Genome-wide association across Saccharomyces cerevisiae strains reveals substantial variation in underlying gene requirements for toxin tolerance

Sardi, Maria; Paithane, Vaishnavi; Place, Michael; Robinson, De Elegant; Hose, James; Wohlbach, Dana J.; Gasch, Audrey P.; Fay, Justin C.

doi:10.1371/journal.pgen.1007217

Title: Genome-wide association across Saccharomyces cerevisiae strains reveals substantial variation in underlying gene requirements for toxin tolerance

Journal Article · Fri Feb 23 00:00:00 EST 2018 · PLoS Genetics

DOI:https://doi.org/10.1371/journal.pgen.1007217· OSTI ID:1499878

^[1];

^[2];

^[2]; Robinson, De Elegant ^[3]; Hose, James ^[4]; Wohlbach, Dana J. ^[2];

^[5]; Fay, Justin C. ^[6]

Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center, and Microbiology Training Program
Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
Univ. of Wisconsin, Madison, WI (United States). Microbiology Training Program
Univ. of Wisconsin, Madison, WI (United States). Lab. of Genetics
Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center, Lab. of Genetics
Univ. of Rochester, NY (United States)

Cellulosic plant biomass is a promising sustainable resource for generating alternative biofuels and biochemicals with microbial factories. But a remaining bottleneck is engineering microbes that are tolerant of toxins generated during biomass processing, because mechanisms of toxin defense are only beginning to emerge. Here, we exploited natural diversity in 165 Saccharomyces cerevisiae strains isolated from diverse geographical and ecological niches, to identify mechanisms of hydrolysate-toxin tolerance. We performed genome-wide association (GWA) analysis to identify genetic variants underlying toxin tolerance, and gene knockouts and allele-swap experiments to validate the involvement of implicated genes. In the process of this work, we uncovered a surprising difference in genetic architecture depending on strain background: in all but one case, knockout of implicated genes had a significant effect on toxin tolerance in one strain, but no significant effect in another strain. In fact, whether or not the gene was involved in tolerance in each strain background had a bigger contribution to strain-specific variation than allelic differences. Our results suggest a major difference in the underlying network of causal genes in different strains, suggesting that mechanisms of hydrolysate tolerance are very dependent on the genetic background. These results could have significant implications for interpreting GWA results and raise important considerations for engineering strategies for industrial strain improvement.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1499878

Journal Information:: PLoS Genetics, Vol. 14, Issue 2; ISSN 1553-7404

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 30 works

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QTL analysis of natural Saccharomyces cerevisiae isolates reveals unique alleles involved in lignocellulosic inhibitor tolerance de Witt, R. N.; Kroukamp, H.; Van Zyl, W. H. FEMS Yeast Research, Vol. 19, Issue 5 https://doi.org/10.1093/femsyr/foz047	journal	July 2019
Effects of a high-cultivation temperature on the physiology of three different Yarrowia lipolytica strains Hackenschmidt, S.; Bracharz, F.; Daniel, R. FEMS Yeast Research, Vol. 19, Issue 7 https://doi.org/10.1093/femsyr/foz068	journal	October 2019
Determinants of selection in yeast evolved by genome shuffling Biot-Pelletier, Damien; Pinel, Dominic; Larue, Kane Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1283-9	journal	October 2018
QTL analysis reveals genomic variants linked to high-temperature fermentation performance in the industrial yeast Wang, Zhen; Qi, Qi; Lin, Yuping Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1398-7	journal	March 2019
The genetic basis of aneuploidy tolerance in wild yeast Hose, James; Escalante, Leah E.; Clowers, Katie J. eLife, Vol. 9 https://doi.org/10.7554/elife.52063	journal	January 2020
Linkage mapping of yeast cross protection connects gene expression variation to a higher-order organismal trait Stuecker, Tara N.; Scholes, Amanda N.; Lewis, Jeffrey A. PLOS Genetics, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pgen.1007335	journal	April 2018
Correction to: QTL analysis reveals genomic variants linked to high-temperature fermentation performance in the industrial yeast Wang, Zhen; Qi, Qi; Lin, Yuping Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1425-8	journal	April 2019
Proteome response of two natural strains of Saccharomyces cerevisiae with divergent lignocellulosic inhibitor stress tolerance de Witt, R. N.; Kroukamp, H.; Volschenk, H. FEMS Yeast Research, Vol. 19, Issue 1 https://doi.org/10.1093/femsyr/foy116	journal	October 2018

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