A new system for comparative functional genomics of Saccharomyces yeasts

Amy A. Caudy, Yuanfang Guan, Yue Jia, Christina Hansen, Chris DeSevo, Alicia P. Hayes, Joy Agee, Juan R. Alvarez-Dominguez, Hugo Arellano, Daniel Barrett, Cynthia Bauerle, Namita Bisaria, Patrick H. Bradley, J. Scott Breunig, Erin Bush, David Cappel, Emily Capra, Walter Chen, John Clore, Peter A. CombsChristopher Doucette, Olukunle Demuren, Peter Fellowes, Sam Freeman, Evgeni Frenkel, Daniel Gadala-Maria, Richa Gawande, David Glass, Samuel Grossberg, Anita Gupta, Latanya Hammonds-Odie, Aaron Hoisos, Jenny Hsi, Yu Han Huang Hsu, Sachi Inukai, Konrad J. Karczewski, Xiaobo Ke, Mina Kojima, Samuel Leachman, Danny Lieber, Anna Liebowitz, Julia Liu, Yufei Liu, Trevor Martin, Jose Mena, Rosa Mendoza, Cameron Myhrvold, Christian Millian, Sarah Pfau, Sandeep Raj, Matt Rich, Joe Rokicki, William Rounds, Michael Salazar, Matthew Salesi, Rajani Sharma, Sanford Silverman, Cara Singer, Sandhya Sinha, Max Staller, Philip Stern, Hanlin Tang, Sharon Weeks, Maxwell Weidmann, Ashley Wolf, Carmen Young, Jie Yuan, Christopher Crutchfield, Megan McClean, Coleen T. Murphy, Manuel Llinás, David Botstein, Olga G. Troyanskaya, Maitreya J. Dunham

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

Whole-genome sequencing, particularly in fungi, has progressed at a tremendous rate. More difficult, however, is experimental testing of the inferences about gene function that can be drawn from comparative sequence analysis alone. We present a genome-wide functional characterization of a sequenced but experimentally understudied budding yeast, Saccharomyces bayanus var. uvarum (henceforth referred to as S. bayanus), allowing us to map changes over the 20 million years that separate this organism from S. cerevisiae. We first created a suite of genetic tools to facilitate work in S. bayanus. Next, we measured the gene-expression response of S. bayanus to a diverse set of perturbations optimized using a computational approach to cover a diverse array of functionally relevant biological responses. The resulting data set reveals that gene-expression patterns are largely conserved, but significant changes may exist in regulatory networks such as carbohydrate utilization and meiosis. In addition to regulatory changes, our approach identified gene functions that have diverged. The functions of genes in core pathways are highly conserved, but we observed many changes in which genes are involved in osmotic stress, peroxisome biogenesis, and autophagy. A surprising number of genes specific to S. bayanus respond to oxidative stress, suggesting the organism may have evolved under different selection pressures than S. cerevisiae. This work expands the scope of genome-scale evolutionary studies from sequence-based analysis to rapid experimental characterization and could be adopted for functional mapping in any lineage of interest. Furthermore, our detailed characterization of S. bayanus provides a valuable resource for comparative functional genomics studies in yeast.

Original languageEnglish (US)
Pages (from-to)275-287
Number of pages13
JournalGenetics
Volume195
Issue number1
DOIs
StatePublished - Sep 17 2013

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Saccharomyces
Genomics
Yeasts
Genes
Genome
Sequence Analysis
Saccharomyces cerevisiae
Gene Expression
Saccharomycetales
Peroxisomes
Osmotic Pressure
Autophagy
Meiosis
Oxidative Stress
Fungi
Carbohydrates
Pressure

All Science Journal Classification (ASJC) codes

  • Genetics

Cite this

Caudy, A. A., Guan, Y., Jia, Y., Hansen, C., DeSevo, C., Hayes, A. P., ... Dunham, M. J. (2013). A new system for comparative functional genomics of Saccharomyces yeasts. Genetics, 195(1), 275-287. https://doi.org/10.1534/genetics.113.152918
Caudy, Amy A. ; Guan, Yuanfang ; Jia, Yue ; Hansen, Christina ; DeSevo, Chris ; Hayes, Alicia P. ; Agee, Joy ; Alvarez-Dominguez, Juan R. ; Arellano, Hugo ; Barrett, Daniel ; Bauerle, Cynthia ; Bisaria, Namita ; Bradley, Patrick H. ; Scott Breunig, J. ; Bush, Erin ; Cappel, David ; Capra, Emily ; Chen, Walter ; Clore, John ; Combs, Peter A. ; Doucette, Christopher ; Demuren, Olukunle ; Fellowes, Peter ; Freeman, Sam ; Frenkel, Evgeni ; Gadala-Maria, Daniel ; Gawande, Richa ; Glass, David ; Grossberg, Samuel ; Gupta, Anita ; Hammonds-Odie, Latanya ; Hoisos, Aaron ; Hsi, Jenny ; Hsu, Yu Han Huang ; Inukai, Sachi ; Karczewski, Konrad J. ; Ke, Xiaobo ; Kojima, Mina ; Leachman, Samuel ; Lieber, Danny ; Liebowitz, Anna ; Liu, Julia ; Liu, Yufei ; Martin, Trevor ; Mena, Jose ; Mendoza, Rosa ; Myhrvold, Cameron ; Millian, Christian ; Pfau, Sarah ; Raj, Sandeep ; Rich, Matt ; Rokicki, Joe ; Rounds, William ; Salazar, Michael ; Salesi, Matthew ; Sharma, Rajani ; Silverman, Sanford ; Singer, Cara ; Sinha, Sandhya ; Staller, Max ; Stern, Philip ; Tang, Hanlin ; Weeks, Sharon ; Weidmann, Maxwell ; Wolf, Ashley ; Young, Carmen ; Yuan, Jie ; Crutchfield, Christopher ; McClean, Megan ; Murphy, Coleen T. ; Llinás, Manuel ; Botstein, David ; Troyanskaya, Olga G. ; Dunham, Maitreya J. / A new system for comparative functional genomics of Saccharomyces yeasts. In: Genetics. 2013 ; Vol. 195, No. 1. pp. 275-287.
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abstract = "Whole-genome sequencing, particularly in fungi, has progressed at a tremendous rate. More difficult, however, is experimental testing of the inferences about gene function that can be drawn from comparative sequence analysis alone. We present a genome-wide functional characterization of a sequenced but experimentally understudied budding yeast, Saccharomyces bayanus var. uvarum (henceforth referred to as S. bayanus), allowing us to map changes over the 20 million years that separate this organism from S. cerevisiae. We first created a suite of genetic tools to facilitate work in S. bayanus. Next, we measured the gene-expression response of S. bayanus to a diverse set of perturbations optimized using a computational approach to cover a diverse array of functionally relevant biological responses. The resulting data set reveals that gene-expression patterns are largely conserved, but significant changes may exist in regulatory networks such as carbohydrate utilization and meiosis. In addition to regulatory changes, our approach identified gene functions that have diverged. The functions of genes in core pathways are highly conserved, but we observed many changes in which genes are involved in osmotic stress, peroxisome biogenesis, and autophagy. A surprising number of genes specific to S. bayanus respond to oxidative stress, suggesting the organism may have evolved under different selection pressures than S. cerevisiae. This work expands the scope of genome-scale evolutionary studies from sequence-based analysis to rapid experimental characterization and could be adopted for functional mapping in any lineage of interest. Furthermore, our detailed characterization of S. bayanus provides a valuable resource for comparative functional genomics studies in yeast.",
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Caudy, AA, Guan, Y, Jia, Y, Hansen, C, DeSevo, C, Hayes, AP, Agee, J, Alvarez-Dominguez, JR, Arellano, H, Barrett, D, Bauerle, C, Bisaria, N, Bradley, PH, Scott Breunig, J, Bush, E, Cappel, D, Capra, E, Chen, W, Clore, J, Combs, PA, Doucette, C, Demuren, O, Fellowes, P, Freeman, S, Frenkel, E, Gadala-Maria, D, Gawande, R, Glass, D, Grossberg, S, Gupta, A, Hammonds-Odie, L, Hoisos, A, Hsi, J, Hsu, YHH, Inukai, S, Karczewski, KJ, Ke, X, Kojima, M, Leachman, S, Lieber, D, Liebowitz, A, Liu, J, Liu, Y, Martin, T, Mena, J, Mendoza, R, Myhrvold, C, Millian, C, Pfau, S, Raj, S, Rich, M, Rokicki, J, Rounds, W, Salazar, M, Salesi, M, Sharma, R, Silverman, S, Singer, C, Sinha, S, Staller, M, Stern, P, Tang, H, Weeks, S, Weidmann, M, Wolf, A, Young, C, Yuan, J, Crutchfield, C, McClean, M, Murphy, CT, Llinás, M, Botstein, D, Troyanskaya, OG & Dunham, MJ 2013, 'A new system for comparative functional genomics of Saccharomyces yeasts', Genetics, vol. 195, no. 1, pp. 275-287. https://doi.org/10.1534/genetics.113.152918

A new system for comparative functional genomics of Saccharomyces yeasts. / Caudy, Amy A.; Guan, Yuanfang; Jia, Yue; Hansen, Christina; DeSevo, Chris; Hayes, Alicia P.; Agee, Joy; Alvarez-Dominguez, Juan R.; Arellano, Hugo; Barrett, Daniel; Bauerle, Cynthia; Bisaria, Namita; Bradley, Patrick H.; Scott Breunig, J.; Bush, Erin; Cappel, David; Capra, Emily; Chen, Walter; Clore, John; Combs, Peter A.; Doucette, Christopher; Demuren, Olukunle; Fellowes, Peter; Freeman, Sam; Frenkel, Evgeni; Gadala-Maria, Daniel; Gawande, Richa; Glass, David; Grossberg, Samuel; Gupta, Anita; Hammonds-Odie, Latanya; Hoisos, Aaron; Hsi, Jenny; Hsu, Yu Han Huang; Inukai, Sachi; Karczewski, Konrad J.; Ke, Xiaobo; Kojima, Mina; Leachman, Samuel; Lieber, Danny; Liebowitz, Anna; Liu, Julia; Liu, Yufei; Martin, Trevor; Mena, Jose; Mendoza, Rosa; Myhrvold, Cameron; Millian, Christian; Pfau, Sarah; Raj, Sandeep; Rich, Matt; Rokicki, Joe; Rounds, William; Salazar, Michael; Salesi, Matthew; Sharma, Rajani; Silverman, Sanford; Singer, Cara; Sinha, Sandhya; Staller, Max; Stern, Philip; Tang, Hanlin; Weeks, Sharon; Weidmann, Maxwell; Wolf, Ashley; Young, Carmen; Yuan, Jie; Crutchfield, Christopher; McClean, Megan; Murphy, Coleen T.; Llinás, Manuel; Botstein, David; Troyanskaya, Olga G.; Dunham, Maitreya J.

In: Genetics, Vol. 195, No. 1, 17.09.2013, p. 275-287.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A new system for comparative functional genomics of Saccharomyces yeasts

AU - Caudy, Amy A.

AU - Guan, Yuanfang

AU - Jia, Yue

AU - Hansen, Christina

AU - DeSevo, Chris

AU - Hayes, Alicia P.

AU - Agee, Joy

AU - Alvarez-Dominguez, Juan R.

AU - Arellano, Hugo

AU - Barrett, Daniel

AU - Bauerle, Cynthia

AU - Bisaria, Namita

AU - Bradley, Patrick H.

AU - Scott Breunig, J.

AU - Bush, Erin

AU - Cappel, David

AU - Capra, Emily

AU - Chen, Walter

AU - Clore, John

AU - Combs, Peter A.

AU - Doucette, Christopher

AU - Demuren, Olukunle

AU - Fellowes, Peter

AU - Freeman, Sam

AU - Frenkel, Evgeni

AU - Gadala-Maria, Daniel

AU - Gawande, Richa

AU - Glass, David

AU - Grossberg, Samuel

AU - Gupta, Anita

AU - Hammonds-Odie, Latanya

AU - Hoisos, Aaron

AU - Hsi, Jenny

AU - Hsu, Yu Han Huang

AU - Inukai, Sachi

AU - Karczewski, Konrad J.

AU - Ke, Xiaobo

AU - Kojima, Mina

AU - Leachman, Samuel

AU - Lieber, Danny

AU - Liebowitz, Anna

AU - Liu, Julia

AU - Liu, Yufei

AU - Martin, Trevor

AU - Mena, Jose

AU - Mendoza, Rosa

AU - Myhrvold, Cameron

AU - Millian, Christian

AU - Pfau, Sarah

AU - Raj, Sandeep

AU - Rich, Matt

AU - Rokicki, Joe

AU - Rounds, William

AU - Salazar, Michael

AU - Salesi, Matthew

AU - Sharma, Rajani

AU - Silverman, Sanford

AU - Singer, Cara

AU - Sinha, Sandhya

AU - Staller, Max

AU - Stern, Philip

AU - Tang, Hanlin

AU - Weeks, Sharon

AU - Weidmann, Maxwell

AU - Wolf, Ashley

AU - Young, Carmen

AU - Yuan, Jie

AU - Crutchfield, Christopher

AU - McClean, Megan

AU - Murphy, Coleen T.

AU - Llinás, Manuel

AU - Botstein, David

AU - Troyanskaya, Olga G.

AU - Dunham, Maitreya J.

PY - 2013/9/17

Y1 - 2013/9/17

N2 - Whole-genome sequencing, particularly in fungi, has progressed at a tremendous rate. More difficult, however, is experimental testing of the inferences about gene function that can be drawn from comparative sequence analysis alone. We present a genome-wide functional characterization of a sequenced but experimentally understudied budding yeast, Saccharomyces bayanus var. uvarum (henceforth referred to as S. bayanus), allowing us to map changes over the 20 million years that separate this organism from S. cerevisiae. We first created a suite of genetic tools to facilitate work in S. bayanus. Next, we measured the gene-expression response of S. bayanus to a diverse set of perturbations optimized using a computational approach to cover a diverse array of functionally relevant biological responses. The resulting data set reveals that gene-expression patterns are largely conserved, but significant changes may exist in regulatory networks such as carbohydrate utilization and meiosis. In addition to regulatory changes, our approach identified gene functions that have diverged. The functions of genes in core pathways are highly conserved, but we observed many changes in which genes are involved in osmotic stress, peroxisome biogenesis, and autophagy. A surprising number of genes specific to S. bayanus respond to oxidative stress, suggesting the organism may have evolved under different selection pressures than S. cerevisiae. This work expands the scope of genome-scale evolutionary studies from sequence-based analysis to rapid experimental characterization and could be adopted for functional mapping in any lineage of interest. Furthermore, our detailed characterization of S. bayanus provides a valuable resource for comparative functional genomics studies in yeast.

AB - Whole-genome sequencing, particularly in fungi, has progressed at a tremendous rate. More difficult, however, is experimental testing of the inferences about gene function that can be drawn from comparative sequence analysis alone. We present a genome-wide functional characterization of a sequenced but experimentally understudied budding yeast, Saccharomyces bayanus var. uvarum (henceforth referred to as S. bayanus), allowing us to map changes over the 20 million years that separate this organism from S. cerevisiae. We first created a suite of genetic tools to facilitate work in S. bayanus. Next, we measured the gene-expression response of S. bayanus to a diverse set of perturbations optimized using a computational approach to cover a diverse array of functionally relevant biological responses. The resulting data set reveals that gene-expression patterns are largely conserved, but significant changes may exist in regulatory networks such as carbohydrate utilization and meiosis. In addition to regulatory changes, our approach identified gene functions that have diverged. The functions of genes in core pathways are highly conserved, but we observed many changes in which genes are involved in osmotic stress, peroxisome biogenesis, and autophagy. A surprising number of genes specific to S. bayanus respond to oxidative stress, suggesting the organism may have evolved under different selection pressures than S. cerevisiae. This work expands the scope of genome-scale evolutionary studies from sequence-based analysis to rapid experimental characterization and could be adopted for functional mapping in any lineage of interest. Furthermore, our detailed characterization of S. bayanus provides a valuable resource for comparative functional genomics studies in yeast.

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Caudy AA, Guan Y, Jia Y, Hansen C, DeSevo C, Hayes AP et al. A new system for comparative functional genomics of Saccharomyces yeasts. Genetics. 2013 Sep 17;195(1):275-287. https://doi.org/10.1534/genetics.113.152918