Ionizing Radiation, Higher Plants, and Radioprotection: From Acute High Doses to Chronic Low Doses

Abstract

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.

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

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).

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 O₂ to produce dioxygen radicals (O₂^- – ‘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/m², 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/m² – 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).

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 ³³Xe (6.5 EBq, λ = 5.3 days), ¹³²Te (1.15 EBq, λ = 3.25 days), ¹³¹I (1.76 EBq, λ = 8 days), ⁹⁹Mo (0.2 EBq, λ= 2.79 days), ¹⁴¹Ce (0.2 EBq, λ= 33 days). After a few years the remaining radioactivity was dominated by ¹³⁷Cs, ¹³⁴Cs plus some ⁹⁰Sr and ²⁴¹Pu. Radioactivity is now dominated by ¹³⁷Cs. 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).

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).

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.

FIGURE 7

Oxidizing radicals from O₃ exposure compared to those from background IR, Chernobyl and UV. Concentrations of tens of ppb O₃ have documented effects on plants and concentrations of >150 ppb can have visible effects. To calculate the total radical production by O₃ in nM/m²/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 O₃ 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 O₃ dissolved to water at the appropriate range of partial pressures was calculated. To calculate radicals in nM/m²/s we assumed ten thousand liters of air per m² (i.e., a relatively shallow depth of air), an effectively infinite supply of O₃ and that every O₃ molecule produced a radical. The dissolution of O₃ 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 O₃ deemed to have no oxidative effects on plants. (Details of calculations are given in Supplementary Data Sheet S5).