Chronic Ionizing Radiation of Plants: An Evolutionary Factor from Direct Damage to Non-Target Effects

Abstract

In present times, the levels of ionizing radiation (IR) on the surface of Earth are relatively low, posing no high challenges for the survival of contemporary life forms. IR derives from natural sources and naturally occurring radioactive materials (NORM), the nuclear industry, medical applications, and as a result of radiation disasters or nuclear tests. In the current review, we discuss modern sources of radioactivity, its direct and indirect effects on different plant species, and the scope of the radiation protection of plants. We present an overview of the molecular mechanisms of radiation responses in plants, which leads to a tempting conjecture of the evolutionary role of IR as a limiting factor for land colonization and plant diversification rates. The hypothesis-driven analysis of available plant genomic data suggests an overall DNA repair gene families' depletion in land plants compared to ancestral groups, which overlaps with a decrease in levels of radiation exposure on the surface of Earth millions of years ago. The potential contribution of chronic IR as an evolutionary factor in combination with other environmental factors is discussed.

Keywords: DNA damage; acute exposure; antioxidants; chronic exposure; hormesis; nuclear accident; plant evolution; plant terrestrialization; repair pathway; trade-off.

Figure 1

Overview of ionizing radiation (IR) sources and their effect on living organisms. IR can cause direct (green arrow) or indirect (blue arrows) damage to living organisms. The latter is a consequence of the generation of reactive oxygen species (ROS) due to the radiolysis of water by the ionizing high-energy particles or waves. Yet, ROS are also innate to cell metabolism and act as signalling molecules, meaning that upon IR exposure the cells undergo homeostatic imbalance.

Figure 2

Scheme representing the IR-promoted water radiolysis steps, resulting in the generation of free radicals and ROS. H₂O* represents excited water molecule. Adapted from [64].

Figure 3

Environmental factors that may have contributed to the evolution of the plant DNA repair machinery. The gases’ partial pressure, relative solar flux, and sea level UV are in comparison to present time values. Both panels are plotted as a function of time in billions of years. Geological eras are represented at the bottom and include main life evolution events according to fossil records [196,231,232,233] and phylogenetic inference [207,208,209]. (A). Curves 1 (1–20 Å, high-energy) and 2 (920–1200 Å) represent solar normalized fluxes over time [15,189]. Curves 3 and 4 represent the relative CO₂ and O₂ pressures over time [234,235]. The blue-shaded area represents the expected establishment of the shielding ozone layer ca. 600 Mya, which may have depended on the increase of Earth’s magnetosphere [15,226]. (B). Curve 5 represents the sea level UV flux over time, which had sharp drops attributed to atmosphere oxygenation [188]. Curve 6 shows the changes in background radiation levels over time [188].

Figure 4

Evolution of DNA repair gene families in Viridiplantae. (A) Comparison of family expansion/depletion among basal Viridiplantae (Chlorophyta + Prasinodermophyta), basal land plants (Lycopodiopsida + Anthocerotopsida + Marchantiopsida + Bryopsida), and remaining land plants (Magnoliopsida + Pinopsida). The gene family evolution rate (ER) values are given in Table S1, and calculation details are given in Appendix A. In summary, family expansion is represented by values > 1 and depletion by values < 1. The ER was assessed by the gene copy number of a given family compared to the proteome size of each species, normalized over all species. Gene families’ data were retrieved from PLAZA V5 (https://bioinformatics.psb.ugent.be/plaza/, accessed on 1 October 2021) and are provided in Table S1. (B–D). For each DNA repair gene family (y axis), the relative fold change of the ER was calculated between each Streptophyta (vascular plants, x axis) and each basal Viridiplantae: C. reinhardtii (panel B), M. commode (panel C), and P. colonial (panel D). The representation of the gene families in the y axis (top-bottom) follows the same order as the x axis labels in panel (A) (left-right).