Genetic variation in Arabidopsis thaliana reveals the existence of natural heat resilience factors for meiosis

Heat interferes with multiple meiotic processes, leading to genome instability and sterility in flowering plants, including many crops. Despite its importance for food security, the mechanisms underlying heat tolerance of meiosis are poorly understood. In this study, we analyzed different meiotic processes in the Arabidopsis (Arabidopsis thaliana) accessions Columbia (Col) and Landsberg erecta (Ler), their F1 hybrids, and the F2 offspring under heat stress (37°C). At 37°C, Col exhibits significantly reduced formation of double-strand breaks (DSBs) and completely abolished homolog pairing, synapsis, and crossover (CO) formation. Strikingly, Ler and Col/Ler hybrids exhibit normal CO formation and show mildly impacted homolog pairing and synapsis. Interestingly, only 10% ∼ 20% of F2 offspring behave as Ler, revealing that heat tolerance of meiotic recombination in Arabidopsis is genetically controlled by several loci. Moreover, F2 offspring show defects in chromosome morphology and integrity and sister-chromatid segregation, the levels of which exceed those in either inbreds and/or hybrids, thus implying a transgressive effect on heat tolerance of meiosis. Furthermore, correlation and cytogenetic analyses suggest that homolog pairing and/or synapsis have an impact on heat tolerance of chromosome morphology and stability at post-recombination stages. This study reveals natural heat resilience factors for meiosis in Arabidopsis, which have the great potential to be exploited in breeding programs.