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Heat Stress Interferes with Formation of Double-Strand Breaks and Homology Synapsis in Arabidopsis thaliana

Meiotic recombination (MR) drives reciprocal exchange of genetic information which allows novel combination of alleles and contributes to genomic diversity of eukaryotes. In this study, we report that heat stress (36-38°C) over fertile threshold fully abolishes crossover occurrence by lowering the formation of SPO11-dependent double-strand breaks (DSBs) in Arabidopsis. The high temperature partially suppresses chromosome fragmentation in the rad51 and syn1 mutants by reducing DSB formation. In addition, we found that although the SYN1-mediated formation of chromosome axis is not influenced by the high temperature, ASY1-associated axial element of synaptonemal complex (SC) is partially compromised, and the ZYP1-dependent central element of axis is severely disrupted, indicating that homology synapsis is another prominent target of high temperature. Besides, we observed that the loading of recombinase DMC1 on chromatin is significantly reduced by high temperatures, suggesting that heat stress interferes with DMC1-dependent MR. Moreover, we found that the numbers of DSB and DMC1 keep stable within a limited range of temperature increase, while decrease when the DSB-processing system reaches threshold to heat. Furthermore, transcriptome study revealed a universal variation of the expression of meiotic genes under low (4°C) and high (32°C) temperatures, suggesting that temperature may influence MR by modulating the transcription of MR-related factors. We also found that the landscape of 5-methylcytosine (5mC) was altered under high temperatures, suggesting that environmental temperature may influence the distribution of MR via reshaped DNA methylation status of chromatin. Taken together, our findings provide evidence shedding light on how environment temperatures influence MR in Arabidopsis.