does radiation affect plant growth experiment

Electromagnetic Fields Impact Tree and Plant Growth

Feb 17, 2018 | 0 comments

Electromagnetic Fields, Tree & Plant Growth

Research has documented crown damage in trees from the radiation from cell towers and scientific reviews show that plants are sensitive. 

Electromagnetic (EMF) frequencies have been found to alter the growth and development of plants.  Studies on wireless EMF frequencies have found physiological and morphological changes , increased micronuclei formation , altered growth as well as adverse cell characteristics such as thinner cell walls and smaller mitochondria.  Plants perceive and respond to electromagnetic fields . 

A field study that monitored over 100 trees for 9 years entitled ​​Radiofrequency radiation injures trees around mobile phone base stations published in Science of the Total Environment found a high level of damage to trees in the vicinity of phone masts  ( Waldmann-Selsam 2016) . The authors conclude that “deployment has been continued without consideration of environmental impact.”

Images and Documentation 

• The 2021 Report “Tree damage caused by mobile phone base stations 2021″ 
• The 2017 Report “Tree damage caused by mobile phone base stations An observation guide” that documents crown damage in trees in the line of sight of mobile phone base stations. 
• Download the 104-page brochure “Tree Damage Caused by Radiofrequency Radiation) from Dr. Waldmann Selsam  that has images of the tree damage and explains the effects using exemplary observations from the period 2005 to 2021. ( PDF in German here )

More Research

A study on Aspen trees near Lyons, Colorado entitled “Adverse Influence of Radio Frequency Background on Trembling Aspen Seedlings” published in the International Journal of Forestry found adverse effects on growth rate and fall anthocyanin production, concluding that “results of this preliminary experiment indicate that the RF background may be adversely affecting leaf and shoot growth and inhibiting fall production of anthocyanins associated with leaf senescence in Trembling Aspen seedlings. These effects suggest that exposure to the RF background may be an underlying factor in the recent rapid decline of Aspen populations. Further studies are underway to test this hypothesis in a more rigorous way.” 

An analysis of 45 peer-reviewed scientific publications (1996–2016) on changes in plants due to the non-thermal RF-EMF effects from mobile phone radiation entitled “ Weak radio frequency radiation exposure from mobile phone radiation on plants ” concludes, “Our analysis demonstrates that the data from a substantial amount of the studies on RF-EMFs from mobile phones show physiological and/or morphological effects (89.9%, p < 0.001). Additionally, our analysis of the results from these reported studies demonstrates that the maize, roselle, pea, fenugreek, duckweeds, tomato, onions and mungbean plants seem to be very sensitive to RF-EMFs. Our findings also suggest that plants seem to be more responsive to certain frequencies….” 

In 2021, the Tree Care Industry Magazine  published an article on the hazards faced by tree care worker s in increasing proximity to the ever-expanding universe of antennas, both regular radio and 5G/wireless. 

Read Beware the Dangers from AM Radio and 5G Transmission Sites ( PDF )

Thousands of new 5G “small” cell towers are being built in residential neighborhoods posing risks to tree canopy. 

Antennas are going on top of street lights and utility poles and new “small” cell tower poles are being installed. New wireless antennas are being attached to buildings, from two story buildings as well as taller apartment complexes.  Each wireless facility includes transmitting antennas and equipment closer to the ground and next to trees. 

Trees canopy is critical to human health the climate and and the environment because trees:

• Capture air pollution and improve air quality.
• Save energy by reducing the temperature and reducing energy use for air conditioning. 
• Remove carbon dioxide from the air and release oxygen. 
• Help prevent flooding and keep the soil nutrient-rich.
• Provide habitat for wildlife.

Wireless infrastructure can impact tree canopy in numerous ways

• Companies have aggressively trimmed trees with no oversight by arborists. 
• Trees are being felled/removed to build infrastructure and/or roads to the facility. 
• Digging to install the poles and related equipment can disrupt the root zone. 
• Research studies have found damage to trees from exposure to the radiofrequency radiation emitted from the wireless antennas. 

Austrian Telecom Giant Telstra is Aware That Trees Absorb Wireless Radiation

“Telstra is also funding research into whether uniquely Australian obstacles – including flora – will disrupt 5G signals, which occupy a higher frequency and don’t travel as far as other mobile signals. “Something that seems to be unique to Australia, and we found with earlier standards, is how gumtrees impact those radio signals and the way they get from the radio tower to the end user,”

-Telstra pushes for 5G that Works in Australia, The Sydney Morning Herald, January 9, 2017,

Research Studies:

Breunig, Helmut. “Tree damage caused by mobile phone base stations An observation guide”  (2017).

Waldmann-Selsam, C., et al. “Radiofrequency radiation injures trees around mobile phone base stations.” Science of the Total Environment 572 (2016): 554-69.

• “In the last two decades, the deployment of phone masts around the world has taken place and, for many years, there has been a discussion in the scientific community about the possible environmental impact from mobile phone base stations. Trees have several advantages over animals as experimental subjects and the aim of this study was to verify whether there is a connection between unusual (generally unilateral) tree damage and radiofrequency exposure.
• To achieve this, a detailed long-term (2006-2015) field monitoring study was performed in the cities of Bamberg and Hallstadt (Germany).
• The measurements of all trees revealed significant differences between the damaged side facing a phone mast and the opposite side, as well as differences between the exposed side of damaged trees and all other groups of trees in both sides. Thus, we found that side differences in measured values of power flux density corresponded to side differences in damage. The 30 selected trees in low radiation areas (no visual contact to any phone mast and power flux density under 50μW/m(2)) showed no damage. Statistical analysis demonstrated that electromagnetic radiation from mobile phone masts is harmful for trees. These results are consistent with the fact that damage afflicted on trees by mobile phone towers usually start on one side, extending to the whole tree over time.”
• Tree damages in Bamberg and Hallstadt – examples from a documentation 2006-2016 DOWNLOAD PDF FOR FREE
• Selection documentation  Trees in Bamberg , Part 1 DOWNLOAD PDF FOR FREE
• Selection documentary  trees in Bamberg , part 2 DOWNLOAD PDF FOR FREE
• Cornelia Waldmann-Selsam and Horst Eger:  Tree damage in the vicinity of mobile phone transmitters , environment – medicine – society 3/2013 PDF DOWNLOAD FOR FREE
• Cornelia Waldmann-Selsam and Horst Eger:  Tree damage in the vicinity of mobile phone base stations , environment – ​​medicine – society 3/2013 PDF DOWNLOAD FOR FREE
• Media reports   ON THE CONTRIBUTION

Martin Pall. “Electromagnetic Fields Act Similarly in Plants as in Animals: Probable Activation of Calcium Channels via Their Voltage Sensor” Current Chemical Biology, Volume 10 , Issue 1 , 2016

• It has been shown that low intensity microwave/lower frequency electromagnetic fields (EMFs) act in animals via activation of voltage-gated calcium channels (VGCCs) in the plasma membrane, producing excessive intracellular calcium [Ca2+]i, with excessive [Ca2+]i leading to both pathophysiological and also in some cases therapeutic effects. The pathophysiological effects are produced largely through excessive [Ca2+]i signaling including excessive nitric oxide (NO), superoxide, peroxynitrite, free radical formation and consequent oxidative stress. The activation of the VGCCs is thought to be produced via EMF impact on the VGCC voltage sensor, with the physical properties of that voltage sensor predicting that it is extraordinarily sensitive to these EMFs.
• It is shown here that the action of EMFs in terrestrial, multicellular (embryophyte) plants is probably similar to the action in animals in most but not all respects, with calcium channel activation in the plasma membrane leading to excessive [Ca2+]i, leading in turn to most if not all of the biological effects. A number of studies in plants are briefly reviewed which are consistent with and supportive of such a mechanism. Plant channels most plausibly to be involved, are the so-called two pore channels (TPCs), which have a voltage sensor similar to those found in the animal VGCCs.

Halgamuge, M.N. “Weak radiofrequency radiation exposure from mobile phone radiation on plants.” Electromagnetic Biology and Medicine 36.2 (2017): 213-235.

• “Our analysis demonstrates that the data from a substantial amount of the studies on RF-EMFs from mobile phones show physiological and/or morphological effects (89.9%, p < 0.001). Additionally, our analysis of the results from these reported studies demonstrates that the maize, roselle, pea, fenugreek, duckweeds, tomato, onions and mungbean plants seem to be very sensitive to RF-EMFs. Our findings also suggest that plants seem to be more responsive to certain frequencies…”

Shikha Chandel, et al. “Exposure to 2100 MHz electromagnetic field radiations induces reactive oxygen species generation in Allium cepa roots.” Journal of Microscopy and Ultrastructure 5.4 (2017): 225-229.

• “The present study investigated the role of cell phone EMF-r in inciting oxidative damage in onion (Allium cepa) roots at a frequency of 2100 MHz. Onion roots were exposed to continuous wave homogenous EMF-r for 1, 2 and 4 h for single day. The results showed that EMF-r exposure enhanced the content of MDA, H2O2 and O2−. Also, there was an upregulation in the activity of antioxidant enzymes− SOD and CAT− in onion roots. The study concluded that 2100 MHz cell phone EMF-r incite oxidative damage in onion roots by altering the oxidative metabolism.”

Gustavino, B., et al. “Exposure to 915 MHz radiation induces micronuclei in Vicia faba root tips.” Mutagenesis 31.2 (2016): 187-92.

• The increasing use of mobile phones and wireless networks raised a great debate about the real carcinogenic potential of radiofrequency-electromagnetic field (RF-EMF) exposure associated with these devices. Conflicting results are reported by the great majority of in vivo and in vitro studies on the capability of RF-EMF exposure to induce DNA damage and mutations in mammalian systems. Aimed at understanding whether less ambiguous responses to RF-EMF exposure might be evidenced in plant systems with respect to mammalian ones, in the present work the mutagenic effect of RF-EMF has been studied through the micronucleus (MN) test in secondary roots of Vicia faba seedlings exposed to mobile phone transmission in controlled conditions, inside a transverse electro magnetic (TEM) cell.
• Results of three independent experiments show the induction of a significant increase of MN frequency after exposure, ranging from a 2.3-fold increase above the sham value, at the lowest SAR level, up to a 7-fold increase at the highest SAR. These findings are in agreement with the limited number of data on cytogenetic effects detected in other plant systems exposed to mobile phone RF-EMF frequencies and clearly show the capability of radiofrequency exposure to induce DNA damage in this eukaryotic cell system.
• It is worth noticing that this range of SAR values is well below the international limits for localised exposure (head, trunk), according to the ICNIRP guidelines (35) and IEEE std C95.1 (38), which are 10 (8.0) W/kg for occupational exposure and 2.0 (1.6) W/kg for general public exposure respectively.

Halgamuge, Malka N., See Kye Yak and Jacob L. Eberhardt. “Reduced growth of soybean seedlings after exposure to weak microwave radiation from GSM 900 mobile phone and base station.” Bioelectromagnetics 36.2 (2015): 87-95.

• The aim of this work was to study possible effects of environmental radiation pollution on plants. The association between cellular telephone (short duration, higher amplitude) and base station (long duration, very low amplitude) radiation exposure and the growth rate of soybean (Glycine max) seedlings was investigated.
• The exposure to higher amplitude (41 V m−1) GSM radiation resulted in diminished outgrowth of the epicotyl. The exposure to lower amplitude (5.7 V m−1) GSM radiation did not influence outgrowth of epicotyl, hypocotyls, or roots. The exposure to higher amplitude CW radiation resulted in reduced outgrowth of the roots whereas lower CW exposure resulted in a reduced outgrowth of the hypocotyl. Soybean seedlings were also exposed for 5 days to an extremely low level of radiation (GSM 900 MHz, 0.56 V m−1) and outgrowth was studied 2 days later. Growth of epicotyl and hypocotyl was found to be reduced, whereas the outgrowth of roots was stimulated.
• Our findings indicate that the observed effects were significantly dependent on field strength as well as amplitude modulation of the applied field.

Senavirathna, M.D., et al. “Nanometer-scale elongation rate fluctuations in the Myriophyllum aquaticum (Parrot feather) stem were altered by radio-frequency electromagnetic radiation.” Plant Signal Behav 9.3 (2014).

• Statistically significant changes to this plant from a non thermal effect.

Soran, M.L., et al. “Influence of microwave frequency electromagnetic radiation on terpene emission and content in aromatic plants.” Journal of Plant Physiology 171.15 (2014): 1436-43.

• Microwave irradiation resulted in thinner cell walls, smaller chloroplasts and mitochondria, and enhanced emissions of volatile compounds, in particular, monoterpenes and green leaf volatiles (GLV). These data collectively demonstrate that human-generated microwave pollution can potentially constitute a stress to the plants.
• The above is only a small sampling of the research showing biological effects at non thermal levels on living organisms.

Haggerty, Katie. “Adverse Influence of Radio Frequency Background on Trembling Aspen Seedlings.” International Journal of Forestry Research 2010.836278 (2010).

• “This study suggests that the RF background may have strong adverse effects on growth rate and fall anthocyanin production in aspen, and may be an underlying factor in aspen decline.”

Kouzmanova, M., et al. “Alterations in enzyme activities in leaves after exposure of Plectranthus sp. plants to 900 MHz electromagnetic field.” Biotechnology & Biotechnological Equipment 23.sup1 (2009): 611-615.

• “The purpose of our study was to investigate the alterations in enzyme activities in leaves after exposure of plants Plectranthus sp. to 900 MHz EMF and their dependence on the time elapsed after exposure.
• Alterations in activity of isocitrate dehydrogenase, malate dehydrogenase and glucose-6-phosphate dehydrogenase in leaves were registered immediately after the end of the exposure and 1, 2 and 24 hours later. Irradiation of plants induced different alterations in enzyme activities depending on the time elapsed after irradiation. Immediately after exposure the activity of the three investigated enzymes decreased, but increased at 24th hour.
• In conclusion, the data provide evidence that plants perceive and respond to electromagnetic fields and are a good model to study the effects of mobile phone radiation.”

Trebbi, Grazia, et al. “Extremely low frequency weak magnetic fields enhance resistance of NN tobacco plants to tobacco mosaic virus and elicit stress‐related biochemical activities.” Bioelectromagnetics 28.3 (2007): 214-223.

• “Increasing evidence has accumulated concerning the biological effects of extremely low frequency magnetic fields (ELF-MFs) in different plant models.
• Following ELF-MFs exposure, an increased resistance was detected, particularly after an 8-h treatment, as shown by the decrease in lesion area and number. Moreover, two enzyme activities involved in resistance mechanisms were analyzed: ornithine decarboxylase (ODC) and phenylalanine ammonia-lyase (PAL). Uninoculated leaves previously exposed to ELF-MFs in general showed a significant increase relative to controls in ODC and PAL activities, in particular for 13 microT static MF plus 28.9 microT, 10 Hz sinusoidal MF (24 h) treatment.
• In conclusion, ELF-MFs seem to influence the HR of tobacco to TMV, as shown by the increased resistance and changes in ODC and PAL activities, indicating the reliability of the present plant model in the study of bioelectromagnetic interactions.” 

International Conference on EMF Impacts to Trees

“the effect of electromagnetic radiation on trees” the groene paviljoen, baarn, 2.

Website of Conference  http://www.boomaantastingen.nl/

Download Program of Conference 

Tree Damage from Chronic High Frequency Exposure  Volker Schorpp; physicist  Lecture  (about 31 MB)

Unknown Tree Diseases in Urban Surroundings and the Possible Effects of WiFi Access Points on Ash Trees (in the lab) – Dr. André van Lammeren

Unexpected Effects on Changing Environmental Factors – Dr. Ing. Rein Roos

Innovative Assessments of Tree Health – Ir. Lies Steel

Visible Damage on Free-standing Trees – Dr. ing. Dipl. Phys. Volker Schorpp

Click here to see a PDF of one of the presentations “ Tree Damage from Chronic High Frequency Exposure Mobile Telecommunications, Wi-Fi, Radar, Radio Relay Systems, Terrestrial Radio, TV etc. ” by  Dr.  Volker Schorpp

Effects of Electromagnetic Stress on Trees – BSc PhD. Andrew Goldsworthy

Call for Support for Further Study – Hans Groen in ’t Wout

“Trees Under High Frequency”  PDF German 

Vimeo   Tree damage by electromagnetic radiation from Boomaantastingen on Vimeo .

TEN YEAR REPORT

Do WiFi Signals Stunt Plant Growth?

The claim behind a 2013 school science project purportedly documenting that wireless signals wilt cress plants remains unproven., kim lacapria, published april 8, 2017.

About this rating

On 4 April 2017, the web site Safe Living published an article reporting that high schoolers put together a science experiment involving cress and wifi that purportedly showed wireless connectivity is harmful to seedlings:

Foreign researchers are extremely excited for a biology project from five 9th grade girls ... Take 400 Cress seeds and place them into 12 trays. Then place six trays in two rooms at the same temperature. Give them the same amount of water and sun over 12 days, and remember to expose half of them to mobile [Wi-Fi] radiation. It is a recipe for a biology test so brilliant that it has attracted international attention among acknowledged biologists and radiation experts. Behind the experiment are five girls from 9b in Hjallerup School in North Jutland, and it all started because they found it difficult to concentrate during the school day ... The school was not equipped to test the effect of mobile phone radiation on them. Therefore, the girls had to find an alternative. And the answer was Cress. Six trays of seeds were put into a room without radiation, and six trays were put into another room next to two [Wi-Fi] routers. Such routers broadcast the same type of radiation as an ordinary mobile. And the result spoke was clear: cress seeds next to the router did not grow, and some of them were even mutated or dead.

Most versions of the story did not provide any further detail. After its initial appearance in 2013, the claim regularly pops up as "new news," spiking again in December 2013 in an article describing the school project as a study (rather than an experiment) and raising health concerns .

However, a 2013 meta-study suggested that, while research showed mixed results, there was little to cause immediate concern and proposed more research on the topic:

The lack of an apparent biophysical mechanism of interaction and the generally negative results of other studies using RF exposures at similar levels as Wi-Fi (Jauchem 2008; Habash et al. 2009; Vecchia et al. 2009; IARC 2011) provide no basis to anticipate that Wi-Fi exposure will cause any biological effects. The overwhelming consensus of health agencies around the world is that RF exposures below international (ICNIRP or IEEE) exposure limits have not been shown to produce any health hazard (Verschaeve 2012).

A May 2013 analysis written by skeptic and mathematician Pepijn van Erp as the claim made its way around the Internet unpacked concerns about the project:

Who are the scientists who are so enthusiastic about this poor study? The article on the Danish website mentions Olle Johansson, who received the ‘Misleader of the Year‘ Award from the Swedish skeptics in 2004. He is well known for having unsubstantiated ideas of negative health effects of radiation. He is cited in the Danish article as having plans to replicate the girls’ experiment in cooperation with senior researcher Marie-Claire Cammaerts from the Université libre de Bruxelles. We shouldn’t expect anything good from this replication, because as I’ve shown in a blog some while ago, Cammaerts probably cannot be trusted with this kind of experiments (see: Ants Performing Statistical Miracle under GSM Phone Radiation?). [Update 4-1-2016: Cammaerts and Johansson published a replication, in which they managed to make even more mistakes] Tjomlid also mentions Andrew Goldsworthy, another well known fear monger, and Dutchman Niek van ‘t Wout, who is head of green space of a Dutch city and the instigator of research into the possible deteriorating effect of WiFi on trees (so he is not a scientist himself). After a not so convincing first experiment, Wageningen University started a follow up, of which we never heard again.

The Guardian posited that heat generated by routers could be a possible plant growth inhibitor, and observed that the students didn't rule out other causes for sleep disruption near mobile phones (such as light or general distracting properties).

It is true that in May 2013 a small school science project was done by five Danish schoolgirls, its findings cyclically reported and shared on social media for years thereafter. Although anti-technology sites continue to present the claim as novel and credible, seasoned researchers almost immediately identified significant flaws in the methodology.

A study published in March 2016 has been widely billed as a replication of the Danish high school project. That study, which is published in an obscure journal ( Current Chemical Biology ) and written by a professor actively involved in pushing claims about the dangers of EMF, as well as a “ consultant ” who works for a company that offers to “measure your home, office and/or school for Dirty Electricity, Radio Frequency Radiation, Electric and Magnetic fields and provide simple solutions to reduce your exposure to ‘electrosmog’, is literally the opposite of a replication of the Danish study, as they did not actually replicate their results:

We did not get the same results as the high schools students in Denmark. Of the four species we tested, garden cress (Lepidium sativum) seemed to be the least sensitive to Wi-Fi radiation under controlled laboratory conditions. There was no difference in germination or biomass at the end of the 28-day experiment.

While this study did test the effects of Wi-Fi on other plants (broccoli, red clover, and peas) and purported to find negative effects on them, science is still waiting for a successful replication to the Danish cress study (as well as a replication of new results presented in this paper).

Bean, Daniel.   "Can WiFi Signals Stunt Plant Growth?"     ABC News .   24 May 2013.

Gage, Suzi.   "Wi-Fried: Do Wireless Routers Really Kill Plants?"     The Guardian .   17 December 2013.

Havas, Magda and M. Sheena Symington.   "Effects of Wi-Fi Radiation on Germination and Growth of Broccoli, Pea, Red Clover and Garden Cress Seedlings: A Partial Replication Study."     Current Chemical Biology .   2016.

Howe, Alex.   "No, Wi-Fi Does Not Hurt Plants — Or Anything Else for That Matter."     Science Meets Fiction .   16 December 2013.

Van Erp, Pepijn.   "Danish School Experiment with Wifi Routers and Garden Cress, Good Example of Bad Science."     Pepijn Van Erp .   25 May 2013.

Zolfagharifard, Ellie and Ben Spencer.   "What's Wifi Doing to Us? Experiment Finds That Shrubs Die When Placed Next to Wireless Routers."     Daily Mail .   16 December 2013.

Stop Smart Meters .   "9th Grade Student 'Cress + Wifi' Experiment Attracts International Attention."     21 May 2013.

Safe Living .   "9th Grade Student 'Cress + Wifi' Experiment Attracts International Attention."     4 April 2017.

Updated [6 November 2017]: Added further information about a 2016 study billed as a replication of the original Danish finding.

By Kim LaCapria

Kim LaCapria is a former writer for Snopes.

Article Tags

People Once Used Nuclear Radiation to Grow Really Big Plants

• Boston University
• Planting Guides
• Indoor Gardening
• Urban Farms

The word nuclear has a bad reputation, and for good reason. If you know your history, it may bring to mind the nuclear bombs dropped on Japan during World War II that killed hundreds of thousands of people, or maybe the nuclear arms race between the U.S. and the Soviet Union during the Cold War.

Which is precisely why, in the 1950s and 1960s, the U.S. government launched a program called Atoms For Peace to give nuclear energy some positive press. One of the public relations strategies included so-called gamma gardens, also known as atomic gardens. Basically people used nuclear radiation to try to grow mutant plants.

The hope was that the mutations would be beneficial — that plants would grow faster, be more resistant to cold or pests, produce bigger fruits or simply be more colorful, for example, making the practice more attractive to farmers and gardeners.

Atlas Obscura explains how the radiation worked to affect plant growth:

The mechanism of a gamma garden was simple: radiation came from a radioactive isotope-laden metal rod, which jutted out of the garden’s center and exposed the plants to its silent rays. Radiation slowly bludgeoned the plant DNA like a hammer and changed how genes were expressed.

Some of the gardens covered five acres or more and formed a circle, with the radioactive rod in the center, according to the 99% Invisible radio program , and those rods would radiate the field for 20 hours a day.

Go nuclear in your own backyard

In 1959, across the Atlantic in the U.K., a woman named Muriel Howorth started the Atomic Gardening Society and published a book a year later about how anyone can grow an atomic garden in their own yard. Between the appeal of mutant plants and her handy DIY guide, gamma gardens took off in labs, farms and backyards.

The 99% Invisible radio show detailed more about Howorth's borderline obsession with atomic gardening in one episode:

She would ship members irradiated seeds and ask them to send back any data they could about the plants. Howorth also published an atomic magazine and hosted gatherings and film screenings on atomic topics — in 1950, she even staged a performance where actors pantomimed the structure of an atom. From a review in Time magazine: “Before a select audience of 250 rapt ladies and a dozen faintly bored gentlemen, some 13 bosomy atomic energy associates in flowing evening gowns gyrated gracefully about a stage in earnest imitation of atomic forces at work.”

For some people, the appeal of atomic gardens was to grow a lot of food and ease food shortages after the war. But for others like Howorth, the appeal was simply to try something new and interesting. She lobbied hard for her cause, too. She wrote to Albert Einstein and he agreed to become a patron of her organization, according to a paper published in the British Journal for the History of Science .

Fads fade ... mostly

Alas, despite Howorth's best efforts, enthusiasm for gamma gardens waned as beneficial mutations were rare and amateur growers found it difficult to detect them. However, the concept of genetically modified crops started long before this trend and continues to this day. Gamma gardens even contributed to some varieties of plants today, including these black beans and this type of begonia . And Japan's Institute of Radiation BreedingInstitute of Radiation Breeding has adopted atomic garden techniques to breed various crop species.

The conversation about GMOs is certainly more controversial today than it was back then, but this interesting chapter just shows how attitudes can change over time.

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Effects of Radiation on Seed Survival and Germination

Emily xie february 20, 2017, submitted as coursework for ph241 , stanford university, winter 2017, introduction.

It is important to understand the implications radiation can have on seed survival and germination, because plants are a vital part of most sustainable ecosystems. Germination, the process by which a plant grows from a seed, is shown in Fig. 1.

Radiation on Seed Germination

Exposure to radiation has been found to cause a large range of effects on seeds. In a study done by Marcu et al. on the effects of radiation on seeds, it was found that radiation not only impacts the germination potential and actual qualities of the germinated seedlings (such as root and shoot lengths), where germination potential is the percentage of seeds that that germinated overall and the time of germination compared to when the seed was planted. [1] Furthermore, seeds were also found to have decreased photosynthetic pigment content when they were irradiated compared to those that were not irradiated. [1] Thus, it is clear that radiation not only impacts the quantity of seedlings, but also the quality of them.

From the Marcu et al. research, it is also clear that plants and seeds are much more radiation tolerant than are other living beings. For example, the smallest dose mentioned in the paper is more than 20 times what would be required to kill a vertebrate animal. [1] Even at radiation levels 200 times the dose required to kill a person, some seeds still germinated. Seeds are clearly more hearty than other animals, and likely even full grown plants.

While research has shown clearly that radiation has a large impact on both the quantity and quality of seedlings, it has also been shown that radiation impacts various seed varieties differently. [2] There has been research dedicated to determining how to increase the shelf-life of various plants and sprouts through the use of radiation. [2] Each type of produce seed and sprout has a different level of approved radiation, with the ultimate goal being the safety of the consumer. [2]

Radiation on Seedlings

Even if seeds germinate, radiation can have long-lasting effects on the subsequent seedlings. When seeds are exposed to high levels of radiation, even if the seeds germinate, the subsequent seedlings are at high-risk of mortality. [1] In fact, when exposed to ≤ 0.5 kGy of radiation, subsequent seedlings only survived for a maximum of 10 days. [1] Because radiation can often lead to genetic mutations, seedlings are at high risk for reduced growth, seed production, and mortality at all radiation levels. [3] Continued radiation to seedlings will only continue to exacerbate these effects. [3]

Radiation not only impacts the probability of seed germination, but it also results in longer-term effects on seedlings and their ultimate rate of survival after germination. This is extremely relevant, because of the importance of plants within sustainable ecosystems. Plants are also often the key to an ecosystem reestablishing itself after a disaster and it is important to consider how radiation can impact the reestablishment of an ecosystem in terms of both quantity of plants and in quality of subsequent plants. Furthermore there has been quite a bit of research regarding the use of radiation within agriculture to manage bacteria growth. [4]

© Emily Xie. The author grants permission to copy, distribute and display this work in unaltered form, with attribution to the author, for noncommercial purposes only. All other rights, including commercial rights, are reserved to the author.

[1] D. Marcu et al. , "Gamma Radiation Effects on Seed Germination, Growth and Pigment Content, and ESR Study of Induced Free Fadicals in Maize (Zea mays)," J. Biol. Phys. 39 , 625 (2013).

[2] V. Komolprasert and K. Morehouse, Irradiation of Food and Packaging: Recent Developments (American Chemical Society, 2004), pp. 107-116.

[3] R. Miller, " Effects of Radiation on Plants ," Physics 241, Stanford University, Winter 2015.

[4] I. Piri et al. , " The Use of Gamma Irradiation in Agriculture ," Afr. J. Microbiol. Res. 5 , 5806 (2011).

REVIEW article

Ionizing radiation, higher plants, and radioprotection: from acute high doses to chronic low doses.

• Centre for Research in Biosciences, University of the West of England, Bristol, Bristol, United Kingdom

Understanding the effects of ionizing radiation (IR) on plants is important for environmental protection, for agriculture and horticulture, and for space science but plants have significant biological differences to the animals from which much relevant knowledge is derived. The effects of IR on plants are understood best at acute high doses because there have been; (a) controlled experiments in the field using point sources, (b) field studies in the immediate aftermath of nuclear accidents, and (c) controlled laboratory experiments. A compilation of studies of the effects of IR on plants reveals that although there are numerous field studies of the effects of chronic low doses on plants, there are few controlled experiments that used chronic low doses. Using the Bradford-Hill criteria widely used in epidemiological studies we suggest that a new phase of chronic low-level radiation research on plants is desirable if its effects are to be properly elucidated. We emphasize the plant biological contexts that should direct such research. We review previously reported effects from the molecular to community level and, using a plant stress biology context, discuss a variety of acute high- and chronic low-dose data against Derived Consideration Reference Levels (DCRLs) used for environmental protection. We suggest that chronic low-level IR can sometimes have effects at the molecular and cytogenetic level at DCRL dose rates (and perhaps below) but that there are unlikely to be environmentally significant effects at higher levels of biological organization. We conclude that, although current data meets only some of the Bradford-Hill criteria, current DCRLs for plants are very likely to be appropriate at biological scales relevant to environmental protection (and for which they were intended) but that research designed with an appropriate biological context and with more of the Bradford-Hill criteria in mind would strengthen this assertion. We note that the effects of IR have been investigated on only a small proportion of plant species and that research with a wider range of species might improve not only the understanding of the biological effects of radiation but also that of the response of plants to environmental stress.

Introduction

There has been much recent interest in the health of organisms at radioactively contaminated sites such as those at Chernobyl and Fukushima. Thriving communities of flora and fauna (e.g., Deryabina et al., 2015 ) have surprised many people but there are also reports of significant effects of chronic irradiation at surprisingly low doses (e.g., Boratyński et al., 2016 ). This ‘paradox’ persists, in part, because the observed effects on organisms from different doses of environmental radioactivity have yet to be synthesized into a coherent understanding. It is important to do this because ionizing radiation (IR), whilst occurring naturally, is a pollutant, both actual and potential, from a nuclear industry of global significance – at the beginning of 2018 there were numerous polluted nuclear-legacy sites and 448 on-grid civil nuclear reactors generating >10% of the world’s electricity, with 58 under construction ( International Atomic Energy Agency [IAEA], 2018 ) and many more planned. Almost all of the highly active nuclear waste ever generated is yet to be stored in permanent repositories, and credible environmental safety cases will be necessary prior to their construction. If nuclear power is to be a significant source of low carbon electricity in the future and if we are to deal with the nuclear legacy and any further nuclear accidents or detonations, it is desirable to demonstrate that the effects of IR on flora and fauna are understood. This review is based on a compilation of current data for plants that, we suggest, helps to resolve the ‘paradox’ of the effects of IR in the environment by analyzing the available data within a stress-response context and then uses this to propose new contexts for research.

Ionizing Radiation and the Evolution of Plants

Few biological phenomena can be fully understood without knowledge of their evolution. From an evolutionary perspective IR is a primordial stressor. Life on Earth evolved in varying natural background IR of cosmic and geologic origin. The activities of β and γ radiation from geological sources have decreased by about a factor of eight since the origin of life between 3.5 and 4 Ga ago ( Karam and Leslie, 1999 ). Eukaryotic life ( Archibald, 2015 ) probably began >2.5 Ga ago under conditions that received five times current background levels of β/γ radiation. When plants first colonized the land surface ( c. 460 Ma ago) ( Gensel, 2008 ) background IR levels were still significantly higher than at present. These figures are global averages – if background IR varied spatially as much in the past as it does now, many early life forms were exposed to much higher background IR than was average at the time. If life’s early exposure to IR helped drive the evolution of processes, such as DNA repair, that have found important roles ever since, it might help to explain the current occurrence of radio-resistance, and sometimes even the ability to adapt to radiation, in some extant prokaryotes ( Siasou et al., 2017 ).

Estimating external doses of background radiation at the Earth’s surface depends on understanding geological events, with the coalescing of crustal plates probably the most important (Figure 1 ). About 460 Ma ago plants did not just colonize the land surface but also the above-surface atmosphere ( Willey, 2016 ). They did this using morphology of increasing leaf area index, that not only increased light capture but also allowed increased exchange of gases with the near surface atmosphere. In addition to background β and γ, 222 Rn contributes very significantly (>60%) to current background doses to humans ( Health Physics Society [HPS], 2015 ) and we suggest, therefore, that during their evolution it may also have contributed to doses to some higher plants, especially those inhabiting canopies with low air flow. Further, we note how important to understanding the effects of IR on higher plants that the exposure of ancient prokaryotes to IR might be – the key to the success of higher plants is that they house plastids of prokaryotic origin (mitochondria and chloroplasts) at the Earth’s surface-atmosphere interface. It is, therefore, estimated that average background doses in the range up to 7 mGy/y (c. 20 μGy d -1 ) occurred for a significant period of the evolution of plant life but that high background areas may have had significantly higher dose rates.

FIGURE 1. Estimated ionizing radiation (IR) dose rate through geological time at the Earth’s surface. Geological estimates based on β+γ doses taken from Karam and Leslie (1999) . Rn-222 is a significant current contributor to background radiation doses (c. 1.2 mSv/y current global average) for inhabitants in contained environments on the Earth’s surface, including plants in canopies, which have evolved to exchange gases in the near surface environment. Rn-222 contribution to dose rate is, therefore, included and is estimated from geologic background, which is dominated by U decay series radioisotopes. K-40, estimated from its half-life, dominates internal doses to organisms and is thus a proxy for them. Total estimated dose rate is combined internal and external dose for an organism at the Earth’s surface – although, of course, for much of the last 4.5 Ga there were no organisms at the Earth’s surface. The geologically driven peak reflects events in the Earth’s crust including the formation of continental plates. Current global mean background dose rate is 2.5 mGy/y. (Details of calculations in Supplementary Data Sheet S1 ).

When energy from IR is deposited directly into DNA it can damage it. There are numerous chemical and physical processes that can damage DNA in a variety of ways, but IR is one of the few that can induce a range of damage, including double stranded breaks (DSBs) ( Oladosu et al., 2016 ). Factors that cause damage on a single strand probably helped favor the evolution of a double-stranded molecule as genetic material – a second strand provides a template for repair of damaged bases or nucleotides ( Freidberg, 1997 ). Multiple copies of chromosomes underpin further processes of DNA repair – for example homologous recombination (HR), which in many eukaryotes helps produce variation in haploid gamete cells during meiosis, is also involved in the repair of DSBs ( Jackson and Bartek, 2009 ). Homologous pairing, and hence an important DSB repair pathway, is promoted in archaea by RadA , in bacteria by RecA and in eukaryotes by Rad51 , which are slightly different versions of the same gene in all organisms – eukaryotic nuclear DNA probably acquired Rad51 via transfer of RecA from prokaryotic endosymbionts ( Lin et al., 2006 ). Rad51 was identified through its radiation responsiveness although IR was not necessarily the DSB-causing agent that drove its evolution. It has long been suggested that there is a link between DNA damage and the evolution of sex ( Bernstein et al., 1985 ; Rocha, 2016 ) with RecA having a crucial role in both ( Bernstein and Bernstein, 2010 ). Overall, the ubiquitous, and esthetically appealing, static image of the double helix of DNA detracts from the reality of dynamic processes of DNA damage and repair that underpin life on Earth ( Friedberg, 2003 ) and that evolved in response to primordial stressors, perhaps including IR. Direct effects of background IR on DNA are probably less significant now than they have ever been but, especially in ancient high background areas, they may have played a role in the evolution of both the genetic architecture and the DNA curation processes of life.

Ionizing radiation can also damage DNA indirectly via the products of radiolysis, which causes a cascade of reactive molecules (Figure 2 ). Many of these molecules play key roles in the processes of life, their reactivity making them useful in signaling and defense but also potentially damaging to biomolecules ( Foyer and Noctor, 2016 ). The reactive oxygen species (ROS) resulting from radiolysis of water are important in producing its effects at high doses, including for example during radiotherapy or corrosion of pipes in nuclear reactors. In an aqueous environment, e.g., cells, ROS production can be calculated from dose rates ( Smith et al., 2012 ; Figure 2 ). However, during the evolution of life, UV, which can also cause direct DNA damage, has been a much more significant source of ROS than IR. UV-C with a wavelength below 100 nm is ionizing but is also absorbed by many atmospheric constituents, perhaps including some that occurred in the early atmosphere ( Hessen, 2008 ), and has likely never been a particularly significant source of ROS in aqueous environments, including cells, at the Earth’s surface. UV with wavelengths longer than 100 nm does not generally ionize water but can ionize other organic molecules, including proteins. In an aqueous solution, these photoionized molecules can induce the production of ROS from H 2 O ( Pattison and Davies, 2006 ). The probability of this occurring is relatively low compared to the probability of radiolysis induced by IR but the amount of UV arriving at the Earth’s surface is, even after the formation of the ozone layer, much more significant than the amount of background IR. Calculations of the production of ROS produced by UV over geological time compared to that from IR suggest that UV has, throughout evolution, been the most significant radiative source of ROS that organisms have had to contend with (Figure 3 ). Overall, understanding the effects of IR must occur with recognition that it was a feature of the primordial environment that is now less intense than it once was and that there are other radiative stressors that can damage DNA and promote the formation of ROS, often at much more significant rates, than does IR.

FIGURE 2. The products of the radiolysis of water (×10 -16 mol/g). Smith et al. (2012) describe the above cascade for the production of oxidizing species by radiolysis. During chronic irradiation, several of the molecules produced react continuously to give the products shown above. For each product, G -values describe the relationship between energy deposited and the amount of product produced. G -values for β/γ radiation from Cs-137 were used to calculate, in ×10 -16 mol/g, the amount of product at a range of dose rates. HO is short-lived but strongly oxidizing and e - aq (a solvated electron) can combine with O 2 to produce dioxygen radicals (O 2 - – ‘superoxide’). The consequences of HO and e - aq production dominate the oxidative effects of radiolysis on organisms.

FIGURE 3. Radical induction-potential from water by different radiation sources through Earth’s history. UV radiation with λ > 100 nm is not energetic enough to directly ionize water but π-bonds and n -electrons in organic molecules can absorb UV, producing exited molecules that, in aqueous solution, can induce the formation of radicals from water. Radiation-induced chemical yields from ionization ( G -values in moles per 100 eV energy deposited) were used to calculate potential radical production from both UV and background radiation through Earth’s history. For UV acting on organic molecules G = 0.01 was, conservatively, assumed and for background radiation acting on water G = 2.8 (the value for Cs-137 emissions). For UV, current energy in the 250–350 nm range was taken as 1.5 W/m 2 , converted to eV and an estimate of variation in total geological irradiance of UV ( Cockell and Horneck, 2001 ) used to calculate the potential for radical production. For comparison, the potential for Chernobyl radiation to induce radicals was calculated assuming 1MBq of Cs-137/m 2 – an activity that occurs widely in the Chernobyl Exclusion Zone. For Cs-137 an energy of 1.127 MeV per Bq was used to include both β and γ emissions. The massive drop in potential radical production from UV at Earth’s surface reflects the formation of the ozone layer. The concentrations of radicals to which life was actually exposed is not necessarily directly related to the predictions above because: constituents of the Earth’s atmosphere other than ozone, which have changed significantly over time, can affect UV penetration to the surface; early organisms may have lived in significant depths of water; life probably evolved UV screening molecules at an early stage. (Details of calculations given in Supplementary Data Sheet S2 ).

Environmental Protection and the Dose-Effects Data

In general, data from accidents and controlled experiments suggest that, with some differences between species, acute high doses of IR in the range of 10–1000 Gy can be fatal to plants ( United Nations Scientific Committee on the Effects of Atomic Radiation [UNSCEAR], 1996 ). Although fewer studies have examined chronic low dose effects of IR in plants, United Nations Scientific Committee on the Effects of Atomic Radiation [UNSCEAR] (1996) suggested 10 mGy/d (417 μGy h -1 ) as a threshold dose rate for radio-protection of plants ( Nelson-Beyer and Meador, 2011 ). This confirmed a long-established International Atomic Energy Agency (IAEA) threshold for radiation dose rates of <10 mGy d -1 having ‘no detrimental effects’ for populations of terrestrial plants in the field ( International Atomic Energy Agency [IAEA], 1992 ). To help account for differences in response between different organisms, including different types of plant, the International Commission on Radiological Protection developed ( International Commission on Radiological Protection [ICRP], 2008 ) the use of a set of reference animals and plants (RAPs). These were later supplemented with DCRLs for each RAP ( International Commission on Radiological Protection [ICRP], 2014 ) – a range of dose rates that might prompt evaluation of potential radiological impacts. The ICRP’s RAPs include plant DCRLs for grass of 1–10 mGy d -1 (41.7–417 μGy h -1 ) and for pine trees of 0.1–1 mGy d -1 (4.17–41.7 μGy h -1 ). The grass RAP provides a reference range for herbaceous higher plants and pine trees a reference range for the more IR-sensitive woody plants. The EU-funded ERICA project suggested, after including a safety factor of 5, a chronic exposure screening value of 10 μGy h -1 for ecosystems ( Garnier-Laplace and Gilbin, 2006 ). Ecosystems will, however, include some organisms that are more sensitive than plants. Here we focus on discussing published data on the effects IR on plants with an ultimate focus on the DCRLs for grass and pine RAPs because they are a well-developed international framework for protecting plants from the effects of IR.

There are several reasons for probing the appropriateness of these DCRLs. The development of RAPs emphasized that the understanding of the effects of radiation on plants is much less than that for humans or other animals. This continues to be the case and can, in part, be attributed to the challenges of studying radiological impacts on plants. For example, when studying pine trees, it can be challenging to establish either accurate external doses at different heights or accurate internal doses arising from accumulation in different parts of a large organism ( International Commission on Radiological Protection [ICRP], 2008 ). Additional complications when studying plants, and about which relatively little is known, include the radio-sensitivity of different above- and below-ground organs (for example buds, roots, and root hairs), significant differences in life-span of different species and seasonality in responses. Further, in radiobiology, IR-induced effects are generally divided into deterministic effects that occur when a dose-threshold is exceeded and can be estimated by endpoints such as mortality, morbidity or reproductive success, and stochastic effects that are probabilistic and measured by endpoints whose incidence increases proportionately with dose ( United Nations Scientific Committee on the Effects of Atomic Radiation [UNSCEAR], 2006 ). The importance of stochastic effects in plant radiological protection, especially at chronic low doses, is unclear. In 2005, a European Commission report suggested that, despite observed impacts on some individuals, stochastic effects arising from chronic low doses of IR may be of little relevance to protecting populations of non-human biota, although the report did acknowledge that effects at a population level are not well known ( Björk and Gilek, 2005 ). This is in part because stochastic effects can produce differences between not only individuals but also, for example, between different parts of a plant ( Esnault et al., 2010 ). This presents some statistical challenges not least because in plants with a small biomass data is often pooled from several individuals and many responses can be hidden. Esnault et al. (2010) suggested that there is a need for experiments to generate high definition intra-plant data. Such data are not yet available and the importance of stochastic effects to the protection of flora, although unlikely to be significant, are not clear.

Further, many areas on Earth have a naturally enhanced background of IR ( Saghirzadeh et al., 2008 ) and, for example, it has been suggested that the chronic exposure at Ramsar in Iran can have effects on plants up to a dose rate (4 μGy h -1 ) that is only about 10 times higher than the global average background ( Ghiassi-Nejad et al., 2003 ) and is at the low end of the range of the DCRL for sensitive plants. Effects at similarly ‘ultra-low’ dose rates have been reported at Fukushima ( Hayashi et al., 2015 ). In addition, many studies that have contributed to the development of DCRLs have used field locations with dose rate gradients as the basis for their research design. An association between existing environmental contamination and effects is only one indicator of cause, because locations with different dose rates can vary in other ways, often to an unknown extent, in both systematic and specific respects, i.e., there can be significant confounding factors. For example, due to the short-half lives of most of the radioisotopes emitted from the Chernobyl NPP (Figure 4 ) most contaminated locations with elevated dose rates post-1987 had much higher, and short-lived, dose rates during 1986 in the immediate aftermath of the accident. At Chernobyl, when attempting to assess the effects of a particular dose rate it can be difficult to separate any lasting effects of 1986–1987 dose rates from any effects of the post-1987 dose rates. Clearly, although there are established transgenerational effects of IR, in studies conducted a significant time after the accident this may be less of a complication.

FIGURE 4. The Activity of radionuclides in the environment from the accident at Chernobyl. The total activity of radionuclides released from Chernobyl over a few days in 1986 was in excess of 11 EBq. Much of this was short-lived radionuclides such as 33 Xe (6.5 EBq, λ = 5.3 days), 132 Te (1.15 EBq, λ = 3.25 days), 131 I (1.76 EBq, λ = 8 days), 99 Mo (0.2 EBq, λ= 2.79 days), 141 Ce (0.2 EBq, λ= 33 days). After a few years the remaining radioactivity was dominated by 137 Cs, 134 Cs plus some 90 Sr and 241 Pu. Radioactivity is now dominated by 137 Cs. Many of the short-lived radionuclides are gaseous and emitted to the atmosphere but there was still a dramatic decrease in the dose to terrestrial organisms in the first year after the accident. (Full calculations given in Supplementary Data Sheet S3 ).

In order to aid discussions of the effects of IR on plants, we compiled published studies of the effects of IR on plants and classified them according to exposure to IR (Figure 5 ). It is clear that there is a paucity of data on the effects of chronic low doses of IR on plants that were generated under controlled conditions. The studies that have investigated the effects of IR at contaminated sites clearly, and crucially for managing them, reveal what is happening at these sites under field conditions but they provide primarily associative evidence that the cause of any effects is exposure to chronic low-level IR. Published field studies of the effects of IR on plants are essentially epidemiological and, we suggest, attribution of cause should therefore meet the relevant criteria of causality. In epidemiology, the nine Bradford Hill criteria for establishing if association might be cause have not only a long-established use as…‘the most frequently cited framework for causal inference in epidemiology’… but also interpretations fit for the molecular age ( Fedak et al., 2015 ). They are used in studies of the effects of IR on humans ( McLean et al., 2017 ) and we suggest that they could be more widely used in plant studies. Table 1 highlights that radioecologists have, mostly in a short time frame and under challenging conditions, generated significant data for some of these criteria. In the last decade, there have been calls for research that would, in effect, help fill radioecological gaps in the Bradford-Hill criteria, e.g., investigations of plant populations exposed to low doses of IR over a number of generations (e.g., Saghirzadeh et al., 2008 ), but few such studies have been reported or been focused explicitly on the relevant criteria. We emphasize that now data are available for some of the criteria in Table 1 , future studies guided by the other criteria would be useful in determining how chronic low-dose IR affects plants over several generations.

FIGURE 5. The doses and dose rates used in studies of the effects of IR on plants. Where possible, dose rates and total doses from published studies were determined from methods sections or by calculation of them from details provided. The bars on the points above represent the ranges of dose and/or dose rate used in the published works. Studies in the field are coded in green, those from the laboratory in black. Although not all published studies could be included because doses or dose rates were not provided or could not be calculated, this significant selection of the published data shows that there are few laboratory studies at low doses, especially for chronic exposures (Details of studies are in Supplementary Data Sheet S4 ).

TABLE 1. Preliminary assessment of data for observed effects on plants being caused by chronic low doses of ionizing radiation (IR) at about derived consideration reference level (DCRL) dose rates using the Bradford-Hill criteria.

Thus, overall, the frameworks used for radiological protection of the environment have more solid foundations, including those related to causality, at acute high doses and for humans and other animals than for plants. Here we use data about the effects IR on plants at all doses to provide a new synthesis that highlights, for protection of the environment, the importance of generating data under controlled conditions from multiple generations of plants growing at chronic low doses of IR.

The Effects of Ionizing Radiation on Plants

The effects of IR in higher plants are of interest to agriculture, horticulture, ecology, and space science. We suggest that four particular aspects of plant biology provide a vital context for understanding the effects of IR. First, the light reactions of photosynthesis are initiated with photolysis of water – a processes with the same products as the radiolysis of water and that can result in the formation of enormous amounts of oxidative radicals that plants are generally able to disarm because of their high production of anti-oxidants ( Willey, 2016 ). Second, in multicellular plants the dividing cells occur in meristematic tissues that have quiescent centers with functional equivalence to stem cells but that are not identical to them and do not have, for example, the same p-53 mediated apoptotic capacity as animal stem cells. Meristems in plants are a biologically distinct product of an independent evolution of multicellularity ( Fulcher and Sablowski, 2009 ) and the effects of IR on them are not well known. Third, the meiotic divisions that produce the gametophyte generation in reproductive organs in plants are separated in each generation by many vegetative cell divisions in the sporophyte generation – i.e., plants have an alternation of generations and no reserved germline. And fourth, although tumors can occur in plant tissues ( Athena Aktipis et al., 2015 ), because of different controls on groups of multiplying plant cells ( Doonan and Sablowski, 2010 ) and the reduced probability of metastasis in organisms without circulatory systems, plants do not suffer adverse cancerous effects of tumors to anything like the same extent as many animals. In plants there are, therefore, not likely to be the same stochastic effects of IR as in animals in which many such effects are cancers. Thus, current knowledge about the effects of IR on multicellular organisms is dominated by knowledge of effects on organisms with less anti-oxidant capacity than plants, that have stem cells and germ lines without exact plant equivalents, and that suffer stochastic effects unlikely to occur in plants.

Molecular Biological Effects

Mutagenesis.

The botanist Hugo de Vries introduced the concept of ‘mutation’ and suggested in 1904 that X-rays might induce them ( Blakeslee, 1936 ). Thus, some of the earliest attempts at mutagenesis used plants exposed to X-rays and then radium ( Stadler, 1928a , b , 1930 ). More than 2500 crop cultivars in current use, and that produce a significant proportion of all food consumed by humans, were developed using mutagenesis induced by acute high-dose IR (10 s of Gy or more) ( Cheng et al., 2014 ). Purposeful IR-induced mutagenesis continues to play a significant role in the improvement of the world’s most important crops, e.g., rice and wheat, including through the use of ion-beams ( Cheng et al., 2014 ; Zhang et al., 2016 ). The FAO/IAEA Mutant Variety Database registers numerous new cultivars each year, including many produced using IR. Such mutagenesis also has an important role in the development of new horticultural varieties (e.g., Taheri et al., 2014 ).

Oladosu et al. (2016) suggest that the changes in DNA during IR-induced mutagenesis can be of three sorts: (1) intragenic (point mutations within a gene sequence), (2) intergenic (inversions, deletions, duplications, translocations of DNA), and, (3) changes in chromosome number. Compared to other mutagens, IR can induce a relatively high incidence of DSBs in DNA. Mutagenesis experiments have frequently confirmed this with plants (e.g., Doná et al., 2013 ). High DSB incidence accords with the large deletions reported by Sato et al. (2006) and the many indels and copy number variations reported by Cheng et al. (2014) but single stranded breaks (SSBs) and other damage still occurs widely after IR exposure. For example, Cheng et al. (2014) analysis of Red-1 rice, a variety produced via IR mutagenesis, described altered sequences in approaching 9% of all genes primarily due to a rich variety of single nucleotide polymorphisms (SNPs). SNPs are not a simple product of strand breaks but of a plethora of differences, including in DNA repair systems. Further, the simple oxidation of bases can constitute 10–15% of all such DNA damage ( Doná et al., 2013 ). Together with increases in alkali-labile sites, DNA–DNA, DNA-protein cross-links ( Ventura et al., 2013 ), and long-known cytogenetic effects, such data show that acute high-dose IR can induce not just DSBs but essentially the full gamut of DNA damage in plants.

Mutagenesis experiments often note the capacity of plants to quickly repair a significant proportion of the damage caused by acute exposure to IR. For example, for horticultural breeding Taheri et al. (2014) note that Curcuma alismatifolia recovered significantly within 24 h from a 10 Gy dose and recommended that 20 Gy or more is necessary for useful net rates of mutagenesis. A frequent limitation to the use of comet assays in plant studies of the effects of IR on DNA is the significant capacity that plants have for DNA repair ( Lanier et al., 2015 ). This is also a reminder that an acute external dose of IR is one of the mutagenic scenarios for which an acute dose is truly possible – in contrast to chemical mutagens that often continue to persist in a biological system after exposure has ceased. For example, in comet assays the ‘tails’ of damaged plant nuclei take longer to disappear after acute chemical exposure than after acute IR exposure ( Ventura et al., 2013 ). Acute doses of 10–100 s Gy of IR are reported to produce ‘net’ rates of mutation from 10 -9 base pair (bp) mutations per Gy ( Fulcher and Sablowski, 2009 ) to 6.13 × 10 -6 bp mutations per 500 Gy ( Sato et al., 2006 ). Much radiological assessment of possible effects at low doses is based on extrapolation (using the linear-no threshold assumption) from observed effects at acute high doses down to low doses. In plants, such extrapolations, which assume a directly proportional relationship between dose and mutation rate, suggest that doses in the μGy and even mGy range will not induce mutation rates significantly above those that occur routinely in plants under field conditions. We suggest, however, that measurements of ‘net’ rates of mutation after acute exposure are unlikely to be appropriate for extrapolation to chronic exposures. With acute exposure, the period of DNA damage is essentially not contemporaneous with the subsequent period of repair, so comet assays in particular indicate that, even if it was appropriate to describe a ‘net’ mutation rate under these circumstances, the capacity for repair is sufficiently great that it is very practically challenging to measure effects with sufficient alacrity.

A variety of post-Chernobyl studies have suggested that chronic low-level irradiation of plants induces greater rates of mutation than predicted from acute high dose studies. Kovalchuk et al. (2000b) , using wheat planted in soil contaminated from the Chernobyl NPP, suggested that a dose of 0.3 Gy over a growing season (assuming 100 days, i.e., 2400 h, gives dose rate of c. 125 μGy h -1 ) produced a sixfold increase in mutation rate. Studies of Arabidopsis growing wild at Chernobyl have revealed that the incidence of genetic effects correlate with doses in contaminated areas ( Abramov et al., 1992 ) as have a number of studies of Scots Pine ( Geras’kin et al., 2016 ). The planting of previously unexposed populations of plants into contaminated soils at Chernobyl has suggested elevated mutation rates at dose rates around and sometimes below 100 μGy h -1 . Overall, investigations of mutagenesis are a reminder of how high acute doses have to be in order to produce agriculturally or horticulturally useful mutation rates in plants, and also that the mutation rates reported at acute high doses are not particularly meaningful as ‘net’ rates because damage and repair are not occurring simultaneously. Although mutation rates reported in some chronic low doses studies are higher than predicted by extrapolation from high doses, and assuming the possibility of confounding factors in such studies can be discounted, it is still possible that such mutation rates are associated in some way with IR. Resolving this inconsistency between IR effects reported at acute high and surprisingly low chronic doses might be aided by an understanding of the processes of DNA repair in plants.

DNA repair mechanisms that help reverse oxidative adducts and other chemical changes to DNA occur in higher plants, as does the induction of the cell cycle checkpoints necessary for the repair of strand breaks ( Hu et al., 2016 ). Although the details of many of these processes are less well known in plants than in other organisms, it is clear that the mechanisms in plants for repairing strand breaks in particular are similar, though not identical, to those in other eukaryotes ( Hu et al., 2016 ). In general, plant cells have greater resistance to the production of DSBs by IR and repair them more quickly than do animal cells, such that at a given dose they carry about 1/3 the DSBs that animal cells do ( Yokota et al., 2005 ). This accords with known differences in radiosensitivity between plants and many animals and is likely a product of plant life strategies. Both the regular initiation of meristematic and reproductive tissue from vegetative cells and a sessile life-style that has to involve withstanding regular environmental insult from DNA-damaging agents, such Al 3+ in acidic soils ( Willey, 2016 ), promotes both a significant capacity for DNA repair and a resistance to the net effects of DNA damage. Interestingly, in contrast to multicellular animals, mutations of DSB repair proteins in plants tends just to reduce biomass production rather than change fundamental aspects of development ( Manova and Gruszka, 2015 ) – emphasizing that the developmentally plastic modular growth form of plants provides a way not available to animals of resisting damage from mutagens.

In plants, the KU70/KU80 heterodimer recognizes DSBs, with ku70 and ku80 mutants being especially sensitive to DSB-inducing agents ( Weimer et al., 2016 ). As in animals, in plants the MRN complex binds to DSBs and the RPA complex to SSBs, activating, respectively, the ATM and ATR pathways ( Hu et al., 2016 ). In plants, ATM triggers the expression of SOG1 ( S uppressor O f G amma response 1) a transcription factor that acts as a key regulator of DNA repair processes ( Yoshiyama, 2015 ). ATR acts through WEE1 to arrest the cell cycle and, probably through SOG1, to activate DNA repair. There are cyclins in plants that control cell cycle progression and the cyclin-dependent kinases (CDKs) that in turn control their activity. Cyclins are particularly functionally diverse in plants with, for example, CYCB1s and CDKB1s helping to regulate the repair of DSBs by either non-homologous end joining (NHEJ) or HR ( Weimer et al., 2016 ). NHEJ, in which broken DNA strands are often simply ligated back together by LIG4 (DNA ligase 4) and XRCC4 (X-RAY REPAIR CROSS COMPLEMENTATION PROTEIN 4) ( Bray and West, 2005 ), can result in altered DNA sequence if nucleotides are lost during breakage. At least three variations of the NHEJ pathways occur in plants ( Charbonnel et al., 2011 ). Much HR repair uses a homologous chromatid as a template for high fidelity repair of DSBs and, therefore, occurs after the S phase of the cell cycle when chromatids have been duplicated but it can also occur between chromosomes or between homologous regions of a chromatid during the G1 phase of the cell cycle. Homology search, and strand incision, on sister chromatids is initiated by RAD51, of which there are five paralogs in plants. Weimer et al. (2016) suggest that a high level of redundancy in NHEJ and HR repair in plant cells contributes to, compared to animal cells, high resistance in plants to DSB-inducing agents. Redundancy in this context means not only a much greater capacity than is usually necessary but also a resilient capability based on multiple genes or pathways.

Acute high doses of IR to plants have been useful in elucidating the details of many of these DNA repair pathways but there are also reports of chronic low doses of IR inducing DNA repair – with studies of HR at Chernobyl, for example, providing a good example ( Kovalchuk et al., 2000a , 2003 ). In general, based on conclusions drawn from mutagenesis studies, the sensitivity of induction of DNA repair in low dose/low dose rate IR regions is greater than predicted from that at acute high doses. It has also been shown that, at 100 mGy h -1 exposure, the radiosensitivity of plants to DNA damage declines with age ( Biermans et al., 2015 ). The processes of DNA repair have evolved as a protective response to environmental insult and there are many other environmental variables that, at low intensity, cause an increase in the rate of DNA repair ( Willey, 2016 ). Elevated rates of DNA repair at chronic low-dose rates are not necessarily detrimental even at the cellular level and it is certainly necessary to investigate their impacts at higher levels of biological organization to understand the biological significance of the effects.

Gene Expression

Numerous authors have reported, in response to IR exposure, changes in gene expression in plants. In general, in experiments using high acute doses that have affected plant growth, the expression of 100 s, even 1000 s, of genes can change. This accords with the magnitude of changes in gene expression induced by, for example, growth change-inducing drought, temperature or salinity stress. No synthesis has yet emerged as to which particular pathways or processes are most effected by exposure to IR. Genes with altered expression generally include some that are involved in DNA repair and anti-oxidant defenses but also many others involved in a notable diversity of processes, including many Gene Ontology (GO) categories. For example, with acute doses of 100–2000 Gy over 24 h, Kim et al. (2014) revealed that the most numerous genes with changed expression had a role in; (a) catalytic activity, (b) the endomembrane system, and (c) active in metabolism. Hwang et al. (2014) using doses of 200 Gy gamma irradiation and 40 Gy Ion Beam irradiation over 24 h, noted gene expression related to sugar and starch metabolism were particularly affected. Published data include a notable proportion of reports of changes in flavonoid (e.g., Van Hoeck et al., 2017 ) and lignin metabolism (e.g., Lee et al., 2014 ). Park et al. (2015) investigated the radiation responsive OsGIRP1 gene at 100–400 Gy in rice, revealing that its expression helped to control the degradation of key photosynthetic proteins that might have been damaged by high dose IR.

Kovalchuk et al. (2007) revealed differences in gene expression in Arabidopsis thaliana exposed to a total of 1.0 Gy as an acute dose (delivered at 90 Gy h -1 ) and as a chronic dose (21 days at 1.8 mGy h -1 ). The acutely exposed plants demonstrated up-regulation of genes involved with DNA repair, oxidative stress response and signal transduction pathways, whilst the chronically exposed plants showed no alteration of expression profiles of genes associated with DNA repair or cell antioxidant response. Goh et al. (2014) demonstrated a similar effect at 200 Gy, which induced changes in gene expression when spread over hours but when spread over 2 or 3 weeks had no effect on gene expression. There is also evidence that the stage of plant development affects both the expression of IR sensitive genes in unexposed plants and their general plant response to IR ( Biermans et al., 2015 ). Kimura et al. (2008) studied gene expression changes on rice seedling leaves post low-dose exposure to IR from contaminated soil in the Chernobyl vicinity. Experiments showed that >500 genes responded to radiation. Up-regulated genes were associated with cellular processes and signaling actions to specifically include defense, cell wall synthesis, and secondary metabolite biosynthesis. Down-regulated genes indicated suppression of information and storage functions alongside non-specific metabolic pathways. Sahr et al. (2005) reported changes in the expression of 46 genes involved in fundamental cellular processes in the roots of Arabidopsis from internal dose rates of 50–100 μGy h -1 from 134 Cs. It seems clear, therefore, that not only high acute doses but also quite low chronic doses of radiation can affect gene expression in plants. Although the pathways and processes particularly effected are not clear, there are indications that over time the effect on gene expression at chronic low doses might attenuate. It should, however, be noted that genomic technologies are sensitive, so changed expression in a few tens of genes out of many thousands does not necessarily lead to adverse effects at higher levels of biological organization.

Effects on Plant Proteomes and Metabolomes

Acute high doses of IR to plants change their protein and metabolite profiles. For example, Roitinger et al. (2015) using atm and atr mutants reported changes in ATM- and ATR-dependent pathways and in phosphorylation patterns of the proteome. In rice varieties produced by IR mutagenesis Hwang et al. (2015) report, for example, changed carbohydrate and protein degradation metabolism. Often such changes include those to anti-oxidant systems ( Goh et al., 2014 ; Ramabulana et al., 2015 ). Several studies have shown that γ-radiation has an effect on chlorophyll content. Alikamanoǧlu et al. (2007) found that total chlorophyll content (from both chlorophyll a and b ) increased when Paulownia tomentosa was exposed to 5–50 Gy at a rate of 10 Gy h -1 . Chlorophyll content was also significantly increased in red pepper ( Capsicum annum ) at 16 Gy ( Kim et al., 2011 ). As with changes reported in gene expression during high-dose exposure, such data suggest that; (1) the magnitude of changes in proteomes and metabolomes is as expected from severe environmental stress, (2) what might differentiate IR-induced changes from those induced by other stressors is not yet clear, and (3) that few changes might be expected at much lower doses.

At Chernobyl, however, differences in seed proteins, have been reported between contaminated and control plots ( Klubicová et al., 2012 ; Rashydov and Hajduch, 2015 ), and Hayashi et al. (2015) reported changes in rice proteomes at ‘ultra-low’ level gamma doses. In Chernobyl seed studies, contamination levels of c. 20 kBq 137 Cs/kg soil plus c. 5 kBq 90 Sr/kg soil probably give doses to plants of no more than 100 μGy/h (though doses to plant parts might be different depending on internal accumulation of radioisotopes), whilst in the aforementioned Fukushima studies ( Hayashi et al., 2015 ) doses were a maximum of 4 μGy/h. Overall, proteomic data from field experiments on seeds at Chernobyl showed that plants growing in the zone responded similarly in their proteome to plants undergoing stress from heavy metals ( Danchenko et al., 2009 ). Thus, there is evidence of effects of IR on the proteome and metabolome at low chronic doses. However, again it must be remembered that many of the ‘omics’ techniques are very sensitive, and that sessile plants experience the environment as constantly changing and are, therefore, constantly responding to it. For example, plants respond daily to the day/night light cycle with profound changes in their proteomes and metabolomes. It is, therefore, vital to assess not just whether changes in genotypes, proteomes and metabolomes can be detected but whether these chronic low-dose induced changes translate into significant changes in phenotypes because it is, primarily, phenotypes that determine the fitness of individuals and populations in the environment.

Effects of IR at Whole Plant Level

Acute high external doses of IR have long been known to affect most aspects of shoot growth, with recent reports including effects on developmental timings ( Nishiguchi et al., 2012 ; Sidler et al., 2015 ), morphology ( Celik et al., 2014 ; Sever-Mutlu et al., 2015 ), anatomy ( De Micco et al., 2014 ), and the development of bulbs ( Mostafa et al., 2015 ). As there have been for many years, there are recent reports that acute high doses, mostly to propagules, sometimes have positive as well as negative effects on subsequent growth. For example, at 10 Gy given over 10 s Hamideldin and Hussien (2014) , using different potato varieties, noted some positive as well as negative effects on subsequent height, leaf area, stem diameter, and tuber diameter. Several studies carried out in the immediate aftermath of the Chernobyl accident not only confirmed the sensitivity of the shoots of some species to IR and but also detailed a variety of effects that supplemented significantly knowledge about acute effects of IR in the field. These studies have now been complemented by some research to elucidate the effects of chronic low doses.

Mousseau et al. (2013) using wood cores of Pinus sylvestris at Chernobyl provided evidence that trees in locations near the reactor had different, and more variable, growth rates of above ground parts after irradiation from the accident. Although these effects were correlated with dose rates in 2009, it was not possible to disentangle the effects of high acute post-accident doses from any due to subsequent lower doses. At Fukushima, studies of Abies firma growth from before and after the accident also found effects on growth that, although they correlated with dose rate in 2015 were not necessarily produced by it ( Watanabe et al., 2015 ). The extensive studies carried out on P. sylvestris in the Bryansk region of Russia since 2003, and that include detailed dose calculations, can more clearly distinguish effects caused by chronic low doses in the period remote from the accident. In general, these studies ‘are consistent with an international recommendation to consider radiation exposure of 100 mGy/a (c. 10 μGy/h) as a margin for biota safety in chronic irradiation’ ( Makarenko et al., 2016 ). However, recent studies at this location have supported the assertion that P. sylvestris is particularly sensitive to IR. They have noted an increased frequency of gene mutations at 1.14 μGy/h (10 mGy/a – below the low end of the DCRL for P. sylvestris ) and changes in anti-oxidant concentrations at 5.7 μGy/h (50 mG/a – just in the range of DCRL for P. sylvestris ) ( Volkova et al., 2017 ). It is notable that of the many endpoints measured in these studies, there are some in which significant effects of IR are reported, especially cytogenetic ones, but that these are not, overall, adverse enough at the level of the individual or above to merit a reconsideration of the DCRLs. At the Semipalatinsk nuclear test site in Kazakhstan, studies of Koeleria gracilis (crested hair grass) that had inhabited for 50 years soils contaminated with radioactivity and with a current dose rate of 4–285 mGy/a, also showed cytogenetic effects at the highest doses but no morphological effects ( Geras’kin et al., 2012 ). Seeds collected from the most exposed plants did not differ in their response to irradiation suggesting that IR has not exerted any selection pressure over 50 years and that recommended dose limits were appropriate.

Studies carried out near Chernobyl have also provided evidence of effects on whole plants at chronic low doses. In studies on P. sylvestris planted after the accident at Chernobyl and investigated 25 years later, normalized dose rates for the period, based on the sum of both internal and external doses, of 10 μG/h and less were related to significant cytogenetic and morphological effects ( Yoschenko et al., 2011 ). At 40 G/h there were significant effects on apical dominance, with cytogenetic effects being related to incidence of morphoses. However, in experiments with Lemna minor , which enables detailed developmental analysis under controlled conditions, doses of 80 μG/h to 4.95 mGy/h had no effect on physiological, morphological, or developmental parameters ( Van Hoeck et al., 2015 ). Overall, therefore, some effects of chronic low dose IR on individual plants shoots have been reported at the low end of DCRL ranges but it has not been suggested that they are significant at the population or community level.

Plants are well known to respond to soil stresses via changes in their roots (e.g., Bochicchio et al., 2015 ), which can then affect overall plant function. Gunckel (1956) noted that roots are shielded from much α and some β IR by the soil which, together with practical difficulties of experimenting with roots, may have contributed to relatively few studies of the effects of IR on roots having been reported. However, the fact that the long-term fate of much contamination following accidents at Kyshtym, Chernobyl, and Fukushima has been soil root zones highlights how important the effects of IR on roots might be. This is particularly relevant in the earliest stages in the plant life-cycle that have particular proximity to the soil and that are generally the most susceptible to the effects of stress. Further, even for the biologically mobile Cs, accumulation from root uptake is almost always higher in roots than shoots ( Danchenko et al., 2016 ) – a distribution that is generally more pronounced the less mobile a radioisotope is.

Acute high doses of IR have long been known to quickly affect roots, primarily via the root meristem. Gray and Scholes (1951) found that irradiated Vicia faba roots (1.2 Gy) had inhibited growth and that exposing only root meristems had the same effect as exposing the entire root system. In pea and maize, survival of root apical meristems post-irradiation event (3–32 Gy) showed that radioresistance at different points in the cell cycle varied slightly between species, and that there were overall differences in resistance depending on phases of early growth ( Gudkov and Grodzinsky, 1982 ). Duration of individual phases of the cell cycle and overall cell cycle period was also changed depending on species. Exposing Arabidopsis roots to 3 kGy inhibited elongation from the root tip and induced root hair elongation and cell expansion ( Nagata et al., 2004 ). Some studies report either root elongation or growth inhibition depending on dose ( Maity et al., 2005 ; Yadav, 2016 ). Acute doses from ion beams on root meristems indicate that they are a key exposure site ( Zhang et al., 2016 ) and several studies note the role of changes in ROS in roots after acute high exposures (e.g., Nagata et al., 2004 ).

Biermans et al. (2015) using solution cultures reported that, over 7 days, doses of 11 mGy/h from 241 Am reduced the root growth of Arabidopsis and affected its dry matter but that lower doses did not. Sahr et al. (2005) reported that dose rates of 100 μGy/h (from 60 kBq/L 134 Cs in a solution culture) affected Arabidopsis root growth but that doses of 50 μGy/h did not. Below these dose rates there are no reports of morphological changes, although several studies have reported genetic and cytogenetic changes. A standard Allium root tip test revealed a linear relationship between dose and chromosome aberrations up to a dose of about 80 μGy/h in Chernobyl contaminated soil ( Kovalchuk I. et al., 1998 ; Kovalchuk O. et al., 1998 ). Similar studies with 90 Sr contaminated sites have also shown similar effects at even lower dose rates. In naturally enhanced background areas at Ramsar (with up to 12,500 Bq 226 Ra/kg soil and doses of up to 100 μGy/h) Saghirzadeh et al. (2008) also described chromosomal aberrations in Allium root tips. However, in neither of these studies were threshold relationships tested.

There is, therefore, much to be learned about the effects of IR on the ‘hidden half’ of plants. It seems likely that there are detectable effects of chronic low doses at the genetic and cytogenetic levels at the low end of DRCLs, and perhaps below. There is some evidence of morphological, or other whole root effects, close to DCRLs. Downie et al. (2015) emphasized how often roots are examined artificially flat and that there is still a lack of focus on root-environment interactions. Methods for examining roots in situ have been developed for a variety of media including soil ( Yuan et al., 2016 ), paper wick ( Adu et al., 2014 ), and gels ( Bochicchio et al., 2015 ), which would be very useful for examining the effects of chronic low dose IR on root systems.

Overall, plant morphology has long been known to alter when exposed to high doses of radiation. In recent years, advances in image-based analysis has enabled the study of phenomics. Phenomics is concerned with phenotypic variation and its causes, effects, and implications. Houle et al. (2010) explained that understanding of phenomics is far less comprehensive than that of genomics, and we suggest that the same can be said to an even larger extent within the field of radioecology. Morphometrics, the quantitative analysis of shape and/or form of a subject is fast-becoming a key method of producing high-throughput data for phenomics. We suggest root and shoot studies in radioecology should employ high throughput image analysis to complement the increasing plant stress biology phenomic data – it is a powerful way of analyzing subtle environmentally induced changes in plants.

Reproductive and Transgenerational Effects

Reproductive organs are often especially sensitive to the effects of environmental stress, with potential implications at the community and population level. Thus, in Caenorhabditis elegans investigations of the impact of IR often use reproductive end points ( Buisset-Goussen et al., 2014 ). In general, propagules in plants almost always have very high, often extremely high, levels of redundancy, i.e., the toll of adverse environmental effects (which essentially always exist in the wild) on success is overcome by the high numbers produced. There are many reports that acute exposure of seeds to high dose rates of IR produce hormetic effects on subsequent growth (recently, e.g., Maity et al., 2009 ; Marcu et al., 2013a , b ; Ahuja et al., 2014 ; Yadav et al., 2015 ). The effects are generally short-term and the role of, for example, heating or commensal micro-organisms in producing the effects is unknown. Acute high dose rates have also been shown to affect a variety of seed constituents (e.g., Jan et al., 2012 ; Tilaki et al., 2015 ; Vaizogullar and Kara, 2016 ), which might affect subsequent germination and growth. In the field, soon after the Chernobyl NPP accident, dose rates around 2 mGy/h produced lethal embryo mutations in A. thaliana ( Abramov et al., 1992 ) and extensive studies of P. sylvestris near the Chernobyl NPP have shown that plants that received total doses of >2 Gy in areas of high short-term contamination had decreased reproductive ability and that this effect lasted for more than a decade ( Fedotov et al., 2006 ). Boubriak et al. (2008) reported in pollen collected from control and contaminated sites near the Chernobyl NPP different IR exposure affected the rate of DNA synthesis. In general, seeds and pollen have high resistance to environmental stressors but, perhaps because some IR can penetrate their protective coats, it seems that relatively low total doses delivered at high dose rates can have effects, including hormetic effects, whilst large doses received at high dose rates produce significant adverse effects.

Based on studies with 94 species ( Kordium and Sidorenko, 1997 ) and 111 species ( Møller et al., 2016 ), it has been suggested that, at time periods remote from the high post-accident doses, in the area around the Chernobyl NPP about 10% of species have slightly decreased pollen viability associated with enhanced doses of IR. Møller et al.’s (2016) study was carried out in 2008–2011 and included maximum dose rates of about 150 μGy/h. In long-term studies of P. sylvestris in the Chernobyl-contaminated Bryansk Oblast of Russia, germinating seeds have rates of cytogenetic damage of up to 1.3% that correlate with dose rate ( Geras’kin et al., 2011 ), and that is repeated elsewhere at even lower dose rates ( Evseeva et al., 2011 ). Several detailed studies of plants growing in the East Urals Radioactive Trace, which has the longest history (1957 onwards) of any widely studied radioactively contaminated site and has dose rates of up to 240 mGy/y ( c. 28 μGy/h), have shown dose-dependent effects on germination or viability of seeds of Taraxacum officinale ( Pozolotina et al., 2012 ), Melandrium album ( Antonova et al., 2013 ), and Leonurus quinquelobatus ( Karimullina et al., 2015 ). Several authors have noted that chronic low dose rates of IR can make germination more variable, particularly in response to weather conditions ( Antonova et al., 2013 ; Geras’kin et al., 2016 ) and other soil contaminants ( Evseeva et al., 2009 ; Karimullina et al., 2015 ). There is, however, evidence from studies in Bryansk, Russia, that such effects do not alter the overall reproductive capacity of P. sylvestris ( Geras’kin et al., 2016 ).

Studies in areas contaminated from the Chernobyl NPP accident (in particular with the relatively sensitive P. sylvestris ), and especially in the EURT, have shown that chronic low dose effects on plant propagules can be sustained for many generations. Boratyński et al. (2016) hypothesized that effects of IR on life history responses might be sustained for generations in the absence of irradiation. Wild carrot plants, sampled from around Chernobyl (0.08–30.2 μGy/h) and then grown in uncontaminated soils in a greenhouse showed correlations between previous radiation dose and the timing of developmental events. The presence of trans-generational effects has perhaps helped prompt some discussion about ‘adaptation’ of plants to chronic low-level doses of IR. For example, studies of flax and soya seeds grown over several generations near the Chernobyl NPP have shown differences in seed constituents and prompted suggestions of adaptation to chronic low dose IR ( Gabrisova et al., 2016 and references therein), as have effects of high doses on pollen ( Boubriak et al., 2008 ), the ability of plants from Chernobyl to resist the effects of mutagens ( Kovalchuk et al., 2004 ) and studies at a number of other contaminated sites (e.g., Geras’kin et al., 2013 ; Møller and Mousseau, 2015 ; Boubriak et al., 2016 ). These references, and references therein, provide evidence that at chronic low doses in the range of a few 10 s of μGy/h, some plants can have increased heterozygosity, increased rates of DNA repair, and increased variability of key seed properties and constituents. There is also evidence of some increase in radioresistance, at the DNA and cytogenetic level, in some species at these dose rates. We suggest that great care has to be used in interpreting these effects as ‘adaptation.’ An adaptation increases the fitness of an organism, i.e., its ability to survive under conditions of natural selection ( Futuyama, 2009 ). No data that we are aware of has actually demonstrated this to be the case for plants exposed to chronic low levels of IR. However, an increase in diversity of many phenotypes is common under other stress conditions and, in some instances, has been shown to provoke the evolution of an adaptation to them.

There have also been some investigations of epigenetic effects of chronic low-dose IR on plants. Epigenetic effects are inheritable changes in phenotypes that cannot be explained by changes at the genetic level ( Waddington, 1942 ; Weinhold, 2006 ). They occur because of, for example, heritable changes in methylation of DNA (which effects gene expression rather than sequence) or changes in histones (which control DNA packing and unpacking). Exposure to stressors has the potential to reshape not just the genome but also the epigenome, changes to the later probably being quite common in organisms ( Grossniklaus et al., 2013 ). There is, however, some debate about how significant these effects might be in the long-term in plants ( Pecinka and Scheid, 2012 ), in part because of the higher basal rates of methylation in plant DNA than animal DNA. Nevertheless, epigenetic changes can be important in plants. In the halophytic species Mesembryanthemum crystallinum , under drought conditions the plant has the ability to switch metabolic pathways from C 3 -photosynthesis to Crassulacean Acid Metabolism (CAM). This change of pathway involves profound changes in the control of, for example, stomata function and enzyme activity, and is mediated to changes in DNA methylation ( Dyachenko et al., 2006 ). High doses of radiation (10 Gy) that effect plant development of 20 days old plants change the expression of enzymes that mediate DNA methylation ( Sidler et al., 2015 ) and P. sylvestris trees exposed to high doses post-Chernobyl have hyper-methylated DNA ( Kovalchuk et al., 2003 ). Germinating soya bean seeds from plants grown in Chernobyl-contaminated soil for six generations produced rootlets with slightly enhanced levels of DNA methylation ( Georgieva et al., 2017 ).

Overall, chronic low doses (in a range as low as 5–50 μG/h) have been reported to have detectable effects on plant seeds. The data on which this assertion is made is primarily field based and, given that there is some evidence that effects can be sustained through the generations, an assumption that current exposure to IR explains currently observed effects must, in a number of instances at least, come with the usual caveats about confounding variables in field studies. It must also be noted that the effects tend to be of low frequency in a structure that is generally produced with a high level of redundancy. There is, overall, little real evidence of any adaptation to chronic low-level IR across generations ( Møller and Mousseau, 2016 ) and we suggest that if it occurred to a significant extent it would have been more securely established in field studies – many plant species can adapt quickly and obviously to, for example, the presence of inorganic and organic contaminants in soils ( Willey, 2016 ). In addition, environmental variables such as temperature or water availability frequently have significant, often catastrophic, effects on the production or viability of seed in any given year without necessarily affecting populations in the long-term. Against such a background, the significance of some low-incidence effects on reproductive propagules just below the DCRL range needs to be assessed at the population and community level but seems unlikely to be significant to populations in natural ecosystems.

Effects on Plant Populations and Communities

Key insights into plant population biology and community ecology have been derived from studies of stress and disturbance. From early on in the nuclear age, high dose IR of 10–100 s of Gy was used not just to understand its effects but also to gain fundamental ecological insights using its unique properties as a stressor – high activity point sources produced predictable, continuous gradients of stress and could be switched on and off using shielding. For example, the United States Atomic Energy Commission’s experiments, primarily in the 1960s, with high activity point sources in a variety of ecosystems ( Jordan, 1986 ) informed early thinking about tropical forests in particular ( Lugo, 2004 ) and the results of studies at US nuclear weapons test sites in Micronesia probably influenced important conceptions of ecosystem ecology ( DeLoughrey, 2013 ). Aside from ecological insights, from these studies, and from those in the USSR, it became clear that populations of plants were most sensitive in the order trees > shrubs > herbs, and that coniferous trees were more sensitive than hardwood trees. It was originally suggested that sensitivity of plant populations correlated with chromosome size and number (e.g., Woodwell, 1962 ) but later syntheses of these experiments suggest a better correlation with proportion of non-photosynthetic to photosynthetic material ( Jordan, 1986 ). Plant populations that were killed by massive doses close to point sources had, when studied, not recovered decades later ( Stalter and Kincaid, 2009 ) but plants more distant from sources helped inform the early IAEA suggestion that a dose rate of 100 μGy/h or less did not affect plant populations.

Numerous studies post-Chernobyl in locations proximal to the reactor that received high acute doses added an impressive range of details to the understanding of high dose effects and, overall, supported previous suggestions about the adverse effects of high doses and of the sensitivity of plant populations. In particular, P. sylvestris was found to be particularly sensitive and Picea abies even more so ( Geras’kin et al., 2008 ). At sites contaminated from the Chernobyl accident together with other studies in Russia in the EURT and at U-mine tailings, lower dose rates (even at around previously suggested dose limits) have shown cytogenetic effects ( Geras’kin et al., 2013 ), decreasing significantly the dose rates at which effects have been demonstrated. The significance of these effects for plant population health is unclear – at U-mine tailing sites there is the possibility of chemical toxicity explaining some of the effects that might change populations and at Chernobyl-contaminated sites the possibility of persistence of effects from previous high dose exposure to populations might do so. At the Semipalatinsk test site, there is good evidence of cytogenetic changes at doses of 10 s μGy/h but also good evidence that it does not affect plant populations ( Geras’kin et al., 2013 ). Climate, soil type, species of plant, and the topographical and geological features of a region all affect the behavior and effects of IR in natural ecosystems. Research on the dynamics and effects of forest contamination in the long-term is still vital because, even though more than 30 years have passed since the Chernobyl accident, such a time period is only half of an average forest cropping cycle in many contaminated areas ( Takahashi et al., 2016 ). Overall, the evidence suggests that the cytogenetic changes found in the DCRL range probably do not affect population characteristics or that if they do the effects are subtle. Subtle effects may be of some ecological significance, with the magnitude of stress and disturbance from other sources perhaps playing a key confounding role.

Plant Biology and Ionizing Radiation – a Stress Response Context

The land surface is a challenging environment for life, not only because some of life’s essential resources (e.g., water and nutrients) can be in short supply but also because terrestrial environments tend to be more variable, both spatially and temporally, than the aquatic environment in which life originated. It was many years after it evolved that multicellular life adapted to the challenges of life on land, as evidenced by the relatively late colonization of the land surface by plants approximately 450 Ma ago. Numerous aspects of the biology of terrestrial plants are a product of the challenges of life on land. A biological hierarchy of effects that such challenges provoke can be used to visualize this (Figure 6 ). It is within such stress-response perspectives that the responses of terrestrial plants to IR might most fruitfully be viewed.

FIGURE 6. A biological hierarchy of effects in response to IR. The biological level at which effects of IR are described is important because there is not necessarily a direct relationship between effects at different levels. Increased mutation rates in DNA are commonly induced by IR but do not necessarily translate directly into effects on individuals or on individual fitness because plants have the capacity to repair them. If effects do, however, occur in individuals they do not necessarily affect their reproductive fitness or if they do, do not necessarily affect the functioning of communities and ecosystems. Protection of the environment from the effects of IR focuses on protecting biodiversity, populations, communities, and ecosystems and it is effects at these levels that are of significance rather than the detection of particular effects at the genetic level.

Higher plant shoots, for example, are adapted, often from molecular to population scales, to capture light, exchange gasses and transpire water – reflecting the key sources of stress to terrestrial plants. Taking these in turn, the land surface is often bathed in more light than plants need and photoinhibition of photosynthesis is common, even after the evolution of many adaptations to control it ( Raven, 2011 ). Photoinhibition results from loss of control over photolysis – the splitting of water in photosystem II (PSII) – producing ROS that damage photosynthetic machinery. Plants are adapted, at various biological levels and to different extents depending on their environment, to both minimize the production of oxidizing radicals that routinely leak from PSII and to nullify their effects as much as possible. Photoinhibition occurs when, relative to those produced from radiolysis at even medium dose rates, very high amounts of oxidizing radicals are produced. Photoinhibition is common not just in high light environments but also in northern latitudes when it is cold ( Takahashi and Murata, 2008 ). Many of the gasses that plants can be exposed to, naturally and as pollutants (e.g., CO 2 , SO 2 , NO x , and O 3 ) enter through stomata and dissolve first in the apoplastic solution, which causes, amongst other stresses, redox control challenges that can result in the production of ROS ( Shapiguzov et al., 2012 ). When fresh water is in short supply, which is a very important stress to higher plants on land ( Claeys and Inze, 2013 ), cellular redox balance is disturbed and unusual concentrations of ROS occur in cells. The production of ROS induced by these, and other, abiotic stressors adds to those that routinely leak out of mitochondria and those produced in response to a variety of biotic attacks.

There have been numerous reports of changes in anti-oxidant concentrations due to chronic exposure to low-dose IR (often with reports of oxidative ‘stress’) ( Einor et al., 2016 ; Volkova et al., 2017 ), and some studies consider that the ‘dominating effect of IR in cells is the formation of free radicals from water or oxygen’ ( Danchenko et al., 2016 ), but we suggest that these claims must be considered within an appropriate stress response context for higher plants. Not just in plants but in any aerobic organism, the disturbance of the delicate redox balance of life, rather than a change in anti-oxidant concentration, underpins oxidative stress. In plants ‘stress’ is usually defined as, for example, ‘any unfavorable condition or substance that affects or blocks a plant’s metabolism, growth, or development’ ( Lichtenthaler, 1998 ). Anti-oxidants exist to buffer the redox poise of a cell against change and a change in their concentration does not necessarily show that redox poise has been changed or that normal metabolism, growth, or development has been blocked. And stress produces radicals that are both a cause and a consequence of ‘stress’ – so changes in anti-oxidant concentrations might be a consequence of other damage rather than direct oxidative stress. The radicals produced by low doses of chronic IR even in contaminated environments are few compared to those produced routinely by life processes and by other stressors, and plants have adapted to deal with them at a full range of biological scales. It is possible that IR’s penetrating power, compared to UV for example, and its uncompartmentalized production of radicals, compared for example to those produced in plastids, is particularly challenging to life but we suggest that the reported changes in anti-oxidant concentrations should not be used as evidence that IR in currently contaminated environments is directly causing oxidative stress in plants, especially at the population and community level, and compared to that from other sources. Given the significant anti-oxidant capacities of higher plants and their adaptation at a variety of biological scales to oxidative challenge produced by variation in many other environmental variables, it seems unlikely that there will ever be evidence for biologically significant direct oxidative stress to plants from low-dose chronic IR.

When it occurs, chronic oxidative challenge can, of course, have significant effects on plants – tropospheric O 3 contamination is estimated, through oxidative effects, to decrease global production of staple crops by 3–12%, which equates to 10 s of $bi per year lost production ( Van Dingenen et al., 2009 ). The ‘O 3 equivalent’ of IR exposure provides a revealing comparison for the chronic long-term oxidative effects of IR. A preliminary comparison (Figure 7 ) suggests that activities of environmental IR not just at, for example, DCRLs but also some orders of magnitude above, will produce many fewer ROS than ambient O 3 concentrations and that increases in O 3 , which are occurring in many parts of the Earth’s terrestrial surface, are likely to be much more oxidatively challenging to plants than low-dose chronic IR. Given the stress response context for higher land plants and the established production of so many ROS under so many conditions it is, we suggest, difficult to see how chronic low dose exposure to IR at DCRLs, and perhaps a magnitude above at least, adds significantly to ‘stress’ from oxidizing radicals. This might also prompt more thought about claims of ROS and anti-oxidant capacity being important for the effects on animals of chronic exposure to low doses of IR.

FIGURE 7. Oxidizing radicals from O 3 exposure compared to those from background IR, Chernobyl and UV. Concentrations of tens of ppb O 3 have documented effects on plants and concentrations of >150 ppb can have visible effects. To calculate the total radical production by O 3 in nM/m 2 /s its partial pressures were calculated in Pa for the 0–500 ppb range and, using the ideal gas equation (PV = nRT), the molarity in air was calculated. Using an Oswaldt’s constant ( H ) of 0.25 for O 3 in air/water mixture (effectively an air/water distribution coefficient that is equivalent to Henry’s law constant) and the relationship molarity in air = H × molarity in water, the molarity of O 3 dissolved to water at the appropriate range of partial pressures was calculated. To calculate radicals in nM/m 2 /s we assumed ten thousand liters of air per m 2 (i.e., a relatively shallow depth of air), an effectively infinite supply of O 3 and that every O 3 molecule produced a radical. The dissolution of O 3 to water is affected by numerous factors including temperature, solutes, the presence of anti-oxidants and so on but it is clear that the number of oxidizing radicals produced by IR at Chernobyl are several orders of magnitude less than the concentrations of O 3 deemed to have no oxidative effects on plants. (Details of calculations are given in Supplementary Data Sheet S5 ).

Thus, if there are effects of chronic exposure to low dose IR at the lower end of the DCRL range or below, we suggest that a stress response context indicates that they will be primarily as a result of DNA damage rather than ‘oxidative stress.’ The life strategy of terrestrial plants involves coping with stress using high cellular capacity for DNA repair, especially DSBs, the development of reproductive structures de novo in each generation rather than from a dedicated germline (which helps limit the multi-generation effect of deleterious mutations), and high redundancy of reproductive structures during reproduction. Overall, the effects of IR on plant populations at chronic low doses, if or when they occur, are likely due to DNA damage and can be expected to occur at doses that are higher than in more IR sensitive organisms. Given that plants are adapted to a hierarchy of effects induced by stress ( Willey, 2016 ), and that this adaptation is often based on processes with a high level of redundancy, it is clearly possible that effects detected in cells or individuals do not manifest as biologically significant effects at the population or community level.

Discussion and Conclusion

Particular consideration of the effects of chronic low-dose IR on plants is necessary because of the predominance in the literature of data derived from acute high doses to organisms with a different biology plus a lack of data from plants experiencing chronic low doses under controlled conditions. Field data following nuclear accidents is vital not only for managing contaminated sites but also because it provides insights into the effects of chronic low-dose IR under conditions in which; other abiotic and biotic stressors are present, competition is likely to be occurring, complex ecosystem interactions are present, and in which exposure can include emissions from hot particles ( Sandalls et al., 1993 ). More data on the effects of low dose IR under controlled conditions might help clarify not only its effects but also help to identify the role of interactions with other variables in producing effects of IR observed in the field. However, in general, currently available data collected over several decades suggests that: (a) biological contexts are important when trying to understand effects across a range of doses and at different levels of biological organization; (b) at the sub-cellular level, low dose chronic IR can have detectable effects on plants primarily via minor changes to genetic material; and, (c) that in DCRL dose ranges these effects do not have significant adverse consequences for plant populations and communities. Thus, overall, we conclude that existing evidence in appropriate context suggests that current environmental protection frameworks for flora are generally fit for purpose. The sessile life strategy of plants and the static icon of the DNA double helix can be distracting. The survival of individual plants, and their populations and communities, is based on a life strategy which, although it does not involve much individual mobility, uses dynamic processes at a wide range of biological scales that often have high levels of redundancy.

A situation in which effects might be detectable but a fundamental change in environmental protection frameworks is unnecessary is not necessarily paradoxical and arises from, and is acceptable under, the following circumstances. First, the available data. Much relevant data from field studies is available and, although it was often not designed, for good reason, to test dose limits, only some of the data indicate effects at the low end of DCRLs and often for plants long-known to be sensitive to IR. Further, in data that include effects at these levels the evidence for causality is often associative and meets only some of the Bradford-Hill criteria. Thus, especially when many data sets do not report significant effects at relevant dose rates, there is not a conclusive enough body of evidence to change, for example, DCRLs for plants. Second, the type of effects reported. Where effects have been reported at DCRLs or sometimes below, they are sub-cellular and there is no real body of evidence of effects at higher levels of biological organization. DCRLs, and other frameworks for radiological protection of flora and fauna, aim to protect biodiversity, conserve species and protect the health of communities and ecosystems – which the evidence suggests that they do. Third, the biological context. Sessile life on the land surface is stressful and plants have evolved to cope with high levels of variation in their environment. They do this in part using DNA repair mechanisms and anti-oxidant pathways that have a higher capacity than many other multicellular organisms and that cope routinely with stress more than equivalent in magnitude to that from chronic low dose IR at DCRLs. Just because an environmental variable causes a change in a cell it does not mean that the cell, or the individual it is part of, is stressed or that it will necessarily be adversely affected. During the evolution of plants average dose rates probably peaked at 20 μGy d -1 and it seems sensible to suggest that high levels of DNA repair and anti-oxidant activity in plants prompted by other stressors enable them to generally suffer no adverse consequences of IR, at the population and community level at least, up to the low end of the DCRL range for sensitive plants (4 μGy h -1 ). It is, however, notable that the species for which IR effects data is available constitute a very small proportion of the world’s plant species so there is likely to be room for improving our understanding of which species in particular are protected by the grass and pine tree RAPs. It is possible that there are plant species, perhaps those that have specialized in living in particular conditions, that are especially sensitive or resistant to the effects of IR and that merit their own DCRLs.

Investigating data on the effects of plants at a range of exposures provides some directions for further research. First, it emphasizes the importance of the particular biological context. More data on the effects of IR, especially low-dose chronic IR, on roots, meristems, plant reproductive structures, and plant developmental endpoints over multiple generations seem especially important. Second, it emphasizes the plant stress-response context. Plants are adapted at a hierarchy of biological scales to resist significant environmental stressors, including many that act via mechanisms similar to those through which IR acts, so the existence of effects at a sub-cellular level should not be viewed as necessarily having adverse consequences at higher levels of biological organization. Third, IR is a primordial stressor. At a time in Earth’s history when unprecedented anthropogenic environmental changes are occurring and plant responses to these changes are vital to global food supplies and ecosystem functioning, understanding the effects of IR on plants might also be useful for understanding the evolution of plant stress responses in general. Finally, it emphasizes the societal context of the protection afforded to the environment. If the protection of biodiversity, communities, and ecosystems from the effects of IR is the goal then the evidence suggests that current systems are appropriate. If, however, as is the case with protection of humans from the effects of carcinogens, protection of individuals from rare stochastic effects is important, then it is possible that between the dose rates that all individuals can withstand and the DCRLs that protect populations, there are some individual plants experiencing adverse effects.

Author Contributions

NC conceived the approach, produced some of the figures, and wrote the first drafts. NW wrote the final draft and contributed some of the figures.

The work was carried out as part of the Radioactivity and the Terrestrial Environment (RATE) Program in the United Kingdom funded by the Natural Environment Research Council, the Environment Agency, and Radioactive Waste Management Ltd. (Grant Number NE/L000342/1).

Conflict of Interest Statement

The Environment Agency (England) and Radioactive Waste Management Ltd. have part funded the research and are potential beneficiaries of the results.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2018.00847/full#supplementary-material

DATA SHEET S1 | Estimated ionizing radiation dose rate through geological time at the Earth’s surface.

DATA SHEET S2 | Radical induction-potential from water by different radiation sources through Earth’s history.

DATA SHEET S3 | The activity of radionuclides in the environment from the accident at Chernobyl.

DATA SHEET S4 | The doses and dose rates used in studies of the effects of IR on plants.

DATA SHEET S5 | Oxidizing radicals from O 3 exposure compared to those from background IR, Chernobyl and UV.

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Keywords : ionising radiation, radiobiology, environmental protection, DNA damage, oxidative stress, plant stress

Citation: Caplin N and Willey N (2018) Ionizing Radiation, Higher Plants, and Radioprotection: From Acute High Doses to Chronic Low Doses. Front. Plant Sci. 9:847. doi: 10.3389/fpls.2018.00847

Received: 21 March 2018; Accepted: 31 May 2018; Published: 26 June 2018.

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Copyright © 2018 Caplin and Willey. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Neil Willey, [email protected]

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Electromagnetism and plant development: a new unknown in a known world

• Published: 13 November 2019
• Volume 31 , pages 423–427, ( 2019 )

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• João Paulo Ribeiro-Oliveira   ORCID: orcid.org/0000-0003-1017-4154 1  

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How does the new affect the old but mutable living systems? This is the question that electromagnetism stress has been provoking. There are many evidence that non-ionic radiation can affect animal cells since their plasticity is limited when compared to plants. However, the way plants perceive and process this stressor is still poorly understood. So here are some intriguing facts that lead us to reflect on how and why electromagnetism can become a very common stressor for years to come for plant species.

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Acknowledgements

I am grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES) for a scholarship; to the Programa de Pós-Graduacão em Agronomia (UFU) for the support currently given to me as a Post-doctoral (PNPD); to Professor Marli A. Ranal for criticism and support; to Mr. Roger Hutchings for suggestions and the English review of the manuscript; and to the anonymous reviewer for the important observations on the manuscript.

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Ribeiro-Oliveira, J.P. Electromagnetism and plant development: a new unknown in a known world. Theor. Exp. Plant Physiol. 31 , 423–427 (2019). https://doi.org/10.1007/s40626-019-00163-9

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DOI : https://doi.org/10.1007/s40626-019-00163-9

Exploring the impact of space radiation on plants

Texas a&m-led, nasa-funded study investigates plant survival on long space missions.

December 20, 2022 - by Adam Russell

The future of space exploration depends on plants.

Rockets and other exploratory technology can take astronauts to the moon and beyond, but plants will sustain their trips over longer periods. As NASA explores the potential for longer space flights, continued stays on the International Space Station or even the future colonization of the moon or planets like Mars, their scientists know that plants are needed for survival.

From food and water purification to carbon dioxide removal and oxygen production, plants are the foundation of humanity’s life on Earth and beyond.

However, exposure to extreme environmental factors related to space travel, including microgravity and space radiation, impacts biological systems like plants.

Researchers in the Department of Biochemistry and Biophysics at the Texas A&M College of Agriculture and Life Sciences are striving to understand the largely unknown effects of these extreme conditions in space.

The impact of radiation on plant telomeres

Dorothy Shippen, Ph.D., University Distinguished Professor and Regents Professor in the Department of Biochemistry and Biophysics, is leading a study to determine how radiation exposure in space impacts plant telomeres, which are basic building blocks in the DNA at the very ends of chromosomes. Much like plastic tips on shoelaces prevent the lace from fraying, telomeres help keep chromosomes stable and healthy.

Telomeres are not static, Shippen said. They contract and expand due to environmental stressors, and if they get outside the normal size range, they lose their protective function. There is evidence in plants and humans that chromosomes become unstable when telomeres get too short, and various cancers in humans are associated with telomeres lengthening. 

NASA is interested in learning how and why some of the extreme stressors in space, particularly space radiation like gamma and cosmic rays, impact plants. This is where the Shippen Lab at Texas A&M saw an opportunity to contribute.

“Plants are obviously very important for space travel, and so from a practical point of view we want to understand how we can help them survive the extreme conditions of space,” Shippen said. “There is so much we don’t know, but this telomere research will answer some of the basic questions we have related to plants and space radiation.”

The team and the study

Shippen is known internationally for her pioneering work in establishing the plant Arabidopsis thaliana as a model for telomere biology. She will act as principal investigator and team with collaborators Sarah Wyatt, Ph.D., at Ohio University and Susan Bailey, Ph.D., at Colorado State University .

Wyatt is an international leader in plant molecular biology who has been involved in several spaceflight experiments with Arabidopsis. Bailey is a renowned radiation biologist who first reported changes in telomere length dynamics associated with a long-duration mission by astronaut Scott Kelly during the NASA Twins Study .

Borja Barbero Barcenilla, a postdoctoral fellow in the Shippen Lab, will conduct experiments and collect data for the study.

The team’s specific goals are to assess the impact of space radiation on oxidation status, telomere length dynamics and genome stability in plants.

“There is interest in telomeres because they are linked to survivability, and it turns out the environment can influence the size of telomeric DNA tract,” Shippen said. “The telomeres are like a reporter for the physiological health of organisms and a biomarker for their ability to be healthy. We are interested in understanding how plants respond to the stress of space radiation and then figure out how to protect them.”

Space radiation’s impact on plants

The research team hypothesizes that exposure to space radiation triggers genome oxidation and an increase in the activity of telomerase, a specialized enzyme responsible for maintaining telomeric DNA. The preliminary data suggests a strong connection between them.

The preliminary data of Shippen and Wyatt was gathered from Arabidopsis seedlings sent into low Earth orbit on a previous space flight. The team showed that the telomere lengths of the plants did not change, but that telomerase activity increased significantly – at least 150-fold. This unexpected finding suggests the telomerase enzyme may play some protective role during space travel.

The NASA-funded research will allow Shippen’s team to send their own plants into space in the future and perform radiation experiments in laboratories that will mimic the environment plants might be exposed to in space.

Land plants may, in fact, be very well equipped to go to space because they are remarkably tolerant to a broad range of environmental stresses on Earth like drought, disease and pests, she said. The researchers are interested to see how space radiation impacts plants directly from seed to flower. In addition, the team will collect seeds and test the progeny to see how radiation affects plants across generations. Chronic exposure to space radiation is expected to pepper the plant genome with mutations.

Our need to learn more

Scientists have learned many things about how plants react to microgravity environments through experiments designed by the Wyatt lab for flights to the International Space Station.

But little is known about how plants react to space radiation, Barcenilla said. He expects Arabidopsis plants involved in the project will be aboard a flight to the International Space Station sometime in 2024.

“This is all very new, and we need to understand how this exposure to radiation plays out,” Barcenilla said. “Right now, the level of radiation these samples were exposed to in our preliminary experiments in low Earth orbit aboard the International Space Station are much less than what they will suffer on the moon or Mars. The radiation exposure will exponentially increase on those missions, so we need to understand how plants will react to the much higher levels of radiation.”

An important first step

Barcenilla said the study is an important step forward for space travel but could also help scientists better understand how plants react and adapt to stressors here on Earth.

Intentionally exposing plants to radiation has led to beneficial mutations for plant breeding purposes, with the goal of generating plant varieties better suited to contend with a variety of stressors, he said.

“In the end, we are trying to develop better, smarter ways to help plants withstand stressors,” he said. “It just happens that we are studying stressors that are very, very harsh on plant DNA. So, the mutations that benefit us in space can also benefit us here on Earth.”

Shippen said it is exciting the project has classical agriculture and engineering components focused on revealing basic science for an innovative field like interstellar travel. But the research may also advance scientific understanding about how space travel can impact other biological systems, including humans, and offer insights into adaptations. 

“I think we are in a really good position to deliver some interesting data,” she said. “We have the right collaborators, and we feel privileged that NASA sees the value in these experiments and trusts us with them.”

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Effect of Long Duration Space Exposure on Seeds

Launch information.

X-37B Orbital Test Vehicle-6 (OTV-6) launched on May 17, 2020.

Science Objectives for Everyone

• This collaborative activity consists of two experiments, namely RAD-SEED 1 and RAD-SEED 2, utilizing the X-37B, an experimental reusable space vehicle operated by the United States Space Force.
• The primary goal is to investigate the effects of long duration exposure to microgravity and space radiation on seed viability and quality. This knowledge gap is relevant to future interplanetary missions and for the establishment of permanently inhabited planetary surface bases.
• Seeds from two plant model organisms and eleven crop plants species or cultivars were selected. Seeds recovered from this long duration mission will be evaluated for viability, germination rates, developmental abnormalities, and molecular changes compared to ground control seeds.

Experiment Description

Research overview.

• With the renewed goal of manned Mars exploration, continuous fresh food production during long duration deep space missions can be a critical addition to the processed food system to meet astronauts’ nutritional requirements and to provide potential psychological benefits for crew in the isolation and confinement of deep space.
• However, critical knowledge gaps, such as the impact of deep space radiation on long-term seed storage and plant growth, must be addressed prior to dependence on crop systems for any portion of a deep space food system. These knowledge gaps are also relevant to the establishment of permanently inhabited planetary surface bases.
• The X-37 vehicle is uniquely suited to return experiments to Earth after each flight. Therefore, we utilized this unique flight opportunity to investigate the impact of long-duration space exposure on plant seeds to test whether nutritious and high-quality produce can be reliably grown from seeds stored long-term in the space environment, and if not, to provide a baseline to guide future radiation countermeasure development for crop produce.
• The response of each crop species to long term space environment exposure will also help identify candidate traits for successful plant growth on deep space vehicles.
• The hypothesis is that long duration space exposure will affect seeds viability and quality, causing detrimental effects on germination and plant development compared to ground control seeds.
• There are three Objectives: (1) Evaluate the effect of long-duration exposure to the space environment on seed viability and quality. (2) Explore the mechanisms on how seeds respond differently to long-term space environment exposure. (3) Validate the OTV passive sample exposure platform for potential future missions to expose biological samples to long-duration space environment.

Description

• The experimental approach outlined here is designed for maximum science gain for this long-duration mission.
• Model Organisms: 2 model plant organisms and 11 space crop candidates were selected for this project. Most of these species have been grown successfully under spaceflight-like conditions (temperature, air, humidity, lighting, etc.) in ground analogs at KSC, and either have been or will be grown on ISS (in some cases for crew consumption). These seeds include: (1) The model plant organisms Arabidopsis thaliana and Brachypodium sp. , both of which have been grown on the ISS; (2) Crop species that have been or will be grown on the ISS (Mizuna, Lettuce, Tomato, Pak Choi, Radish, Hatch chile pepper, and Dwarf Wheat); (3) Crop species that have unique seed shapes and characteristics, including Chard, Onion, rice, and Cucumber.
• Design of Comparable Radiation Scenarios using the NASA Space Radiation Laboratory (NSRL) at Brookhaven National Lab: In addition to the flight experiment, this project also includes multiple ground-based control experiments to allow data comparison. Some ground control samples will be exposed to modified GCRsim in NSRL to simulate the radiation environment of the flight condition based on the radiation dose/dose rate measurements.
• For post-flight analysis, we will use growing conditions (22°C, 40-45% RH, 3000 ppm CO 2 , 300 μmol·m 2 ·s -1 light, and 16hr/8hr photoperiod) comparable to those used during ISS Veggie plant growth experiments, within a controlled environment chamber at KSC. Seeds from each model plant, and crop species will be planted and collected at 6-10 days (durations are species dependent) for assessment of germination rates and morphological and histological analyses. Images will be acquired for evaluating signs of stress, developmental abnormalities and measuring root length. At different time-points, seedlings will be fixed in RNAlater for potential transcriptomic and mutation analysis to explore the mechanisms behind different responses cross species/variant. To analyze edible biomass, seeds from selected crop species will be planted under the same environmental conditions described above. The crops will be harvested at day 28-90 after planting (species dependent) at which time morphological assessments will be conducted (e.g. appearance, size, weight). Subsequently, the fresh produce will be harvested for potential analysis for a panel of nutrition-relevant minerals and vitamins.
• The results obtained from this flight experiment will be compared with those from KSC ground controls, and seeds exposed to simulated space radiation scenarios using NSRL. We will also compare the data with those obtained from our MISSE project, an HRP funded Seed Radiation project using NSRL, and other literatures. These comparisons will provide valuable and integrated baseline database for establishing crop production and seed storage capabilities for long-term deep space explorations.

Space Applications

• Data collected from this study will address several knowledge gaps for establishing deep space crop production capabilities, particularly space radiation impact/protection and seed storage conditions for a diverse variety of candidate “space crops”.

Earth Applications

• The response of each crop species/variant to long term space environment exposure and its mechanism will also help identify candidate traits for successful plant growth not only for deep space explorations, but also for improving agriculture on Earth, especially for regions with harsh or extreme environment.
• PI: Ye Zhang, Ph.D., NASA Kennedy Space Center
• Howard G. Levine, Ph.D. NASA Kennedy Space Center
• Jeffrey T. Richards, LASSO Contract (Amentum), NASA Kennedy Space Center

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• Published: 21 August 2023

Perspectives for plant biology in space and analogue environments

• Veronica De Micco   ORCID: orcid.org/0000-0002-4282-9525 1 ,
• Giovanna Aronne 1 ,
• Nicol Caplin 2 ,
• Eugénie Carnero-Diaz 3 ,
• Raúl Herranz   ORCID: orcid.org/0000-0002-0246-9449 4 ,
• Nele Horemans 5 ,
• Valérie Legué   ORCID: orcid.org/0000-0003-2090-9580 6 ,
• F. Javier Medina   ORCID: orcid.org/0000-0002-0866-7710 4 ,
• Veronica Pereda-Loth 7 ,
• Mona Schiefloe 8 ,
• Sara De Francesco   ORCID: orcid.org/0000-0001-8280-4237 1 ,
• Luigi Gennaro Izzo   ORCID: orcid.org/0000-0001-5722-2497 1 ,
• Isabel Le Disquet 3 &
• Ann- Iren Kittang Jost 8  

npj Microgravity volume  9 , Article number:  67 ( 2023 ) Cite this article

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Advancements in plant space biology are required for the realization of human space exploration missions, where the re-supply of resources from Earth is not feasible. Until a few decades ago, space life science was focused on the impact of the space environment on the human body. More recently, the interest in plant space biology has increased because plants are key organisms in Bioregenerative Life Support Systems (BLSS) for the regeneration of resources and fresh food production. Moreover, plants play an important role in psychological support for astronauts. The definition of cultivation requirements for the design, realization, and successful operation of BLSS must consider the effects of space factors on plants. Altered gravitational fields and radiation exposure are the main space factors inducing changes in gene expression, cell proliferation and differentiation, signalling and physiological processes with possible consequences on tissue organization and organogenesis, thus on the whole plant functioning. Interestingly, the changes at the cellular and molecular levels do not always result in organismic or developmental changes. This apparent paradox is a current research challenge. In this paper, the main findings of gravity- and radiation-related research on higher plants are summarized, highlighting the knowledge gaps that are still necessary to fill. Existing experimental facilities to simulate the effect of space factors, as well as requirements for future facilities for possible experiments to achieve fundamental biology goals are considered. Finally, the need for making synergies among disciplines and for establishing global standard operating procedures for analyses and data collection in space experiments is highlighted.

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Introduction.

At the beginning of space exploration, research in space life science was focused on the human body to gain a fundamental understanding on the responses to the stressful space environment, to ultimately prevent health risks and protect astronauts by managing space-induced pathological issues 1 , 2 . In the last decades, increasing interest has been raised towards plant space biology due to the awareness that cultivation of higher plants in space is a requirement for long-duration human missions, where the regeneration of resources and plant-based food production onboard must be increased at the expense of re-supply from Earth 3 .

Plants play a crucial role in Bioregenerative Life Support Systems (BLSS). Artificial ecosystems such as the BLSS are high-technology systems, based on the integration of physico-chemical and biological processes, to support long interplanetary missions 4 , 5 . The BLSS concept includes several interconnected compartments in which different organisms are used to sequentially recycle resources 6 , 7 . Within a BLSS, the photoautotrophic compartment enables the production of edible biomass, oxygen, and water as resources for the astronaut, starting from carbon dioxide, wastewater and other wastes. An example of BLSS is the MELiSSA (Micro-Ecological Life Support System Alternative) loop by the European Space Agency (ESA) that aims to sustain astronaut life in space missions to reduce the initial payload and dependency from Earth 8 . The MELiSSA loop is made of interconnected compartments among which the requirements of the higher plant compartment need to be fulfilled at least in part by the outputs of other compartments 9 . As well, the species/cultivar choice and environmental control are dictated by the need to meet the requirements of the other compartments (e.g., oxygen requirements of the animal crew) in addition to the generally accepted requirements including short cultivation cycles, reduced plant size, high harvest index, and resistance to diseases. Increasing effort is posed on plants to produce healthy food specifically designed to sustain crew in long term missions 3 , 10 , 11 .

Additionally, research in space-plant biology and space-agriculture is required alongside the strong efforts to increase the knowledge on human biology in space with the aim to predict risk factors, prevent disease(s), and implement effective countermeasures to manage health emergencies during missions. Among countermeasures for assuring astronauts' well-being against degenerative diseases and psychological issues, there is the introduction, in their nutrition, of plant-derived fresh food produced directly on board or within a habitat. Further, there may also be benefits for crew mental health by allowing crews to participate in plant cultivation in the living and/or working pressurized modules in space 12 , 13 .

What are the main constraints to plant cultivation in space?

From an applied point-of-view, the design and realization of BLSS require a better understanding of plant acclimation and adaptation processes that determine the plant’s capability to complete a full life cycle in space (producing viable offspring) for both model plants and crops. As a matter of fact, the altered growth and behaviour of plants in space can alter the input/output balance between the different compartments as well as the potential nutritional value of the derived fresh-food. Indeed, as any other living organism, plants’ survival and reproduction strongly depend on interactions with environmental factors (e.g. temperature, light, oxygen/carbon dioxide, water, and volume availability) including the novel space factors (e.g., altered gravity and ionizing radiation). Among different environmental factors, altered gravity and ionizing radiation are recognized to be the main constraints for growth in space conditions. In the following section, we briefly summarize the current knowledge about the effects of microgravity and radiation on plants.

What is already known about the effects of microgravity and radiation

To date, European scientists studying plant space biology have focused on understanding the effects of altered gravity on several plant systems (e.g. different species/cultivars, target organs/tissues). Recently, more attention has been dedicated to the effect of ionizing radiation (IR) so far as it represents a clear challenge for exploratory-class missions 14 . Altered gravity and exposure to IR can induce changes in gene expression, cell proliferation and differentiation, signalling and physiological processes (see precise data and references in the following paragraphs). The expected consequence of these changes would be serious structural and functional alterations at the whole organism level. In addition, since these cellular and molecular changes are detected in early developmental stages, developmental alterations would also be expected. However, altered tissue organization, organogenesis and functioning have not always been detected under spaceflight conditions. For example, none of these effects has been reported to occur when plants have been cultured in space: adult organisms were produced with no evident aberrations and the entire seed-to-seed life cycle of plants was successfully achieved under spaceflight conditions 15 , 16 . Interestingly, this phenomenon is not exclusive to plants. It was first detected and reported by Marco et al. 17 in the fruitfly Drosophila melanogaster and defined as “an apparent paradox”. Up to now, this paradox has not been resolved and remains an important challenge for space biology research.

Effect of microgravity and altered gravity on plant growth and reproduction

Since 475 million years ago, land plants have evolved under the same 1  g gravity level. Early pioneering space experiments have demonstrated that plants are able to survive and grow in space, although morpho-physiological alterations were soon reported in crop species as lettuce and lentil 18 , 19 . In early research, deficiencies in the experimental setup and in used facilities were sometimes responsible for confusing and contradictory results. For example, nutrient absorption has been reported to increase, decrease or remain unchanged under reduced gravity, likely due to hardware limitations and species-specific responses 20 . Now, however, there is evidence that microgravity in space environment does not prevent plant growth and reproduction but causes serious alterations in plant physiology and development 21 . Plants respond to changes in mechanical inputs, therefore gravity-related research offers a unique opportunity to elucidate the mechanisms of gravity perception whose knowledge is necessary to better understand fundamental processes and the physiological changes in space. Moreover, in exploratory-class long-term missions, plants will face not only a lack of gravity (or residual gravity) during spaceflight (and inside the International Space Station - ISS) but also the lunar gravity (0.17  g ) and the Martian gravity (0.37  g ) which are substantially lower to what plants normally experience on Earth. Indeed, in forecasting possible acclimation of plants in environments with altered gravity, thresholds for gravity sensing should be considered. Previous studies indicated that the threshold acceleration perceived by lentil roots in spaceflight can be in the order of 10 –3   g or lower 22 , but the effects of altered gravity on cell cycle have been detected at higher levels, intermediate between Moon and Mars gravity, in simulation experiments on Earth 23 . Similarly, the range for the attenuation of phototropism in higher plants occurs in the same range 0.1–0.3  g 24 .

Plant developmental patterns and gravity perception: from gene expression to cell cycle and organ development

Most studies to reveal the effect of altered gravity on plant development have been focused on the root meristem 25 . Experiments under microgravity simulation and onboard the ISS revealed the disruption of the meristematic competence in seedlings, i.e. the loss of the coordinated progress of cell proliferation and cell growth that characterizes meristematic cells under gravity conditions on Earth 26 , 27 , 28 .

An acceleration in the cell cycle was detected in in-vitro cultured Arabidopsis MM2d cells grown in simulated microgravity conditions produced in a Random Positioning Machine (RPM), resulting from downregulation of genes involved in the G2/M transition checkpoint and upregulation of genes controlling the G1/S transition. Other phenomena were the downregulation of significant genes for ribosome biogenesis and the corresponding depletion of the levels of nucleolar proteins, the depletion of the nuclear transcription and an increase in chromatin condensation, related to the epigenetic regulation of gene expression 29 , 30 . Experiments using different levels of reduced gravity and hypergravity indicated modulation of alterations for each level, with Mars gravity inducing milder alterations 23 , 31 . Indeed, studies on gravitropism and phototropism have shown that the reduced gravity level on Mars of 0.38  g should not be a major problem for plant growth 24 .

Auxin is a key factor regulating the connection between perceived stimuli and cellular responses, controlling the balance between cell proliferation and cell differentiation, regulating the cell cycle progression and the coordination between cell growth and cell division 32 , 33 , 34 , 35 . The role of the LAZY proteins in gravity sensing has been recently described, being crucial players linking gravity perception and gravitropic curvature through the proper redistribution of auxin, the relocation of the auxin efflux carrier PIN-FORMED (PIN) proteins for the tropic response of both roots and shoots 36 . However, the role of auxin and its polar transport in plant growth and development under microgravity conditions is not fully understood and requires further investigation to solve controversial concerns due in part to its complex interaction with cytokinin. For example, it has been shown in Arabidopsis that real microgravity does not influence the distribution of auxin in the primary root, whereas it affects that of cytokinin 37 . In contrast, the inhibition of pea hypocotyl growth in microgravity is correlated with an attenuation of polarized auxin transport, a decrease in auxin levels and an increase in cytokinin levels 38 .

Parallel transcriptomic experiments exploring how simulated (i.e. clinorotation, RPM and diamagnetic levitation) and real microgravity change gene and protein expression have shown a complex response of plants at early developmental stages (mostly Arabidopsis seedlings), involving reprogramming of the gene expression pattern 39 . Specific genes of response to gravity alteration have not been found, while the main and most frequent targets of this gene reprogramming are: genes coding for heat shock-related elements, cell wall remodelling factors, oxidative burst intermediates and components of the general mechanisms of plant defence against stressors, being differently affected at the different spaceflight, lunar and martian g levels 40 . The results of several experiments in space using a centrifuge to produce different gravity levels showed a differential response to each level, triggering different adaptive responses, involving changes in the regulation of different sets of genes. Changes in gene expression were lower under Mars gravity compared to microgravity on the ISS 40 , 41 .

Interaction with other factors

Many plant responses are primed by the interaction between gravity and other physical, chemical, or biological factors. In the last decades, orbital platforms enabled comprehensive studies on the mechanisms underlying plant growth in microgravity 42 . Still, there is a need to further investigate the interactions between gravity and other environmental factors including temperature, light, oxygen/carbon dioxide, water availability, electric and magnetic fields, especially in the framework of plant morphogenesis and tropic responses, also considering intra-specific genotypic variability 43 , 44 . With the exception of a limited number of studies concerning microgravity interactions with magnetic fields, water or chemical stimuli on crops (i.e. flax, cucumber and carrot) 45 , 46 , 47 , previous research has mainly focused on the interactions between gravity and light. It has been shown that the sensitivity of plants to light is influenced by microgravity and that phototropic curvature of the shoot and root organs are largely affected by changes in gravity conditions 48 Experiments performed using the EMCS onboard the ISS or the ESA ground-based facilities resulted in discovering novel phototropic responses of plants, both the model Arabidopsis and Brassica oleracea , proving that the interaction between gravity and light changes according to the magnitude of g-force 49 , 50 , 51 . In this framework, light quality has a prominent role in determining the direction and strength of phototropic responses of shoots and roots, with major differences between blue and red wavelengths under a wide range of gravity levels 51 , 52 . On the other hand, previous studies also showed that light can control the sensitivity of plants to gravity through phytochrome-regulated pathways, indicating that phytochromes play a key role in integrating multiple environmental stimuli 53 .

Gene expression studies with different levels of altered gravity showed that the adaptive response appeared enhanced by red light photostimulation. Red light activates cell proliferation and ribosome biogenesis in pea 54 , and in the “Seedling Growth” series of experiments in the ISS, red light caused a concerted upregulation of marker genes for cell proliferation, cell growth and auxin polar transport 55 . Experiments with different levels of gravity (microgravity, Mars gravity and ground control gravity) with and without red light photoactivation have shown that red light restored the auxin distribution patterns which appeared altered under microgravity, while in roots grown at 0.3  g , the auxin polar transport was slightly altered, irrespective of photoactivation 56 . The red light was also shown to counteract the decoupling between cell proliferation and growth in root meristems reported in earlier experiments 41 .

Gene expression alterations, evaluated by RNA-seq, showed different responses to different gravity levels and modulation of gene expression by red light photoactivation. As an example, Mars gravity level induced an adaptive response, consisting of the activation of environmental acclimation-related transcription factors (WRKY and NACs families), especially in photostimulated samples 41 .

It appears clear that plant cultivation in future space missions implies research-based strategies that involve gravity-substituting factors (e.g., light) to counteract the effects of microgravity or partial gravity conditions such as on the Moon and Mars. Nowadays, the technological advancement in cultivation systems is providing effective and affordable tools to control environmental factors for plant growth in space with the possibility of using external cues for both application and research purposes 42 . Gravity might be replaced by specific stimulation in terms of light wavelengths and photon flux density for the regulation of plant growth and development. Prospectively, other factors are expected to play such a role including water, electric and magnetic fields, chemicals, or microorganism, but further investigation is needed.

Seed-to-seed cycle

Nowadays, it is crucial to delve into the mechanisms by which altered gravity conditions can affect plant reproduction and seed viability, in order to develop cultivation strategies for the improvement of plant-based BLSS in future human settlements on the Moon and Mars 57 . The completion of the seed-to-seed cycle, in fact, will be essential to produce viable seeds to be used for the cultivation of plants over time without relying on terrestrial supply.

Early studies with plants grown for extended periods in microgravity reported an overall reduction of plant growth and difficulties in the transition to the reproductive stage 58 . Since the first seed production in space by Arabidopsis thaliana plants in 1982, a few experiments on plant reproduction have been performed 59 . Overall, previous studies showed that the seed-to-seed cycle can be accomplished in most species tested in microgravity, although with reduced quality of embryos and seeds produced by plants due to delayed embryo development, modification in storage reserves, delayed starch use in cotyledons, and decreased cell number in cotyledons 15 , 58 , 60 , 61 , 62 . Furthermore, experiments using simulated microgravity (e.g., clinorotation) showed significant alterations during the development of male gametes in several crop species 63 .

Given that most studies have investigated the effect of microgravity on early stages of plant development with sporadic studies on plant reproduction, there is a large gap of information to be filled to fully the effects on the growth of plants in the adult stage and on plant reproduction.

Effects of ionizing radiation on plant growth and development

Outside Low Earth Orbit, IR is variable in space and time and can severely constrain organisms’ growth 3 , 14 . IR can cause direct damage to the structures encountered, but also indirect due to the generation of reactive oxygen species (ROS) 64 , 65 . The oxidative stress due to ROS production may damage important components of plant cells, including lipids and proteins, but especially DNA 66 , 67 . The degree of direct DNA damage and proper functioning of DNA repair systems determine the consequences of IR exposure for plants at morpho-structural and physiological level 68 .

Nevertheless, plants’ responses to IR are not fully understood yet. Experiments in space where plants, either the model Arabidopsis or crops such as beans and tomato, were exposed to cosmic radiation and on the ground with exposure to low- and high- linear energy transfer (LET) radiation have shown that IR can have positive, null or negative effects on plants, at genetic and morphophysiological levels depending on IR properties and plant intrinsic factors such as type of radiation, its LET, exposure time (acute or chronic), dose, plant species/cultivar, developmental stage at the time of irradiation 69 . The effect of IR is also tissue-specific and depends on tissue architecture: complex tissues in beans and tomatoes seem less sensitive to damage 70 , 71 , and, on the contrary, the meristematic cells are the most sensitive to radiation 72 .

High-LET radiation, like protons and heavy ions, is more harmful in inducing genetic mutations compared to low-LET radiation such as X- and γ-rays 73 , 74 . Concerning the dose of exposure, high doses (>100 Gy for seeds; >50–70 Gy for vegetative stages) can lead to harmful outcomes, such as reduced levels of photosynthesis and germination, embryo lethality, loss of apical dominance, dwarf architecture, altered leaf anatomy, and accelerated senescence 67 , 69 , 75 . Low doses of IR, on the other hand, appear to induce hormetic response in plants, stimulating germination, growth, photosynthetic and respiration rate, improving the content in chlorophyll, carotenoids, non-enzymatic (ascorbic acid, glutathione, and anthocyanin) and enzymatic antioxidants (ascorbate peroxidase, catalase, and superoxide dismutase) and phenolic compounds, effective in counteracting the oxidant action of ROS, thus increasing plant nutritional value and radioresistance 75 , 76 , 77 , 78 , 79 , 80 .

Most of the studies performed on plants have been conducted by irradiating dry seeds with acute doses (due to limitations in the volume and time of irradiation availability) 75 , 81 . Moreover, most of the studies involving crop species have mainly been focused on using IR to introduce genetic variation and selecting plant cultivars with specific traits 82 . Only a few studies have considered the effects on the yield, nutritional value as well as interaction with other factors. A recent study has indicated that the effect of X-rays delivered to germinated seeds at different doses is strongly influenced by light quality during subsequent cultivation 83 .

As a result, little information is available on the variation of radiosensitivity during the different phenological phases in the case of acute exposure and on the effects of chronic exposure. Indeed, it is important to emphasize that resistance to large doses of radiation delivered in an acute way (in shorter times than those necessary for the repair of cellular damage) often does not translate into resistance to chronic exposures for multiple generations and vice versa 84 . Therefore, in the sight of future space exploration, the time is ripe for increasing the efforts to investigate plant responses to chronic low dose-rate and high LET radiation to clarify all the processes and mechanisms behind the radioresistance phenomenon 14 .

Knowledge gaps in microgravity and radiation research in plant biology

According to the current scientific knowledge on plants’ responses to space factors, in order to successfully achieve the in-progress target of crewed missions in space, it is necessary to fill knowledge gaps in plant biology. They can be synthesized in the following five points (Fig. 1 ).

Understanding such processes is fundamental to evaluate the impact on the functioning of BLSS and on the value of plant-derived food for the integration of astronauts’ nutrition.

1 - Understanding the fundamental ways that plants sense and respond to gravity alone or in combination with radiation and other space and environmental/cultivation factors. This point is mainly related to short-term effects and acclimation strategies and includes studies on tropisms and morphogenesis.

2 - Studying the long-term effects of altered gravity, radiation and/or other space environment factors on plants and understanding how plants adapt to this new kind of environment.

3 - Studying primary and secondary effects of altered gravity, radiation and/or other space factors on plant growth and reproduction.

4 - Investigating the interaction between microorganisms and plants (beneficial and pathogenic) under space conditions in light of the realization of cultivation modules in BLSS.

5 - Investigating the effects of space factors on yield and nutritional value and quality (e.g. production of nutraceutical compounds) of edible organs targeting the use of plant-derived fresh food as countermeasures to improve astronauts’ health.

Points 3–5 can be investigated in the short-period, thus being mainly targeted to unravelling the acclimation strategies of plants to space factors. The same points can be investigated in the long-term and over multiple generations to evaluate the heritability of varied traits, hence leading to adaptation. In the latter case, constraints to reproduction become crucial to be analyzed.

Overall, the main objective of research activities in plant space biology is to reveal potential acclimation and adaptation mechanisms and processes in the response of plants (crops and model species) to microgravity, partial gravity and variable space radiation in combination with other environmental/cultivation conditions (e.g. airflow, light), through the developmental phases of a whole life cycle. This will allow the resolution of the “apparent paradox” between molecular and cellular effects versus organismic and developmental effects by understanding the mechanisms by which plants overcome the impacts occurring at early plant life stages after exposure to spaceflight conditions.

To understand if exposure to adverse space conditions potentially leads to acclimation and adaptation, the long-term responses of plants have to be investigated through sequential studies of plants after different times of exposure to single or multiple space factors, at different phases of the plant development. The acclimation has to be studied during the life cycle of the plant and adaptation has to be studied after several generations of plants exposed to a space environment.

Knowledge of plant-microorganism interactions is also important. Plants naturally attract microorganisms, some detrimental to plant health while others establish symbiotic relationships. Plants also have endophytes (bacteria and fungi) living between plant cells, some of which are transmitted to the following generations. Understanding the effect of the space environment on the relations between microorganisms and plants can help assess risks to future crew food supply or discover opportunities for microorganisms-mediated enhanced crop yield.

Unravelling the plant acclimation and adaptation processes, responsible for producing essentially viable adult individuals, is important not only for our fundamental understanding within plant biology but also for the realization of BLSS.

Indeed, addressing the five points mentioned above would allow to evaluate:

How the growth processes and regeneration capacity of plants are affected by space factors and thus impact the cultivation requirements in producers’ modules of BLSS.

If reproductive success is achieved and whether multiple generations of plants are possible to obtain, in order to guarantee the possibility to produce seeds for successive cultivation cycles.

If and how the yield and nutritional value and quality of edible organs are affected and thus impact the astronauts’ nutrition.

The two first points regard every plant species, not only crops but also model species such as Arabidopsis , while the second and third mainly refer to crop species.

Facilities in space and on Earth to study the effects of microgravity and radiation on plants

The ISS is an important research platform to study not only the effects of reduced gravity but also the long-term consequences of low dose space radiation on plants. The daily dose received in the ISS has been estimated at 0.5 mSv, assessed by physical dosimetry using phantoms 85 , which is about 100 times higher than the dose on Earth, and about 2.6 and 1.28 times lower than the dose on the Moon and Mars surface 86 , 87 . By combining studies on ISS of plants exposed to various space factors (gravity/space radiation) and environmental cultivation conditions (e.g. different airflow or light conditions), additional required knowledge for future space agriculture can be obtained. Long-term experiments and full cycle studies of plants require a minimum cultivation area. Although the growth area has become larger in the newer ISS facilities (compared to systems such as Kubik and Icecubes), they are still considered too small for crops and full life cycles. When a 1  g or simulated Moon/Mars gravity exposure is required, the growth area is limited due to the diameter of the centrifuge rotor that has to fit into standard-sized racks on the ISS. An extensive review was done on the space plant growth systems where more than 20 systems are described 42 . The ESA BIOLAB facility on ISS has 4 Advanced Experiment Containers (AEC) on two rotors with a limited growth area per AEC ( http://wsn.spaceflight.esa.int/docs/Factsheets/8%20Biolab%20LR.pdf ) (Fig. 2 ) (Table 1 ). The BIOLAB allows unique experimental equipment to be built inside the AEC, and the available growth area for the plant will depend on the instrumentation required in the AEC to perform the experiment but still remains limited. The NASA systems such as Vegetable Production System (VEGGIE, 2014) and Advanced Plant Habitat (APH, 2017) have increased crop growth area, but they are still relatively small 88 , 89 , 90 . The APH is a closed, controlled growth system with full environmental monitoring and control. The VEGGIE system is simpler, with less control, and designed for more crew interaction (Table 1 ). For plant experiments where smaller volumes are required, the NASA Advanced Biological Research System (ABRS) is available with two experimental research chambers (growth area 0.053 m 2 ). The chamber has light and environment control, and one of the two chambers is outfitted with Green Fluorescent Protein Imaging System. The JAXA Plant Experiment Unit (PEU), available on the Kibo laboratory on ISS, is equipped with a LED lighting system with red and blue LEDs, a growth chamber (growth area 0.027 m 2 ), an automated watering system and a CCD camera.

It appears evident the presence of the centrifuge but the strict limitations of volume available for the experimental containers. Credits: ©ESA/NASA.

What is further required?

Larger growth areas, where both model plants and crop plants can be cultivated for long-term experiments (during the whole life cycle), are needed to fully understand the plant acclimation and adaptation to the space conditions. Such a facility requires the control of environmental factors (including temperature, light, gasses, relative humidity, airflow, nutrient solution, and watering), and continuous imaging of the plant growth (e.g., visible light images, IR images using thermal cameras, fluorescence images). Environmental and imaging data should as a minimum be partially and periodically downloaded for feedback from the science teams collaborating from the ground. To collect data for the molecular, cell and anatomical studies, plant samples need to be harvested after sequential exposures to reduced gravity, preserved on ISS either by freezing or chemical fixation and brought back to the ground for analyses. In addition, the possibility to make microscopy analyses onboard has become a reality with the ESA/DLR Fluorescence Microscopy Analysis System (FLUMIAS), a high-resolution fluorescence microscope for live-cell imaging that is available on the ISS 91 .

A specific point affecting the technical needs of space facilities for plant culture is the possibility of performing comparative studies in spaceflight at different levels of gravity, including the Moon and Mars gravity, as well as the inflight 1  g control. The latter is of the highest importance and makes mandatory the implementation of centrifuges in the facilities used for plant cultivation in the ISS. The advanced sophisticated facilities for plant cultivation now available on ISS, such as VEGGIE, APH and the Exposed Roots On-Orbit Test System (X-ROOTS), which have proven successful in the cultivation of a wide range of plant species, are not equipped with centrifuges. ESA in 2018 decommissioned the European Modular Cultivation System (EMCS), a highly useful facility in which different successful experiments were carried out, some of them including pioneering comparative analyses at different levels of gravity in addition to the necessary in flight 1  g controls. Later on, in 2020, ESA promoted a discussion group to adapt the ESA Biolab facility to harbour experiments using crop species and encompassing the full plant life cycle while being exposed to different gravity levels. Whatever the final decision adopted, the need for an effective plant cultivation facility in space with the capabilities mentioned above, as a key to gaining knowledge to support human life in space exploration, is becoming more and more urgent within the next years.

Applications and benefits for Earth

Understanding how plants are able to grow and adapt to space conditions will ensure reliable and predictable food supplies for human space exploration and has strong synergies with the United Nations Sustainable Development Goals, global food security and circular economy.

The sophisticated agro-technologies developed for space applications (e.g., innovative lighting, watering and nutrient delivery systems, fine environmental monitoring with automated control, imaging systems to analyze plant health, etc.) bring innovations to agriculture on Earth to improve sustainable plant cultivation and food production. For example, developing volume-saving, highly efficient plant growth controlled environments is beneficial for food and drug production particularly in densely populated urban areas in line with vertical farming technologies, in underground facilities with no natural light source, and in general in extreme environments such as deserts and poles.

Developing smart and safe pest control methods is applicable in confined volumes where aerosols are undesirable and natural predation for the reduction/removal of pests is not possible.

Besides these more human operational and exploration-oriented goals, it should also be stressed that the unique near weightlessness environment, as well as the high levels of ionizing radiation, also provide a research laboratory that cannot be obtained in on-ground laboratories and as such can answer specific and fundamental questions in life sciences. Improving the knowledge on how plants respond to ionizing radiation can provide information applicable in all the fields in which radiation is studied on Earth ranging from breeding programs, decontamination methods and radioecology.

Future perspectives and recommendations in the short and long term

Today there is a need for fundamental research that goes beyond the demonstration of plants’ ability to acclimate and adapt to the space environment. A multi-parameter facility would help unravel the effects of altered gravity in combination with other factors, either typical of space (i.e. ionizing radiation) or of confined volumes of cultivation chambers. Moreover, by modulating the exposure to specific environmental conditions (e.g., air flow or light), it would be possible to study the direct and indirect effect of the space factors on plants, bridging the knowledge gaps of the acclimation/adaptation mechanisms.

Currently, to study plant development in the space environment through the whole life cycle of a plant, including crops/food plants, is possible only using the ISS research platform: no other active platforms possess capabilities for answering the plant biology research questions listed in this paper. The infrastructure present on ISS can be modernized to achieve the needed goals to point to the sustainability of space exploration with BLSS.

Using the ISS platform for research will be the defining stepping stone into exploratory-class missions deeper into space. International efforts are ongoing to design and develop additional payloads in the frame of the Artemis program (e.g., NASA PRISM solicitation) ( https://www.nasa.gov/feature/nasa-releases-prism-call-for-potential-lunar-surface-investigations ). The Gateway platform is also currently planned for lunar orbit in the mid-late 2020 s. This should provide opportunities for experiments deeper into space, particularly outside of Earth’s magnetic field and the unique radiation environment can be exploited to further develop our understanding of the effect that different types of radiation may have on plants in combination with other space factors.

It is not straightforward to indicate what are the more urgent goals of plant space biology since it has been recognized that space farming is becoming more and more a necessity as long as the roadmap for human space exploration goes beyond LEO (BLEO). A summary of possible goals (targets) within the main knowledge gaps (open fundamental scientific questions) identified in the previous paragraphs is reported in Fig. 3 .

Other research platforms such as ground, Moon, Mars, LEO and BLEO (beyond LEO) are also included. They represent both the basis for the research on ISS and future research activities post-ISS (e.g. the GATEWAY orbiting the Moon).

The first, second and third knowledge gaps should be addressed in experiments to be performed in the short- and medium-term since they will provide fundamental information that is the basis for the realization of more complex experiments in the long-term. The knowledge obtained in the short- and medium-term will be fundamental to defining requirements and developing new hardware to support long-term exploratory-class human missions. Indeed, in such missions, completely closed BLSS are themselves the “main requirement” although with technological differences depending on the scenarios determining the environmental constraints and mission duration.

In conclusion, to achieve successful space exploration, it is fundamental to apply an integrative approach in space biology merging together the information gained at different biological levels (e.g. molecular, cellular, tissue/organ up to the whole individual) as well as integrating knowledge among organisms (producers, consumers and degraders) also to understand the effect of space factors on their capability of networking in the artificial ecosystem as in nature on Earth. Space biology has been historically divided into sub-disciplines dealing with animals/mammals, microbes and plants without much interaction. However, some processes of altered metabolism as those regarding DNA-repair mechanisms as well as ROS and peptide signaling as stress responses are well conserved among species (including animals and plants). This paves the way towards the need for making synergies among disciplines to achieve an integrated picture of common vs distinct responses to space factors in different organisms. Possibly, the establishment of global standard operating procedures for space omics (including metagenomics) data sets generation and annotation, including but not limited to those generated within the framework of ESA and NASA projects, can allow the expansion of statistical power in space flight experiments by means of the federation of data sets.

Indeed, it has been recognized that to achieve BLSS operating in space and guarantee better protection of human health and well-being in space, an integrated, multidisciplinary approach linking together different branches of life science (e.g. animal and human physiology, plant biology, microbiology, etc.) is needed, as well as the cooperation with physical sciences, technologies and engineering. Therefore, there is a need to bridge and strengthen the interconnections between them also through the design, proposal, and realization of new studies and experiments.

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Acknowledgements

This work was supported by the European Space Agency (ESA). This perspective paper is based upon work from the Contributors to the Topic C “Plant Biology” of the ESA SciSpacE white paper “Biology in Space and Analogue Environments”, listed in alphabetic order: Giovanna Aronne, Nicol Caplin, Eugénie Carnero-Diaz, Raúl Herranz, Nele Horemans, Ann-Iren Kittang Jost (Coordinator), Valerie Legue, F. Javier Medina, Veronica De Micco, (Coordinator), Veronica Pereda-Campos, Mona Schiefloe.

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Department of Agricultural Sciences, University of Naples Federico II, via Università 100, 80055, Portici (NA), Italy

Veronica De Micco, Giovanna Aronne, Sara De Francesco & Luigi Gennaro Izzo

SciSpacE Team, Directorate of Human and Robotic Exploration Programmes, European Space Agency (ESA), Noordwijk, Netherlands

Nicol Caplin

Institute of Systematic, Evolution, Biodiversity, Sorbonne University, National Museum of Natural History, CNRS, EPHE, UA, 45, rue Buffon CP50, 75005, Paris, France

Eugénie Carnero-Diaz & Isabel Le Disquet

Centro de Investigaciones Biológicas Margarita Salas - CSIC, Ramiro de Maeztu 9, 28040, Madrid, Spain

Raúl Herranz & F. Javier Medina

Belgian Nuclear Research Centre (SCK CEN), Biosphere Impact Studies (BIS), Boeretang 200, 2400, Mol, Belgium

Nele Horemans

Université Clermont Auvergne, INRAE, PIAF, F-63000, Clermont-Ferrand, France

Valérie Legué

GSBMS/ Evolsan UFR Santé, University of Toulouse III, Toulouse, France

Veronica Pereda-Loth

NTNU Social Research, Centre for Interdisciplinary Research in Space (CIRiS) Dragvoll Allé 38 B, 7049, Trondheim, Norway

Mona Schiefloe & Ann- Iren Kittang Jost

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V.D., G.A., N.C., E.C., R.H., N.H., V.L., J.M., V.P., M.S. and A.K. developed the concept of this perspective paper. V.D., G.A., S.D. and L.I. developed a first structure of the manuscript. V.D. took lead in coordination and writing; G.A., N.C., E.C., S.D., R.H., N.H., L.I., I.L.D., V.L., J.M., V.P., M.S. and A.K. wrote specific parts of the manuscript. All authors provided critical feedback and helped shape the concept and perspectives. All authors revised and approved the submitted version of the manuscript.

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Correspondence to Veronica De Micco .

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De Micco, V., Aronne, G., Caplin, N. et al. Perspectives for plant biology in space and analogue environments. npj Microgravity 9 , 67 (2023). https://doi.org/10.1038/s41526-023-00315-x

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Received : 10 November 2022

Accepted : 02 August 2023

Published : 21 August 2023

DOI : https://doi.org/10.1038/s41526-023-00315-x

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