Microevolution and stress tolerance of Arabidopsis thaliana from the Chernobyl-affected zone

Arabidopsis thaliana from the Chernobyl Exclusion Zone showed altered stress responses, reduced germination, and genomic signatures of microevolution affecting DNA repair, redox signalling and cell-cycle-related genes. Chronic exposure to ionising radiation (IR) in the Chernobyl Exclusion Zone (CEZ) has created a field experiment for plant evolution. We collected Arabidopsis thaliana seeds from a reference plot (Babchin) and two radioactively contaminated plots (Vygrebnaya Sloboda and Masany), established in vitro seed lines for each plot and studied their physiology and genomes. Seeds were challenged with acute γ-irradiation (150 Gy), heat (50 °C) and oxidative stress (0.01 µM methyl viologen). The radiation legacy manifested as contrasting stress response profiles and suppressed germination in chronically irradiated lines, which was rescued by exogenous ROS. Genome sequencing of plants from the heavily contaminated plot, Masany, revealed decreased nucleotide diversity and signs of a selective sweep, accompanied by increased fixation rates for single-nucleotide polymorphisms (SNPs) in exons. Compared with the non-irradiated reference population, genes that accumulated unique SNPs in Masany were related to DNA repair, cell cycle and mitosis, phragmoplast assembly, response to oxidative stress, Ca 2+ and ROS signalling, and epigenetic processes. Together, the data show that decades of low-dose irradiation drive rapid microevolution in A. thaliana , favouring mutations that bolster genome stability and stress-signalling networks whilst probably compromising seed performance. These findings provide the first field-scale genomic evidence of the targeted accumulation of mutations in specific genomic regions of chronically irradiated plants, suggesting that long-term exposure to chronic ionising radiation may alter population genetic structure.