Heat stress impairs centromere structure and segregation of meiotic chromosomes in Arabidopsis

Heat stress is a major threat to global crop production, and understanding its impact on plant fertility is crucial for developing climate-resilient crops. Despite the known negative effects of heat stress on plant reproduction, the underlying molecular mechanisms remain poorly understood. Here, we investigated the impact of elevated temperature on centromere structure and chromosome segregation during meiosis in Arabidopsis thaliana. Our findings reveal that heat stress causes a significant decline in fertility and leads to the formation of micronuclei in pollen mother cells, along with an extended duration of meiotic division. We also demonstrate a reduction in the amounts of centromeric histone and the kinetochore protein BMF1 at meiotic centromeres with increasing temperature. Furthermore, we show that heat stress prolongs the activity of the spindle assembly checkpoint during meiosis I, indicating impaired efficiency of the kinetochore attachments to spindle microtubules. Our analysis of mutants with reduced amounts of centromeric histone suggests that weakened centromeres sensitize plants to elevated temperature, resulting in meiotic defects and reduced fertility even at moderate temperatures. These results indicate that the structure and functionality of meiotic centromeres in Arabidopsis are highly sensitive to heat stress, and suggest that centromeres and kinetochores may represent a crucial bottleneck in plant adaptation to increasing temperatures.