Negative supercoil senses temperature to modulate meiotic crossovers and chromosomes

Crossover recombination is a hallmark of meiosis, which holds the paternal and maternal chromosomes (homologs) together for their faithful separation, meanwhile, it promotes genetic diversity of progenies. The pattern of crossover is mainly controlled by the architecture of meiotic chromosomes. Environmental factors, especially temperature, also play an important role in modulating crossovers. However, it is unclear how temperature affects crossovers. Here, we examined the distributions of budding yeast axis components (Red1, Hop1, and Rec8) and the CO-associated Zip3 foci in detail in different temperatures, and found that both increased and decreased temperatures result in shorter meiotic chromosome axes and more crossovers. Further investigations showed that altered temperature coordinately enhanced the hyperabundant accumulation of Hop1 and Red1 on chromosomes and the number of Zip3 foci. Most importantly, temperature-induced alterations in axis distribution and Zip3 foci depend on the changes in DNA negative supercoil. These findings suggest that yeast meiosis senses temperature changes by increasing the level of negative supercoil to increase crossovers and modulate chromosome organization. These findings provide a novel view in understanding the effect and mechanism of temperature on meiosis recombination and chromosome organization, and thus also have an important implication in evolution and breeding.交换重组（crossover recombination）是减数分裂（meiosis）的标志性特征，其可使父本与母本染色体（同源染色体，homologs）相互结合，保障二者精准分离，同时还能提升子代的遗传多样性。交换的模式主要受减数分裂染色体轴（meiotic chromosome axes）的结构调控。环境因子，尤其是温度，在调控交换过程中同样发挥着重要作用。然而，温度如何影响交换的具体机制仍未明确。本研究详细分析了不同温度条件下出芽酵母（budding yeast）的轴组分（Red1、Hop1及Rec8）以及与交换相关的Zip3焦点（Zip3 foci）的分布情况，结果发现，温度升高或降低均会导致减数分裂染色体轴缩短，同时增加交换事件的数量。进一步研究显示，温度改变会协同促进Hop1与Red1在染色体上的过度积累，并提升Zip3焦点的数量。最为关键的是，温度诱导的轴分布与Zip3焦点变化，依赖于DNA负超螺旋（DNA negative supercoil）的改变。上述研究结果表明，酵母减数分裂可通过提升负超螺旋水平感知温度变化，进而增加交换事件并调控染色体组织结构。本研究为理解温度对减数分裂重组及染色体组织结构的影响与机制提供了全新视角，同时也为进化与育种研究提供了重要的理论启示。