Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance amongSaccharomycesspecies

Abstract

Over time, species evolve substantial phenotype differences. Yet, genetic analysis of these traits is limited by reproductive barriers to those phenotypes that distinguish closely related species. Here, we conduct a genome-wide non-complementation screen to identify genes that contribute to a major difference in thermal growth profile between two Saccharomyces species. S. cerevisiae is capable of growing at temperatures exceeding 40C, whereas S. uvarum cannot grow above 33C but outperforms S. cerevisiae at 4C. The screen revealed only a single nuclear-encoded gene with a modest contribution to heat tolerance, but a large effect of the species' mitochondrial DNA (mitotype). Furthermore, we found that, while the S. cerevisiae mitotype confers heat tolerance, the S. uvarum mitotype confers cold tolerance. Recombinant mitotypes indicate multiple genes contribute to thermal divergence. Mitochondrial allele replacements showed that divergence in the coding sequence of COX1 has a moderate effect on both heat and cold tolerance, but it does not explain the entire difference between the two mitochondrial genomes. Our results highlight a polygenic architecture for interspecific phenotypic divergence and point to the mitochondrial genome as an evolutionary hotspot for not only reproductive incompatibilities, but also thermal divergence in yeast.

Mitochondrial DNA and temperature tolerance in lager yeasts

“…et al(20), the identification of a role for mtDNA in temperature tolerance of these yeasts extends support for the mitochondrial climatic adaptation hypothesis (1) to fungi and suggests that the outsized role of mtDNA in controlling temperature tolerance may be general to eukaryotes.…”

“…In a companion study, Li et al found that the parent providing mtDNA in hybrids of S. cerevisiae and the cryotolerant species Saccharomyces uvarum had a large effect on temperature tolerance (20). Since Saccharomyces eubayanus is the sister species of S. uvarum but ~7% genetically divergent, we wondered whether the effect of mitotype would extend to industrial hybrids of S. cerevisiae x S. eubayanus, sometimes called Saccharomyces pastorianus (21).…”

Exposure of mammal genetic diversity to mid‐21st century global change

“…However, this assumption of neutrality is increasingly being challenged. Specifically, with regard to global warming, a growing body of research highlights the dual role of variation in the mitochondrial genome both in reflecting local adaptation to climate and in determining the thermal range that an organism can tolerate (Camus et al 2017, Lasne et al 2019, Li et al 2019). High levels of mitochondrial GD, particularly in warmer climates, are indicative of potentially beneficial standing variation that could encode for increased heat tolerance and buffer against rapid warming (Camus et al 2017, Li et al 2019).…”

Synthetic hybrids of six yeast species

“…4A). We recently demonstrated that, during the formation of S. cerevisiae × S. uvarum hybrids, the frequency of strains without a functional mtDNA was higher when the hybrid inherited a S. uvarum mtDNA, but introgression of the F-SceIII homing endonuclease gene restored normal mitochondrial retention 38 . Therefore, the absence of F-SceIII in yHRWh10 may have influenced the loss of mtDNA in its descendants, such as the six-species hybrid yHRWh36, which retained only small regions Step of hybridization Supplementary Fig.…”

“…51 ). Our combined mitochondrial reference genome was built with the mitochondrial assemblies of the aforementioned strains [50][51][52] , except for CBS7001, whose mtDNA is still not completely assembled 38 . Instead, we used the mtDNA of a close relative, S. uvarum CBS395 52 .…”