{"title":"Temperature affects recombination rate plasticity and meiotic success between thermotolerant and cold tolerant yeast species","authors":"Jessica McNeill, Nathan Brandt, Enrique J. Schwarzkopf, Mili Jimenez Gallardo, Caiti Smukowski Heil","doi":"10.1101/2024.08.28.610152","DOIUrl":null,"url":null,"abstract":"Meiosis is required for the formation of gametes in all sexually reproducing species and the process is well conserved across the tree of life. However, meiosis is sensitive to a variety of external factors, which can impact chromosome pairing, recombination, and fertility. For example, the optimal temperature for successful meiosis varies between species of plants and animals. This suggests that meiosis is temperature sensitive, and that natural selection may act on variation in meiotic success as organisms adapt to different environmental conditions. To understand how temperature alters the successful completion of meiosis, we utilized two species of the budding yeast <em>Saccharomyces</em> with different temperature preferences: thermotolerant <em>Saccharomyces cerevisiae</em> and cold tolerant <em>Saccharomyces uvarum</em>. We surveyed three metrics of meiosis: sporulation efficiency, spore viability, and recombination rate in multiple strains of each species. As per our predictions, the proportion of cells that complete meiosis and form spores is temperature sensitive, with thermotolerant <em>S. cerevisiae</em> having a higher temperature threshold for successful meiosis than cold tolerant <em>S. uvarum</em>. We confirmed previous observations that <em>S. cerevisiae</em> recombination rate varies between strains and across genomic regions, and add new results that <em>S. uvarum</em> has higher recombination rates than <em>S. cerevisiae</em>. We find that temperature significantly influences recombination rate plasticity in <em>S. cerevisiae</em> and <em>S. uvarum</em>, in agreement with studies in animals and plants. Overall, these results suggest that meiotic thermal sensitivity is associated with organismal thermal tolerance, and may even result in temporal reproductive isolation as populations diverge in thermal profiles.","PeriodicalId":501246,"journal":{"name":"bioRxiv - Genetics","volume":"30 1","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"bioRxiv - Genetics","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1101/2024.08.28.610152","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
Abstract
Meiosis is required for the formation of gametes in all sexually reproducing species and the process is well conserved across the tree of life. However, meiosis is sensitive to a variety of external factors, which can impact chromosome pairing, recombination, and fertility. For example, the optimal temperature for successful meiosis varies between species of plants and animals. This suggests that meiosis is temperature sensitive, and that natural selection may act on variation in meiotic success as organisms adapt to different environmental conditions. To understand how temperature alters the successful completion of meiosis, we utilized two species of the budding yeast Saccharomyces with different temperature preferences: thermotolerant Saccharomyces cerevisiae and cold tolerant Saccharomyces uvarum. We surveyed three metrics of meiosis: sporulation efficiency, spore viability, and recombination rate in multiple strains of each species. As per our predictions, the proportion of cells that complete meiosis and form spores is temperature sensitive, with thermotolerant S. cerevisiae having a higher temperature threshold for successful meiosis than cold tolerant S. uvarum. We confirmed previous observations that S. cerevisiae recombination rate varies between strains and across genomic regions, and add new results that S. uvarum has higher recombination rates than S. cerevisiae. We find that temperature significantly influences recombination rate plasticity in S. cerevisiae and S. uvarum, in agreement with studies in animals and plants. Overall, these results suggest that meiotic thermal sensitivity is associated with organismal thermal tolerance, and may even result in temporal reproductive isolation as populations diverge in thermal profiles.
减数分裂是所有有性生殖物种形成配子的必要条件,这一过程在整个生命之树上都得到了很好的保留。然而,减数分裂对各种外部因素很敏感,这些因素会影响染色体配对、重组和繁殖力。例如,减数分裂成功的最佳温度因动植物物种而异。这表明减数分裂对温度很敏感,自然选择可能在生物适应不同环境条件时对减数分裂成功率的变化产生作用。为了了解温度如何改变减数分裂的成功完成,我们利用了两种对温度有不同偏好的芽殖酵母:耐热的酿酒酵母和耐寒的酿酒酵母。我们调查了减数分裂的三个指标:孢子效率、孢子活力和每个物种多个菌株的重组率。根据我们的预测,完成减数分裂并形成孢子的细胞比例对温度很敏感,耐热的麦角菌减数分裂成功的温度阈值比耐寒的乌瓦鲁菌要高。我们证实了之前的观察结果,即麦角菌的重组率在不同菌株和不同基因组区域之间存在差异,并补充了新的结果,即uvarum的重组率高于麦角菌。我们发现,温度对 S. cerevisiae 和 S. uvarum 的重组率可塑性影响很大,这与动物和植物的研究结果一致。总之,这些结果表明,减数分裂热敏感性与生物体的热耐受性有关,甚至可能随着种群热分布的差异而导致时间上的生殖隔离。