Gene-by-environment interactions influence the fitness cost of gene copy-number variation in yeast

Robinson, DeElegant; Vanacloig-Pedros, Elena; Cai, Ruoyi; Place, Michael; Hose, James; Gasch, Audrey P.; Hahn, ed., M.

doi:10.1093/g3journal/jkad159

Gene-by-environment interactions influence the fitness cost of gene copy-number variation in yeast

Journal Article · Sat Jul 22 00:00:00 EDT 2023 · G3

DOI:https://doi.org/10.1093/g3journal/jkad159· OSTI ID:2007080

Robinson, DeElegant; Vanacloig-Pedros, Elena; Cai, Ruoyi; Place, Michael; Hose, James; ; Hahn, ed., M.

Abstract

Variation in gene copy number can alter gene expression and influence downstream phenotypes; thus copy-number variation provides a route for rapid evolution if the benefits outweigh the cost. We recently showed that genetic background significantly influences how yeast cells respond to gene overexpression, revealing that the fitness costs of copy-number variation can vary substantially with genetic background in a common-garden environment. But the interplay between copy-number variation tolerance and environment remains unexplored on a genomic scale. Here, we measured the tolerance to gene overexpression in four genetically distinct Saccharomyces cerevisiae strains grown under sodium chloride stress. Overexpressed genes that are commonly deleterious during sodium chloride stress recapitulated those commonly deleterious under standard conditions. However, sodium chloride stress uncovered novel differences in strain responses to gene overexpression. West African strain NCYC3290 and North American oak isolate YPS128 are more sensitive to sodium chloride stress than vineyard BC187 and laboratory strain BY4743. Consistently, NCYC3290 and YPS128 showed the greatest sensitivities to overexpression of specific genes. Although most genes were deleterious, hundreds were beneficial when overexpressed—remarkably, most of these effects were strain specific. Few beneficial genes were shared between the sodium chloride-sensitive isolates, implicating mechanistic differences behind their sodium chloride sensitivity. Transcriptomic analysis suggested underlying vulnerabilities and tolerances across strains, and pointed to natural copy-number variation of a sodium export pump that likely contributes to strain-specific responses to overexpression of other genes. Our results reveal extensive strain-by-environment interactions in the response to gene copy-number variation, raising important implications for the accessibility of copy-number variation-dependent evolutionary routes under times of stress.

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Research Organization:: Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0018409

OSTI ID:: 2007080

Alternate ID(s):: OSTI ID: 2471956
OSTI ID: 1996029

Journal Information:: G3, Journal Name: G3 Journal Issue: 10 Vol. 13; ISSN 2160-1836

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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