liscum Laboratory through grants no. IBN0415970 and IOS-0817737. U.V.P was supported by MU-Monsanto Graduate Fellowship and Multiagency Maize training grant. R.B.C was supported by Monsanto and MU Graduate School Fellowships.

Citation: Pedmale U.V., Celaya R.B., and Liscum E. (2010) Phototropism: Mechanism and Outcomes. The Arabidopsis Book 8:e0125. doi:10.1199/tab.0125

elocation-id: e0125

First published on August 31, 2010

This chapter is an updated version of a chapter originally published on April 4, 2002, doi: http://dx.doi.org/10.1199/tab.0042

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Investigating Phototropism & Geotropism ( OCR A Level Biology )

Revision note.

Biology & Environmental Systems and Societies

Investigating Phototropism & Geotropism

Phototropism in plant shoots.

• Plant shoots are positively phototropic , meaning they grow towards light
• This ensures they maximise the amount of light they can absorb for photosynthesis
• Many of the experiments were conducted using coleoptiles (a sheath that surrounds the young growing shoot of grass plants)
• Darwin discovered that removing the tip of a coleoptile stopped the phototropic response to a unidirectional light source (light coming from one side) from occurring
• To ensure this was not simply due to the wounding caused to the plant, he covered the tip of a coleoptile with an opaque cover or 'cap' instead, to block out the light. This also stopped the phototropic response from occurring, showing that the tip of the coleoptile was responsible for detecting light
• Boysen-Jensen found that if he replaced the cut tip back on top of the coleoptile and inserted a gelatin block as a barrier in between, the phototropic response was restored
• This showed that the stimulus for growth was a chemical (hormone) , which was able to travel through the gelatin block
• Bosen-Jensen then inserted a mica barrier (mica is impermeable to chemicals) halfway through the coleoptile just below the tip, first on the lit side and then on the shaded side
• When the mica barrier was inserted into the lit side , the phototropic response occurred
• When the mica barrier was inserted into the shaded side , the phototropic response did not occur
• This confirmed that the stimulus for growth was a chemical (hormone) and showed that it was produced at the tip , before travelling down the coleoptile on the side opposite to the stimulus (i.e. the shaded side)
• It also showed that the stimulus acted by causing growth on the shaded side (rather than inhibiting growth on the lit side)
• Paál cut off the tip of a coleoptile and then replaced it off-centre in the dark
• The side of the coleoptile that the tip was placed on grew more than the other side, causing the coleoptile to curve (similar to a phototropic response)
• This showed that, in the light, the phototropic response was caused by a hormone diffusing through the plant tissue and stimulating the growth of the tissue
• Went placed the cut tip of a coleoptile on a gelatin block, allowing the hormones from the tip to diffuse into the block
• The block was then placed on the coleoptile, off-centre and in the dark
• As in Paál's experiment, the side of the coleoptile that the block was placed on grew more than the other side, causing the coleoptile to curve
• The greater the concentration of hormone present in the block, the more the coleoptile curved

Four historical phototropism experiments were conducted to investigate the process by which phototropism occurs

Controlling growth by elongation

• Indole-3-acetic acid (IAA), which is an auxin , is a specific growth factor found in plants
• IAA is synthesised in the growing tips of roots and shoots (i.e. in the meristems , where cells are dividing )
• IAA coordinates phototropisms in plants by controlling growth by elongation
• IAA molecules are synthesised in the meristem and pass down the stem to stimulate elongation growth
• The IAA molecules activate proteins in the cell wall known as expansins , which loosen the bonds between cellulose microfibrils , making cell walls more flexible
• The cell can then elongate

The phototropic mechanism

• Phototropism affects shoots and the top of stems
• The concentration of IAA determines the rate of cell elongation within the region of elongation
• If the concentration of IAA is not uniform on either side of a root or shoot then uneven growth can occur
• It is described as positive because growth occurs towards the stimulus
• Experiments have shown that IAA moves from the illuminated side of a shoot to the shaded side
• The higher concentration of IAA on the shaded side of the shoot causes a faster rate of cell elongation
• This causes the shoot to bend towards the light

Higher concentrations of IAA on the shaded side increases the rate of cell elongation so that the shaded side grows faster than the illuminated side

Geotropism in plant shoots and roots

• Gravity affects both plant shoots and roots , but in different ways
• Gravity modifies the distribution of IAA so that it accumulates on the lower side of the shoot
• As seen in the phototropic response, IAA increases the rate of growth in shoots , causing the shoot to grow upwards
• In roots, higher concentrations of IAA results in a lower rate of cell elongation
• The IAA that accumulates at the lower side of the root inhibits cell elongation
• As a result, the lower side grows at a slower rate than the upper side of the root
• This causes the root to bend downwards

Practical: investigating the effect of IAA on root growth

• Experiments can be carried out to investigate the effect of IAA on root growth in seedlings
• Seedlings (of the same age and plant species)
• Cutting tile
• Light source
• Lightproof container
• Blocks of agar (all the same volume)
• Use the scalpel to cut a 1cm section from the root tip of each seedling
• Mark the root tips at 2mm marks
• The water helps to keep the plant tissue alive
• Remove the ends of the root tips using the scalpel
• Transfer root cuttings with the end removed to an agar block
• A uniform light source is present
• Transfer intact root tips to an agar block
• A light-proof container is placed over the seedlings to prevent light from entering
• Apply a directional light source to one side of the root tips
• Leave all the roots in their treatment conditions for 3 hours
• Use the 2mm marker lines to determine if growth has occurred
• Note if the growth has been even on both sides

Results and analysis

• IAA is synthesised in the root tips so removing them means that no IAA is produced
• There is no inhibition of cell elongation
• There is an equal concentration of IAA on both sides of the root tip
• The inhibition of cell elongation is equal on both sides of the root tip
• The roots do not grow as long as those in group A due to the presence of IAA
• There is a greater concentration of IAA on the shaded side
• This results in greater inhibition of cell elongation on the shaded side
• So the illuminated side grows at a faster rate
• The roots bend away from the light – negative phototropism

Limitations

• Certain genotypes may be more prone to bending or have slightly different sensitivities to IAA
• If the root is mishandled the marks can be altered, which will affect the results
• Only general comments can be made about whether there has been even growth on both sides of the roots

The different treatments produce different levels of growth in the root tips. The IAA molecules inhibit cell elongation in roots

You may sometimes see IAA simply referred to as auxin. IAA is a particular type of auxin, which is a more general term for a particular group of plant hormones.

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Author: Alistair

Alistair graduated from Oxford University with a degree in Biological Sciences. He has taught GCSE/IGCSE Biology, as well as Biology and Environmental Systems & Societies for the International Baccalaureate Diploma Programme. While teaching in Oxford, Alistair completed his MA Education as Head of Department for Environmental Systems & Societies. Alistair has continued to pursue his interests in ecology and environmental science, recently gaining an MSc in Wildlife Biology & Conservation with Edinburgh Napier University.

Student Sheet 8 – Phototropism: the Response of Seedlings to Light

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Seedlings growing on a windowsill will often bend towards the window as they respond to light – phototropism. But what exactly are the seedlings responding to? Which wavelengths of light stimulate the phototropic response?

The technique for this experiment helps students design an investigation to find out more about this tropic response. Students germinate seedlings in enclosed containers, with a coloured filter over the small hole allowing light in. Students predict which seedlings will demonstrate phototropism, and which will remain unaffected.

The students’ sheet contains a number of suggestions for further experiments, while the  worksheet outlines the basic technique.

Download the student sheets and teachers’ notes from the links on the right.

What's included?

• SAPS Sheet 8 - The response of seedlings to light - Student Notes
• SAPS Sheet 8 - The response of seedlings to light - Student Sheet
• SAPS Sheet 8 - The response of seedlings to light - Technical and Teaching Notes
• Plant growth
• Plant reproduction
• Plant responses

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• Investigating Thigmotropism
• Tackling tropisms: gravitropism and phototropism

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Understanding phototropism: from Darwin to today

Affiliation.

• 1 Division of Biological Sciences, 109 Christopher S. Bond Life Sciences Center, University of Missouri, Columbia, MO 65211, USA.
• PMID: 19357428
• DOI: 10.1093/jxb/erp113

Few individuals have had the lasting impact on such a breadth of science as Charles Darwin. While his writings about time aboard the HMS Beagle, his study of the Galapagos islands (geology, fauna, and flora), and his theories on evolution are well known, less appreciated are his studies on plant growth responses to a variety of environmental stimuli. In fact, Darwin, together with the help of his botanist son Francis, left us an entire book, 'The power of movements in plants', describing his many, varied, and insightful observations on this topic. Darwin's findings have provided an impetus for an entire field of study, the study of plant tropic responses, or differential growth (curvature) of plant organs in response to directional stimuli. One tropic response that has received a great deal of attention is the phototropic response, or curvature response to directional light. This review summarizes many of the most significant advancements that have been made in our understanding of this response and place these recent findings in the context of Darwin's initial observations.

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9.1: Tropisms

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• Page ID 123942

• Teresa Friedrich Finnern
• Norco College

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Learning Objectives

• Distinguish among phototropism, gravitropism, hydrotropism, and thigmotropism.
• Discuss the adaptive value of tropisms.
• Describe the mechanism of phototropism in shoots.
• Describe the mechanism of gravitropism in shoots and roots.
• Distinguish among thigmotropism, thigmonastic movements, and thigmomorphogenesis.

A tropism is directional growth in response to a stimulus. A positive tropism occurs when a plant (or a part of the plant) grows towards the stimulus, and a negative tropism is growth away from the stimulus.

Phototropism is directional growth in response to light (Figure \(\PageIndex{1}\)). (More generally, photomorphogenesis is the growth and development of plants in response to light.) Stems are positively phototropic, and roots are typically negatively phototropic. Gravitropism is directional growth in response to gravity. Stems are negatively gravitropic, and roots are positively gravitropic. The adaptive value of these tropisms is clear. Stems growing upward and/or toward the light will be able to expose their leaves so that photosynthesis can occur. Roots growing downward and/or away from light are more likely to find the soil, water, and minerals they need. Plants can also grow directionally in response to water ( h ydrotropism ) and touch ( thigmotropism ).

Phototropism in Shoots

Plants can detect different characteristics of light, such as quantity, quality, duration, and direction. They can tell the time of day and time of year by sensing and using various wavelengths of sunlight. Plants are generally capable of detecting and responding to at least three wavelengths of light: blue light, red light, and far-red light . The different wavelengths are detected by different photoreceptors (Figure \(\PageIndex{2}\)​​​​​), an example of which are phototropins.

The Shoot Tip Detects Light and Induces Phototropism

In their 1880 treatise The Power of Movements in Plants , Charles Darwin and his son Francis first described phototropism as the bending of seedlings toward light. The Darwins used grass seedlings for some of their experiments. When grass seeds germinate, the primary leaf pierces the seed coverings and the soil while protected by the coleoptile , a hollow, cylindrical sheath that surrounds it (Figure \(\PageIndex{3}\) ).

Once the seedling has grown above the surface, the coleoptile stops growing and the primary leaf pierces it. If they placed an opaque cover over the tip, phototropism failed to occur even though the rest of the coleoptile was illuminated from one side. However, when they buried the plant in fine black sand so that only its tip was exposed, there was no interference with the tropism — the buried coleoptile bent in the direction of the light (Figure \(\PageIndex{4}\) ). In conclusion, light was perceived by the tip of the plant (the apical meristem), but that the response (bending) took place in a different part of the plant. The signal had to travel from the apical meristem to the base of the plant.

We now know that phototropism is a response to blue wavelengths of light. The detection of light in the apical meristem occurs via phototropins called phot1 and phot2 , which specifically detect blue light (Figure \(\PageIndex{5}\) ). The aptly-named phototropins are protein-based receptors responsible for mediating the phototropic response. Like all plant photoreceptors, phototropins consist of a protein portion and a light-absorbing portion, called the chromophore . Together, the two are called a chromoprotein. In phototropins, the chromophore is a covalently-bound molecule of flavin; hence, phototropins belong to a class of proteins called flavoproteins.

The Hormone Auxin from the Shoot Tip Stimulates Elongation on the Shaded Side of the Stem

In 1913, the Danish plant physiologist Peter Boysen-Jensen demonstrated that a chemical signal produced in the plant tip was responsible for the bending at the base. He cut off the tip of a seedling, covered the cut section with a layer of gelatin, and then replaced the tip. The seedling bent toward the light when illuminated. However, when impermeable mica flakes were inserted between the tip and the cut base, the seedling did not bend. A refinement of the experiment showed that the signal traveled on the shaded side of the seedling. When the mica plate was inserted on the illuminated side, the plant did bend towards the light. When a horizontal incision was made on the illuminated side and the mica inserted in it, phototropism was normal (Figure \(\PageIndex{6}\) ). Therefore, the chemical signal was a growth stimulant because the phototropic response involved faster cell elongation on the shaded side than on the illuminated side.

We now know that auxin is the chemical signal that accumulates and stimulates elongation on shaded side of coleoptile. H. W. Went placed a coleoptile that has previously been illuminated from one side on two separated agar blocks. The block on the side that had been shaded accumulated almost twice as much auxin as the block on the previously lighted side (Figure \(\PageIndex{7}\) ).

Auxin stimulates cell elongation on the shady side of the stem through a process called the acid growth hypothesis : Auxin causes cells to activate proton pumps, which then pump protons out of the cells and into the space between the plasma membrane and the cell wall. The movement of protons into the extracellular space does two things:

• The lower pH activates expansin , which breaks the links between the cellulose fibers in the cell walls, making them more flexible.
• The high concentration of protons causes sugars to move into the cell, which then creates an osmotic gradient where water moves into cell causing the cell to expand.

Phototropism in Roots

Although roots are underground, they can be exposed to light directly as well. Not only can light penetrate up to a few centimeters in the upper layers of some soils, the plant itself can also guide light through the stem to the roots. Additionally, roots can also be exposed to light shortly after germination in the top layer of the soil or because cracks in the soil emerge that trigger a phototropic reaction. Negative phototropism in roots may be evolutionarily advantageous because it increases root efficiency and enhances seedling survival under dry conditions. As in shoots, phototropin 1 is involved in root phototropism. Directional auxin transport and an auxin gradient are associated with root phototropsim, but it is unclear whether they mediate the process.

Gravitropism

Whether or not they germinate in the light or in total darkness, shoots usually sprout up from the ground, and roots grow downward into the ground. A plant laid on its side in the dark will send shoots upward when given enough time. Gravitropism also involves the unequal distribution of auxin.

When an oat coleoptile tip is placed on two separated agar blocks, as shown here, there is no difference in the auxin activity picked up by the two blocks. When the preparation is placed on its side, however, the lower block accumulates twice as much auxin activity as the upper block. Under natural conditions, this would cause greater cell elongation on the underside of the coleoptile and the plant would bend upward (Figure \(\PageIndex{8}\)).

Specialized amyloplasts called statoliths settle downward in response to gravity. Statoliths are found in the inner part of a stem's cortex (the starch sheath) and in the the central column of the root cap (columella). When a plant is tilted, the statoliths drop to the new bottom cell wall. A few hours later, the shoot or root will show growth in the new vertical direction (Figure \(\PageIndex{9}\)).

The mechanism that mediates gravitropism is reasonably well understood. When amyloplasts settle to the bottom of the gravity-sensing cells in the root or shoot, they physically contact the endoplasmic reticulum (ER), causing the release of calcium ions from inside the ER. Calcium may be released by ion channels sensitive to mechanical stimulation. This calcium signaling in the cells causes auxin transport proteins ( PIN proteins ) to redistribute to the underside of the cell leading to the polar transport of auxin to the bottom of the cell. In roots, a high concentration of indoleacetic acid (IAA) inhibits cell elongation. The effect slows growth on the lower side of the root, while cells develop normally on the upper side. IAA has the opposite effect in shoots, where a higher concentration at the lower side of the shoot stimulates cell expansion, causing the shoot to grow up. After the shoot or root begin to grow vertically, the amyloplasts return to their normal position. Another hypotheses—involving the entire cell in the gravitropism effect—have been proposed to explain why some mutants that lack amyloplasts may still exhibit a weak gravitropic response.

Plant Tropisms in Space

Considering the fundamental role of plants in producing fresh food and recycling of air and water, plant tropism research is critical for advancing plant-based life support systems in space. Understanding of the relative strengths of the different root tropisms would be needed to properly guide root growth by technological means, as the gravity vector is absent in space. For example, by exposing roots in microgravity to blue light, they could be induced to develop away from light toward the growth medium. Furthermore, the possibility of performing explorative experiments in the space environment, together with the development of new technologies, is crucial to pave the way toward the goal of deepening our fundamental understanding of plant tropisms and their underlying molecular networks on Earth.

Modified by Melissa Ha from Muthert, L., Izzo, L. G., van Zanten, M., & Aronne, G. (2020). Root Tropisms: Investigations on Earth and in Space to Unravel Plant Growth Direction . Frontiers in plant science , 10 , 1807. https://doi.org/10.3389/fpls.2019.01807 . CC BY

Hydrotropism

Water acquisition is an important function of plant roots. Because water availability in the soil is often spatially and temporally patchy, roots of many species can exert directional root growth toward water; i.e., positive hydrotropism. The underlying mechanisms of hydrotropism are still being researched. Gravitropism is often dominant over hydrotropic responses, making it difficult to study hydrotropism in isolation. In contrast to phototropism and gravitropism, hydrotropism does not result from an auxin gradient resulting from directional auxin transport. However, auxin still appears to play a role in signaling hydrotropism.

Thigmotropism, Thigmomorphogensis, and Thigmonastic Movements

The shoot of a pea plant winds around a trellis while a tree grows on an angle in response to strong prevailing winds. These are examples of how plants respond to touch or wind.

The movement of a plant subjected to constant directional pressure is called thigmotropism , from the Greek words thigma meaning “touch,” and tropism implying “direction.” Tendrils are one example of plants displaying positive thigmotropism (Video \(\PageIndex{1}\)). The meristematic region of tendrils is very touch sensitive; light touch will evoke a quick coiling response. Cells in contact with a support surface contract, whereas cells on the opposite side of the support expand. Application of jasmonic acid is sufficient to trigger tendril coiling without a mechanical stimulus.

Video \(\PageIndex{1}\): This video shows an example of positive thigmotropism in morning glory plants, which require a support structure of some type to grow optimally. The time lapse images were taken at 10 minute intervals. This video has no sound. Here is a description: The morning glory stems (which are modified as tendrils) grow in a counterclockwise pattern, widening their radius with each rotation. When they encounter one of the two wooden stakes on either side of the plant, grow in a tight coil around it.

Plant roots exhibit negative thigmotropism when contacting obstacles in the soil. When plant roots encounter an obstacle in their growth path, the root first continues growing in the same direction until it slips sideways. The root bends away from the stimulus and then bends again in the opposite direction, creating a step-like shape. Note that at this point the root "side stepped" the obstacle and is now continuing to grow in the original direction. If the root contacts another part of the obstacle, the same bending pattern will occur. Thigmotropism in roots may be mediated by calcium, but other signaling mechanisms have also been proposed. Following contact, the calcium concentration in the root cap is greater than that of surrounding regions. (Under regular conditions, calcium concentration in the root cap is lower.) Ultimately, the directional transport of auxin results in an auxin gradient. When touching an obstacle during downward growth, the root bends and auxin accumulates at the higher (concave) side of the root suppressing elongation. Greater elongation on the convex (lower) side of the root causes it to bend away from the obstacle.

Thigmomorphogenesis is a slow developmental change in the shape of a plant subjected to continuous mechanical stress. When trees bend in the wind, for example, growth is usually stunted and the trunk thickens. Strengthening tissue, especially xylem, is produced to add stiffness to resist the wind’s force. Researchers hypothesize that mechanical strain induces growth and differentiation to strengthen the tissues. Ethylene and jasmonate are likely involved in thigmomorphogenesis.

A thigmonastic movement is a touch response independent of the direction of stimulus. In the Venus flytrap, two modified leaves are joined at a hinge and lined with thin fork-like tines along the outer edges (Video \(\PageIndex{2}\)). Tiny hairs are located inside the trap. When an insect brushes against these trigger hairs, touching two or more of them in succession, the leaves close quickly, trapping the prey. Glands on the leaf surface secrete enzymes that slowly digest the insect. The released nutrients are absorbed by the leaves, which reopen for the next meal.

Video \(\PageIndex{2}\): This video below shows an example of thigmonastic movements in a Venus flytrap. There is no only ambient sound in this video and no speaking. Here is a description. At 0:08, a fly enters the taco-shaped trap of the Venus flytrap. It escapes before the tines (prongs) interlock, as shown in a slow-motion replay. At 0:42, another fly crawls into the trap. It crawls around a bit before the trap closes, locking it inside.

Another example of thigmonastic movement occurs in the sensitive plant ( Mimosa pudica ). Its leaflets and leaves retract in response to touch, and this is thought to be an adaptation that deters herbivores (Video \(\PageIndex{3}\)).

Video \(\PageIndex{3}\): The leaflets of the sensitive plant retract when touched. This video has no speaking, but there are natural sounds (such as birds) in the background and laughing when the leaflets retract.

Attributions

Curated and authored by Melissa Ha using the following sources:

• 16.2F: Tropisms from Biology by John. W. Kimball (licensed CC-BY )
• 30.6 Plant Sensory Systems and Responses from Biology 2e by OpenStax (licensed CC-BY ). Access for free at openstax.org .
• Plant Hormones and Sensory Systems by Biology 1520 Introduction to Organismal Biology (licensed CC-BY-NC-SA )
• Muthert, L., Izzo, L. G., van Zanten, M., & Aronne, G. (2020). Root Tropisms: Investigations on Earth and in Space to Unravel Plant Growth Direction . Frontiers in plant science , 10 , 1807. https://doi.org/10.3389/fpls.2019.01807 . (licensed CC-BY )

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Experiments to Show Phototropism (A-level Biology)

Experiments to show phototropism, investigating plant responses, phototropism experiment.

We can investigate phototropism in plants using the following method. This will allow us to see the response of plants to light.

• Use 9 plant shoots. Plant all the shoots in individual plant pots, with the same soil type in each pot. Ensure that all the shoots are roughly the same height.
• Wrap some of the shoots in foil. Now, wrap the tips of 3 shoots in foil. For another 3 shoots, wrap the base of the shoots in foil. Leave the final 3 shoots without foil.
• Place the shoots under a light source. Place all 9 shoots under a light source for 2 days. Ensure that the shoots are equally exposed to the light source. Control the temperature and moisture over the course of the experiment.
• Interpret the results after 2 days. After the shoots have been exposed to the light source for 2 days, interpret the results. The shoots with covered tips will not grow towards the light source, but the other 6 shoots will.
• Record the amount of growth. To get accurate, quantitative results, you can measure the growth of each shoot and write down the direction of growth.

Phototropism is the growth response of a plant towards or away from light.

There are several experiments that can be done to demonstrate phototropism in plants, including: The experiment with potted plants, where a plant is grown in a pot and then covered on one side with a black paper. The plant will grow towards the light source The experiment with grass seedlings, where grass seedlings are grown in a tray and exposed to light from one side. The seedlings will grow towards the light source The experiment with Avena seedlings, where Avena seedlings are grown in a test tube and exposed to light from one side. The seedlings will bend towards the light source The experiment with coleoptiles, which are the protective sheaths surrounding grass shoots. Coleoptiles are placed in a darkened room and exposed to light from one side. The coleoptiles will bend towards the light source

Phototropism works in plants through the unequal distribution of auxin, a hormone responsible for promoting growth in plants. When light is shone on one side of the plant, it stimulates the cells on that side to produce more auxin. This causes the cells on that side to grow faster, bending the plant in the direction of the light.

The knowledge of phototropism has practical implications for agriculture and horticulture, as it can be used to increase crop yields and improve the growth of ornamental plants. By manipulating the light exposure of plants, farmers and horticulturists can encourage the growth of plants in a desired direction, leading to more efficient use of space and resources.

The study of phototropism is important for future careers in Biology because it provides a fundamental understanding of plant growth and development. This knowledge is essential for careers in areas such as botany, plant sciences, agriculture, horticulture, and other related fields, where an understanding of plant growth is crucial.

The study of phototropism is approached in A-level Biology through a combination of theoretical and practical work. Students learn about the mechanisms of phototropism, the role of hormones in plant growth, and the factors that affect the direction of growth. They also conduct practical experiments to demonstrate phototropism in plants and gain hands-on experience in plant growth and development.

Some of the factors that can affect the direction of phototropism in plants include: The intensity of the light The duration of the light exposure The wavelength of the light The age of the plant The species of the plant

Phototropism can be used to grow plants in space as it provides a way to orient the plants towards a light source, even in a low-gravity environment. This can be important for growing food crops or for conducting experiments on plant growth in space.

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CIE 1 Cell structure

Roles of atp (a-level biology), atp as an energy source (a-level biology), the synthesis and hydrolysis of atp (a-level biology), the structure of atp (a-level biology), magnification and resolution (a-level biology), calculating cell size (a-level biology), studying cells: confocal microscopes (a-level biology), studying cells: electron microscopes (a-level biology), studying cells: light microscopes (a-level biology), life cycle and replication of viruses (a-level biology), cie 10 infectious disease, bacteria, antibiotics, and other medicines (a-level biology), pathogens and infectious diseases (a-level biology), cie 11 immunity, types of immunity and vaccinations (a-level biology), structure and function of antibodies (a-level biology), the adaptive immune response (a-level biology), introduction to the immune system (a-level biology), primary defences against pathogens (a-level biology), cie 12 energy and respiration, anaerobic respiration in mammals, plants and fungi (a-level 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techniques (a-level biology), the innate immune response (a-level biology), edexcel a 7: run for your life, edexcel a 8: grey matter, inhibitory synapses (a-level biology), synaptic transmission (a-level biology), the structure of the synapse (a-level biology), factors affecting the speed of transmission (a-level biology), myelination (a-level biology), the refractory period (a-level biology), all or nothing principle (a-level biology), edexcel b 1: biological molecules, inorganic ions (a-level biology), edexcel b 10: ecosystems, nitrogen cycle: nitrification and denitrification (a-level biology), the phosphorus cycle (a-level biology), nitrogen cycle: fixation and ammonification (a-level biology), introduction to nutrient cycles (a-level biology), edexcel b 2: cells, viruses, reproduction, edexcel b 3: classification & biodiversity, edexcel b 4: exchange and transport, edexcel b 5: energy for biological processes, edexcel b 6: microbiology and pathogens, edexcel b 7: modern genetics, 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homeostasis, the resting potential (a-level biology), ocr 5.1.2 excretion, ocr 5.1.3 neuronal communication, hyperpolarisation and transmission of the action potential (a-level biology), depolarisation and repolarisation in the action potential (a-level biology), ocr 5.1.4 hormonal communication, ocr 5.1.5 plant and animal responses, ocr 5.2.1 photosynthesis, ocr 5.2.2 respiration, ocr 6.1.1 cellular control, ocr 6.1.2 patterns of inheritance, ocr 6.1.3 manipulating genomes, ocr 6.2.1 cloning and biotechnology, ocr 6.3.1 ecosystems, ocr 6.3.2 populations and sustainability, related links.

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