Impacts of temperature on recombination rate and meiotic success in thermotolerant and cold-tolerant yeast species

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 completion of 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 comparably high recombination rates. We find significant recombination rate plasticity due to temperature 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.

Fig. 1. Sporulation efficiency and spore viability of all S. cerevisiae and S. uvarum strains.

“Pure” strain diploids are bolded and distinguishable from their heterozygous counterparts by their listed genotype. A Heatmap displaying average sporulation efficiency (%) of each strain calculated from 3 biological replicates sporulated at each temperature for a minimum of 10 days. No data was collected for “pure” strains at temperatures above/below those where no appreciable spores were observed. Additionally, no data were collected for S. uvarum strains at 42 °C. B Average sporulation efficiency (%) of each species at each measured temperature. Plots display data of heterozygous strain, “pure” strain, and all species datasets, respectively. Error bars indicate standard error across all species’ strain replicates. For S. cerevisiae “pure” strains, an average sporulation efficiency of zero was assumed for temperatures measured not collected for some strains (4 °C, 10 °C, and 42 °C) due to failure at more moderate ends of the range. C Spore viability (%) calculated from at least 21 meioses (84 spores) of 6 selected strains from each species. Temperatures were selected to correspond with the known thermal preference and observed lower and upper boundaries of successful sporulation within each species. Stars denote significance as revealed through a Fisher's exact test (assuming a 95% confidence interval), followed with a post-hoc pairwise Fisher’s exact test (p-values corrected using Benjamini-Hochberg FDR method at a 5% cut-off).

Fig. 2. Average recombination rate (cM/kb) calculated for the syntenic intervals of 4 (on ChrVI) and 13 (on ChrXI) in S. cerevisiae and S.uvarum across all measured temperatures.

S. cerevisiae recombination rate estimates were corrected for fluorescence extinction using a maximum likelihood model derived in Raffoux et al. (2018a). S. uvarum recombination rate estimates were corrected for fluorescence extinction using a derivative of this script adjusted for only two fluorescent loci. No data was collected for S. uvarum strains at 42 °C. In strain-level comparisons (A), strain name refers to the parent strain crossed with each fluorescent tester to produce a diploid for sporulation. Error bars indicate standard deviation above and below the mean, as calculated between biological replicates of each strain. In species-level comparisons, (B) error bars indicate standard error across all species’ strain replicates.