ATM-mediated double-strand break repair is required for meiotic genome stability at high temperature

In eukaryotes, meiotic recombination maintains genome stability and creates genetic diversity. The conserved Ataxia-Telangiectasia Mutated (ATM) kinase regulates multiple processes in meiotic homologous recombination, including DNA double-strand break (DSB) formation and repair, synaptonemal complex organization, and crossover formation and distribution. However, its function in plant meiotic recombination under stressful environmental conditions remains poorly understood. In this study, we demonstrate that ATM is required for the maintenance of meiotic genome stability under heat stress in Arabidopsis thaliana. Using cytogenetic approaches we determined that ATM does not mediate reduced DSB formation but does ensure successful DSB repair, and thus meiotic chromosome integrity, under heat stress. Further genetic analysis suggested that ATM mediates DSB repair at high temperature by acting downstream of the MRE11-RAD50-NBS1 (MRN) complex, and acts in a RAD51-independent but chromosome axis-dependent manner. This study extends our understanding on the role of ATM in DSB repair and the protection of genome stability in plants under high temperature stress. Heat stress affects meiotic recombination and thus influences genome diversity and stability in plants. In eukaryotes, the conserved kinase ATM regulates multiple meiotic recombination processes; however, its role in meiotic recombination in plants under high temperature conditions remains unknown. In this study, we report that ATM, by acting downstream of the MRN complex, mediates a RAD51-independent but chromosome axis-dependent DSB repair mechanism to protect meiotic genome integrity in Arabidopsis under heat stress.