Domestication reprogrammed the budding yeast life cycle

Matteo De Chiara; Benjamin Barré; Karl Persson; Amadi Onyetuga Chioma; Agurtzane Irizar; Joseph Schacherer; Jonas Warringer; Gianni Liti

Because the yeast domestication syndrome is shared across genetically distinct, independently domesticated clades, it is unlikely to reflect the retention of ancestral trait that have been lost in wild lineages 71 . Instead, it likely represents convergent evolution where the . CC-BY-NC-ND 4.0 International license author/funder. It is made available under a The copyright holder for this preprint (which was not peer-reviewed) is the . https://doi.org/10.1101/2020.02.08.939314 doi: bioRxiv preprint convergence was driven by domestication. Such a convergence could have both adaptive and neutral explanations. First, the domestication syndrome re-oriented both carbon and nitrogen metabolism from better respiratory to better fermentative growth. This can easily be rationalized as adaptation. Domestication niches, such as grape must with a 20% glucose/fructose content, are often rich in easily fermented sugars. Ethanol production, which is the principle trait selected for in most domestication environments, depends on efficient fermentation of these sugars. Respiration of the sugar, or of the produced ethanol, is both counterproductive to high ethanol content and discouraged by high sugar and, later, low oxygen. The better beer yeast fermentation of malt sugars to ethanol 23 , is widely held to reflect domestication driven adaptation. In contrast, concentrated sugar is relative rare in wild niches and competition for it is fierce, with concentrations unlikely to often exceed the 0.5% threshold at which sugar fermentation kicks in. In contrast to in large industrial tanks where the oxygen is rapidly depleted, oxygen is also often freely available in natural yeast niches, allowing respiration. Second, we found sporulation genes to associate to clade specific loss-of-function variants in genes private to sporulation and meiosis. This is consistent with a neutral drift model, where asexual proliferation in domestication niches relaxes selection on superfluous sporulation and meiosis genes, leaving them free to accumulate mutations. Many of these variants affected the key meiosis specific transcription factors IME1 and NDT80 that are absolutely required for sporulation 72 , underscoring that there is little selective pressure to retain sporulation intact in domesticated isolates.