DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds

Genome integrity is crucial for cellular survival and the faithful transmission of genetic information. The eukaryotic cellular response to DNA damage is orchestrated by the DNA damage checkpoint kinases ATAXIA TELANGIECTASIA MUTATED (ATM) and ATM AND RAD3-RELATED (ATR). Here we identify important physiological roles for these sensor kinases in control of seed germination. We demonstrate that double strand breaks (DSBs) are rate-limiting for germination. We identify that desiccation tolerant seeds exhibit a striking transcriptional DSB damage response during germination, indicative of high levels of genotoxic stress, which is induced following maturation drying and quiescence. Mutant atr and atm seeds are highly resistant to ageing, establishing ATM and ATR as determinants of seed viability. In response to ageing, ATM delays germination, while atm mutant seed germinate with extensive chromosomal abnormalities. This reveals ATM as a major factor which controls germination in aged seed, integrating progression through germination with surveillance of genome integrity. Mechanistically ATM functions through control of DNA replication in imbibing seeds. ATM signaling is mediated by transcriptional control of the cell cycle inhibitor SIAMESE-RELATED 5, an essential factor required for the ageing-induced delay to germination. In the soil seed bank, seeds exhibit increased transcript levels of ATM and ATR with changes in dormancy and germination potential, modulated by environmental signals including temperature and soil moisture. Collectively our findings reveal physiological functions for these sensor kinases in linking genome integrity to germination, thereby influencing seed quality, crucial for plant survival in the natural environment and sustainable crop production.