Comparative Functional Genomics of the Fission Yeasts

Nicholas Rhind; Zehua Chen; Moran Yassour; Dawn A. Thompson; Brian J. Haas; Naomi Habib; Ilan Wapinski; Sushmita Roy; Michael F. Lin; David I. Heiman; Sarah K. Young; Kanji Furuya; Yabin Guo; Alison Pidoux; Huei Mei Chen; Barbara Robbertse; Jonathan M. Goldberg; Keita Aoki; Elizabeth H. Bayne; Aaron M. Berlin; Christopher A. Desjardins; Edward Dobbs; Livio Dukaj; Lin Fan; Michael G. FitzGerald; Courtney French; Sharvari Gujja; Klavs Hansen; Dan Keifenheim; Joshua Z. Levin; Rebecca A. Mosher; Carolin A. Müller; Jenna Pfiffner; Margaret Priest; Carsten Russ; Agata Smialowska; Peter Swoboda; Sean M. Sykes; Matthew Vaughn; Sonya Vengrova; Ryan Yoder; Qiandong Zeng; Robin Allshire; David Baulcombe; Bruce W. Birren; William Brown; Karl Ekwall; Manolis Kellis; Janet Leatherwood; Henry Levin; Hanah Margalit; Rob Martienssen; Conrad A. Nieduszynski; Joseph W. Spatafora; Nir Friedman; Jacob Z. Dalgaard; Peter Baumann; Hironori Niki; Aviv Regev; Chad Nusbaum

doi:10.1126/science.1203357

Research Article

Comparative Functional Genomics of the Fission Yeasts

Nicholas Rhind¹,^¶,
Zehua Chen²,
Moran Yassour³,⁴,⁵,∥,
Dawn A. Thompson³,∥,
Brian J. Haas²,∥,
Naomi Habib⁵,⁶,∥,
Ilan Wapinski³,⁷,∥,
Sushmita Roy³,⁸,∥,
Michael F. Lin⁸,
David I. Heiman²,
Sarah K. Young²,
Kanji Furuya⁹,
Yabin Guo¹⁰,
Alison Pidoux¹¹,
Huei Mei Chen¹²,
Barbara Robbertse¹³,*,
Jonathan M. Goldberg²,
Keita Aoki⁹,
Elizabeth H. Bayne¹¹,†,
Aaron M. Berlin²,
Christopher A. Desjardins²,
Edward Dobbs¹¹,
Livio Dukaj¹,
Lin Fan²,
Michael G. FitzGerald²,
Courtney French⁶,
Sharvari Gujja²,
Klavs Hansen¹⁴,‡,
Dan Keifenheim¹,
Joshua Z. Levin²,
Rebecca A. Mosher¹⁵,§,
Carolin A. Müller¹⁶,
Jenna Pfiffner²,
Margaret Priest²,
Carsten Russ²,
Agata Smialowska¹⁷,¹⁸,
Peter Swoboda¹⁷,
Sean M. Sykes²,
Matthew Vaughn¹⁴,
Sonya Vengrova¹⁹,
Ryan Yoder¹³,
Qiandong Zeng²,
Robin Allshire¹¹,
David Baulcombe¹⁵,
Bruce W. Birren²⁰,
William Brown¹⁶,
Karl Ekwall¹⁷,¹⁸,
Manolis Kellis⁸,³,
Janet Leatherwood¹²,
Henry Levin¹⁰,
Hanah Margalit⁶,
Rob Martienssen¹⁴,
Conrad A. Nieduszynski¹⁶,
Joseph W. Spatafora¹³,
Nir Friedman⁵,²¹,
Jacob Z. Dalgaard¹⁹,
Peter Baumann²²,²³,²⁴,
Hironori Niki⁹,
Aviv Regev³,⁴,²⁴,^¶,
Chad Nusbaum²,^¶

¹Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, 364 Plantation Street, Worcester, MA 01605, USA.
²Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.
³Broad Institute of Massachusetts Institute of Technology and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.
⁴Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.
⁵School of Computer Science and Engineering, Hebrew University, Jerusalem 91904, Israel.
⁶Department of Microbiology and Molecular Genetics, Faculty of Medicine, Hebrew University, Jerusalem 91120, Israel.
⁷Department of Systems Biology, Harvard Medical School, 200 Longwood Avenue, Alpert 536, Boston, MA 02115, USA.
⁸Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street 32-D510, Cambridge, MA 02139, USA.
⁹Microbial Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.
¹⁰Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA.
¹¹Wellcome Trust Centre for Cell Biology, Institute of Cell Biology, School of Biological Sciences, The University of Edinburgh, 6.34 Swann Building, Mayfield Road, Edinburgh EH9 3JR, UK.
¹²Department of Molecular Genetics and Microbiology, Life Science, Room 130, State University of New York, Stony Brook, NY 11794, USA.
¹³Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA.
¹⁴Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USA.
¹⁵Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK.
¹⁶Centre for Genetics and Genomics, University of Nottingham, Queen's Medical Centre, Nottingham NG7 2UH, UK.
¹⁷Center for Biosciences, Department of Biosciences and Nutrition, Karolinska Institute, 141 38 Huddinge, Sweden.
¹⁸Department of Life Sciences, Södertörns Högskola, 141 89 Huddinge, Sweden.
¹⁹Warwick Medical School, University of Warwick, Gibbet Hill Campus, Coventry CV4 7AL, UK.
²⁰Broad Institute of Massachusetts Institute of Technology and Harvard, 301 Binney Street, Cambridge, MA 02141, USA.
²¹Alexander Silberman Institute of Life Sciences, Hebrew University, Jerusalem 91904, Israel.
²²Stowers Institute for Medical Research, Kansas City, MO 64110, USA.
²³Department of Molecular and Integrative Physiology, University of Kansas Medical School, Kansas City, KS 66160, USA.
²⁴Howard Hughes Medical Institute.

↵¶To whom correspondence should be addressed. E-mail: nick.rhind{at}umassmed.edu (N.R.); aregev{at}broad.mit.edu (A.R.); chad{at}broadinstitute.org (C.N.)

↵* Present address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Department of Health and Human Services, 45 Center Drive, Bethesda, MD, 20892, USA.
↵† Present address: Wellcome Trust Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, Dundee DD1 5EH, Scotland, UK.
↵‡ Present address: Evolva Biotech A/S, Bülowsvej 25, 1870 Frederiksberg C, Denmark.
↵§ Present address: The University of Arizona, The School of Plant Sciences, 303 Forbes Building, 1140 East South Campus Drive, Tucson, AZ 87421, USA.

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Science 20 May 2011:
Vol. 332, Issue 6032, pp. 930-936
DOI: 10.1126/science.1203357

Nicholas Rhind

1Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, 364 Plantation Street, Worcester, MA 01605, USA.

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For correspondence: nick.rhind@umassmed.edu aregev@broad.mit.edu chad@broadinstitute.org

Zehua Chen

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Moran Yassour

3Broad Institute of Massachusetts Institute of Technology and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.

4Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.

5School of Computer Science and Engineering, Hebrew University, Jerusalem 91904, Israel.

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Dawn A. Thompson

3Broad Institute of Massachusetts Institute of Technology and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.

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Brian J. Haas

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Naomi Habib

5School of Computer Science and Engineering, Hebrew University, Jerusalem 91904, Israel.

6Department of Microbiology and Molecular Genetics, Faculty of Medicine, Hebrew University, Jerusalem 91120, Israel.

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Ilan Wapinski

3Broad Institute of Massachusetts Institute of Technology and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.

7Department of Systems Biology, Harvard Medical School, 200 Longwood Avenue, Alpert 536, Boston, MA 02115, USA.

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Sushmita Roy

3Broad Institute of Massachusetts Institute of Technology and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.

8Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street 32-D510, Cambridge, MA 02139, USA.

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Michael F. Lin

8Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street 32-D510, Cambridge, MA 02139, USA.

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David I. Heiman

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Sarah K. Young

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Kanji Furuya

9Microbial Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.

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Yabin Guo

10Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA.

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Alison Pidoux

11Wellcome Trust Centre for Cell Biology, Institute of Cell Biology, School of Biological Sciences, The University of Edinburgh, 6.34 Swann Building, Mayfield Road, Edinburgh EH9 3JR, UK.

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Huei Mei Chen

12Department of Molecular Genetics and Microbiology, Life Science, Room 130, State University of New York, Stony Brook, NY 11794, USA.

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Barbara Robbertse

13Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA.

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Jonathan M. Goldberg

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Keita Aoki

9Microbial Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.

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Elizabeth H. Bayne

11Wellcome Trust Centre for Cell Biology, Institute of Cell Biology, School of Biological Sciences, The University of Edinburgh, 6.34 Swann Building, Mayfield Road, Edinburgh EH9 3JR, UK.

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Aaron M. Berlin

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Christopher A. Desjardins

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Edward Dobbs

11Wellcome Trust Centre for Cell Biology, Institute of Cell Biology, School of Biological Sciences, The University of Edinburgh, 6.34 Swann Building, Mayfield Road, Edinburgh EH9 3JR, UK.

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Livio Dukaj

1Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, 364 Plantation Street, Worcester, MA 01605, USA.

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Lin Fan

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Michael G. FitzGerald

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Courtney French

6Department of Microbiology and Molecular Genetics, Faculty of Medicine, Hebrew University, Jerusalem 91120, Israel.

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Sharvari Gujja

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Klavs Hansen

14Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USA.

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Dan Keifenheim

1Biochemistry and Molecular Pharmacology, University of Massachusetts Medical School, 364 Plantation Street, Worcester, MA 01605, USA.

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Joshua Z. Levin

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Rebecca A. Mosher

15Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK.

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Carolin A. Müller

16Centre for Genetics and Genomics, University of Nottingham, Queen's Medical Centre, Nottingham NG7 2UH, UK.

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Jenna Pfiffner

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Margaret Priest

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Carsten Russ

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Agata Smialowska

17Center for Biosciences, Department of Biosciences and Nutrition, Karolinska Institute, 141 38 Huddinge, Sweden.

18Department of Life Sciences, Södertörns Högskola, 141 89 Huddinge, Sweden.

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Peter Swoboda

17Center for Biosciences, Department of Biosciences and Nutrition, Karolinska Institute, 141 38 Huddinge, Sweden.

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Sean M. Sykes

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Matthew Vaughn

14Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USA.

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Sonya Vengrova

19Warwick Medical School, University of Warwick, Gibbet Hill Campus, Coventry CV4 7AL, UK.

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Ryan Yoder

13Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA.

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Qiandong Zeng

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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Robin Allshire

11Wellcome Trust Centre for Cell Biology, Institute of Cell Biology, School of Biological Sciences, The University of Edinburgh, 6.34 Swann Building, Mayfield Road, Edinburgh EH9 3JR, UK.

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David Baulcombe

15Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK.

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Bruce W. Birren

20Broad Institute of Massachusetts Institute of Technology and Harvard, 301 Binney Street, Cambridge, MA 02141, USA.

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William Brown

16Centre for Genetics and Genomics, University of Nottingham, Queen's Medical Centre, Nottingham NG7 2UH, UK.

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Karl Ekwall

17Center for Biosciences, Department of Biosciences and Nutrition, Karolinska Institute, 141 38 Huddinge, Sweden.

18Department of Life Sciences, Södertörns Högskola, 141 89 Huddinge, Sweden.

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Manolis Kellis

8Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, 32 Vassar Street 32-D510, Cambridge, MA 02139, USA.

3Broad Institute of Massachusetts Institute of Technology and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.

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Janet Leatherwood

12Department of Molecular Genetics and Microbiology, Life Science, Room 130, State University of New York, Stony Brook, NY 11794, USA.

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Henry Levin

10Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892, USA.

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Hanah Margalit

6Department of Microbiology and Molecular Genetics, Faculty of Medicine, Hebrew University, Jerusalem 91120, Israel.

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Rob Martienssen

14Cold Spring Harbor Laboratory, 1 Bungtown Road, Cold Spring Harbor, NY 11724, USA.

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Conrad A. Nieduszynski

16Centre for Genetics and Genomics, University of Nottingham, Queen's Medical Centre, Nottingham NG7 2UH, UK.

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Joseph W. Spatafora

13Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA.

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Nir Friedman

5School of Computer Science and Engineering, Hebrew University, Jerusalem 91904, Israel.

21Alexander Silberman Institute of Life Sciences, Hebrew University, Jerusalem 91904, Israel.

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Jacob Z. Dalgaard

19Warwick Medical School, University of Warwick, Gibbet Hill Campus, Coventry CV4 7AL, UK.

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Peter Baumann

22Stowers Institute for Medical Research, Kansas City, MO 64110, USA.

23Department of Molecular and Integrative Physiology, University of Kansas Medical School, Kansas City, KS 66160, USA.

24Howard Hughes Medical Institute.

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Hironori Niki

9Microbial Genetics Laboratory, Genetic Strains Research Center, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan.

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Aviv Regev

3Broad Institute of Massachusetts Institute of Technology and Harvard, 7 Cambridge Center, Cambridge, MA 02142, USA.

4Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA.

24Howard Hughes Medical Institute.

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For correspondence: nick.rhind@umassmed.edu aregev@broad.mit.edu chad@broadinstitute.org

Chad Nusbaum

2Broad Institute of Massachusetts Institute of Technology and Harvard, 320 Charles Street, Cambridge, MA 02141, USA.

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For correspondence: nick.rhind@umassmed.edu aregev@broad.mit.edu chad@broadinstitute.org

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Abstract

The fission yeast clade—comprising Schizosaccharomyces pombe, S. octosporus, S. cryophilus, and S. japonicus—occupies the basal branch of Ascomycete fungi and is an important model of eukaryote biology. A comparative annotation of these genomes identified a near extinction of transposons and the associated innovation of transposon-free centromeres. Expression analysis established that meiotic genes are subject to antisense transcription during vegetative growth, which suggests a mechanism for their tight regulation. In addition, trans-acting regulators control new genes within the context of expanded functional modules for meiosis and stress response. Differences in gene content and regulation also explain why, unlike the budding yeast of Saccharomycotina, fission yeasts cannot use ethanol as a primary carbon source. These analyses elucidate the genome structure and gene regulation of fission yeast and provide tools for investigation across the Schizosaccharomyces clade.

↵∥ These authors made equivalent contributions.

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Comparative Functional Genomics of the Fission Yeasts

Abstract

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