The genomic and phenotypic diversity of Schizosaccharomyces pombe

Daniel C. Jeffares; Charalampos Rallis; Adrien Rieux; Doug Speed; Martin Převorovský; Tobias Mourier; Francesc X. Marsellach; Zamin Iqbal; Winston Lau; Tammy M.K. Cheng; Rodrigo Pracana; Michael Mülleder; Jonathan L.D. Lawson; Anatole Chessel; Sendu Bala; Garrett Hellenthal; Brendan O'Fallon; Thomas Keane; Jared T. Simpson; Leanne Bischof; Bartlomiej Tomiczek; Danny A. Bitton; Theodora Sideri; Sandra Codlin; Josephine E.E.U. Hellberg; Laurent Van Trigt; Linda Jeffery; Juan Juan Li; Sophie Atkinson; Malte Thodberg; Melanie Febrer; Kirsten McLay; Nizar Drou; William Brown; Jacqueline Hayles; Rafael E.Carazo Salas; Markus Ralser; Nikolas Maniatis; David J. Balding; Francois Balloux; Richard Durbin; Jürg Bähler

doi:10.1038/ng.3215

The genomic and phenotypic diversity of Schizosaccharomyces pombe

Daniel C. Jeffares^*, Charalampos Rallis, Adrien Rieux, Doug Speed, Martin Převorovský, Tobias Mourier, Francesc X. Marsellach, Zamin Iqbal, Winston Lau, Tammy M.K. Cheng, Rodrigo Pracana, Michael Mülleder, Jonathan L.D. Lawson, Anatole Chessel, Sendu Bala, Garrett Hellenthal, Brendan O'Fallon, Thomas Keane, Jared T. Simpson, Leanne BischofBartlomiej Tomiczek, Danny A. Bitton, Theodora Sideri, Sandra Codlin, Josephine E.E.U. Hellberg, Laurent Van Trigt, Linda Jeffery, Juan Juan Li, Sophie Atkinson, Malte Thodberg, Melanie Febrer, Kirsten McLay, Nizar Drou, William Brown, Jacqueline Hayles, Rafael E.Carazo Salas, Markus Ralser, Nikolas Maniatis, David J. Balding, Francois Balloux, Richard Durbin, Jürg Bähler

^*Corresponding author for this work

Biological, Environmental Sciences and Engineering

Research output: Contribution to journal › Article › peer-review

112 Scopus citations

Abstract

Natural variation within species reveals aspects of genome evolution and function. The fission yeast Schizosaccharomyces pombe is an important model for eukaryotic biology, but researchers typically use one standard laboratory strain. To extend the usefulness of this model, we surveyed the genomic and phenotypic variation in 161 natural isolates. We sequenced the genomes of all strains, finding moderate genetic diversity (π = 3 × 10 ^-3 substitutions/site) and weak global population structure. We estimate that dispersal of S. pombe began during human antiquity (∼340 BCE), and ancestors of these strains reached the Americas at ∼1623 CE. We quantified 74 traits, finding substantial heritable phenotypic diversity. We conducted 223 genome-wide association studies, with 89 traits showing at least one association. The most significant variant for each trait explained 22% of the phenotypic variance on average, with indels having larger effects than SNPs. This analysis represents a rich resource to examine genotype-phenotype relationships in a tractable model.

Original language	English (US)
Pages (from-to)	235-241
Number of pages	7
Journal	Nature Genetics
Volume	47
Issue number	3
DOIs	https://doi.org/10.1038/ng.3215
State	Published - Feb 25 2015

Bibliographical note

Funding Information:
We thank L. Clissold, H. Musk, D. Baker and R. Davey for their contributions to sequencing, H. Levin for discussions about transposons, and J. Mata and S. Marguerat for comments on the manuscript. This work was supported by a Wellcome Trust Senior Investigator Award to J.B. (grant 095598/Z/11/Z), by the Wellcome Trust to S.B., T.K., J.T.S. and R.D., by grant 260801-BIG-IDEA from the European Research Council (ERC) and grant BB/H005854/1 from the Biotechnology and Biological Sciences Research Council (BBSRC) to A.R. and F.B., by UK Medical Research Council grant G0901388 to D.S. and D.J.B., by a Cancer Research UK Postdoctoral Fellowship to T.M.K.C., by an ERC Starting Grant (SYSGRO) to R.E.C.S., a Wellcome Trust PhD studentship to J.L.D.L. and BBSRC grant BB/K006320/1 to R.E.C.S. and A.C., by a Wellcome Trust grant (RG 093735/Z/10/Z) and ERC Starting Grant 260809 to M.R. (M.R. is a Wellcome Trust Research Career Development and Wellcome-Beit Prize Fellow), by Czech Science Foundation grant P305/12/P040 and Charles University grant UNCE 204013 to M.P. and by Cancer Research UK to L.J. and J.H.

Publisher Copyright:
© 2015 Nature America, Inc. All rights reserved.

ASJC Scopus subject areas

Genetics

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10.1038/ng.3215

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Jeffares, D. C., Rallis, C., Rieux, A., Speed, D., Převorovský, M., Mourier, T., Marsellach, F. X., Iqbal, Z., Lau, W., Cheng, T. M. K., Pracana, R., Mülleder, M., Lawson, J. L. D., Chessel, A., Bala, S., Hellenthal, G., O'Fallon, B., Keane, T., Simpson, J. T., ... Bähler, J. (2015). The genomic and phenotypic diversity of Schizosaccharomyces pombe. Nature Genetics, 47(3), 235-241. https://doi.org/10.1038/ng.3215

@article{ab1ae773932745ecaf68e692f57e6333,

title = "The genomic and phenotypic diversity of Schizosaccharomyces pombe",

abstract = "Natural variation within species reveals aspects of genome evolution and function. The fission yeast Schizosaccharomyces pombe is an important model for eukaryotic biology, but researchers typically use one standard laboratory strain. To extend the usefulness of this model, we surveyed the genomic and phenotypic variation in 161 natural isolates. We sequenced the genomes of all strains, finding moderate genetic diversity (π = 3 × 10 -3 substitutions/site) and weak global population structure. We estimate that dispersal of S. pombe began during human antiquity (∼340 BCE), and ancestors of these strains reached the Americas at ∼1623 CE. We quantified 74 traits, finding substantial heritable phenotypic diversity. We conducted 223 genome-wide association studies, with 89 traits showing at least one association. The most significant variant for each trait explained 22% of the phenotypic variance on average, with indels having larger effects than SNPs. This analysis represents a rich resource to examine genotype-phenotype relationships in a tractable model.",

author = "Jeffares, {Daniel C.} and Charalampos Rallis and Adrien Rieux and Doug Speed and Martin P{\v r}evorovsk{\'y} and Tobias Mourier and Marsellach, {Francesc X.} and Zamin Iqbal and Winston Lau and Cheng, {Tammy M.K.} and Rodrigo Pracana and Michael M{\"u}lleder and Lawson, {Jonathan L.D.} and Anatole Chessel and Sendu Bala and Garrett Hellenthal and Brendan O'Fallon and Thomas Keane and Simpson, {Jared T.} and Leanne Bischof and Bartlomiej Tomiczek and Bitton, {Danny A.} and Theodora Sideri and Sandra Codlin and Hellberg, {Josephine E.E.U.} and {Van Trigt}, Laurent and Linda Jeffery and Li, {Juan Juan} and Sophie Atkinson and Malte Thodberg and Melanie Febrer and Kirsten McLay and Nizar Drou and William Brown and Jacqueline Hayles and Salas, {Rafael E.Carazo} and Markus Ralser and Nikolas Maniatis and Balding, {David J.} and Francois Balloux and Richard Durbin and J{\"u}rg B{\"a}hler",

note = "Funding Information: We thank L. Clissold, H. Musk, D. Baker and R. Davey for their contributions to sequencing, H. Levin for discussions about transposons, and J. Mata and S. Marguerat for comments on the manuscript. This work was supported by a Wellcome Trust Senior Investigator Award to J.B. (grant 095598/Z/11/Z), by the Wellcome Trust to S.B., T.K., J.T.S. and R.D., by grant 260801-BIG-IDEA from the European Research Council (ERC) and grant BB/H005854/1 from the Biotechnology and Biological Sciences Research Council (BBSRC) to A.R. and F.B., by UK Medical Research Council grant G0901388 to D.S. and D.J.B., by a Cancer Research UK Postdoctoral Fellowship to T.M.K.C., by an ERC Starting Grant (SYSGRO) to R.E.C.S., a Wellcome Trust PhD studentship to J.L.D.L. and BBSRC grant BB/K006320/1 to R.E.C.S. and A.C., by a Wellcome Trust grant (RG 093735/Z/10/Z) and ERC Starting Grant 260809 to M.R. (M.R. is a Wellcome Trust Research Career Development and Wellcome-Beit Prize Fellow), by Czech Science Foundation grant P305/12/P040 and Charles University grant UNCE 204013 to M.P. and by Cancer Research UK to L.J. and J.H. Publisher Copyright: {\textcopyright} 2015 Nature America, Inc. All rights reserved.",

year = "2015",

month = feb,

day = "25",

doi = "10.1038/ng.3215",

language = "English (US)",

volume = "47",

pages = "235--241",

journal = "Nature Genetics",

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Jeffares, DC, Rallis, C, Rieux, A, Speed, D, Převorovský, M, Mourier, T, Marsellach, FX, Iqbal, Z, Lau, W, Cheng, TMK, Pracana, R, Mülleder, M, Lawson, JLD, Chessel, A, Bala, S, Hellenthal, G, O'Fallon, B, Keane, T, Simpson, JT, Bischof, L, Tomiczek, B, Bitton, DA, Sideri, T, Codlin, S, Hellberg, JEEU, Van Trigt, L, Jeffery, L, Li, JJ, Atkinson, S, Thodberg, M, Febrer, M, McLay, K, Drou, N, Brown, W, Hayles, J, Salas, REC, Ralser, M, Maniatis, N, Balding, DJ, Balloux, F, Durbin, R & Bähler, J 2015, 'The genomic and phenotypic diversity of Schizosaccharomyces pombe', Nature Genetics, vol. 47, no. 3, pp. 235-241. https://doi.org/10.1038/ng.3215

TY - JOUR

T1 - The genomic and phenotypic diversity of Schizosaccharomyces pombe

AU - Jeffares, Daniel C.

AU - Rallis, Charalampos

AU - Rieux, Adrien

AU - Speed, Doug

AU - Převorovský, Martin

AU - Mourier, Tobias

AU - Marsellach, Francesc X.

AU - Iqbal, Zamin

AU - Lau, Winston

AU - Cheng, Tammy M.K.

AU - Pracana, Rodrigo

AU - Mülleder, Michael

AU - Lawson, Jonathan L.D.

AU - Chessel, Anatole

AU - Bala, Sendu

AU - Hellenthal, Garrett

AU - O'Fallon, Brendan

AU - Keane, Thomas

AU - Simpson, Jared T.

AU - Bischof, Leanne

AU - Tomiczek, Bartlomiej

AU - Bitton, Danny A.

AU - Sideri, Theodora

AU - Codlin, Sandra

AU - Hellberg, Josephine E.E.U.

AU - Van Trigt, Laurent

AU - Jeffery, Linda

AU - Li, Juan Juan

AU - Atkinson, Sophie

AU - Thodberg, Malte

AU - Febrer, Melanie

AU - McLay, Kirsten

AU - Drou, Nizar

AU - Brown, William

AU - Hayles, Jacqueline

AU - Salas, Rafael E.Carazo

AU - Ralser, Markus

AU - Maniatis, Nikolas

AU - Balding, David J.

AU - Balloux, Francois

AU - Durbin, Richard

AU - Bähler, Jürg

N1 - Funding Information: We thank L. Clissold, H. Musk, D. Baker and R. Davey for their contributions to sequencing, H. Levin for discussions about transposons, and J. Mata and S. Marguerat for comments on the manuscript. This work was supported by a Wellcome Trust Senior Investigator Award to J.B. (grant 095598/Z/11/Z), by the Wellcome Trust to S.B., T.K., J.T.S. and R.D., by grant 260801-BIG-IDEA from the European Research Council (ERC) and grant BB/H005854/1 from the Biotechnology and Biological Sciences Research Council (BBSRC) to A.R. and F.B., by UK Medical Research Council grant G0901388 to D.S. and D.J.B., by a Cancer Research UK Postdoctoral Fellowship to T.M.K.C., by an ERC Starting Grant (SYSGRO) to R.E.C.S., a Wellcome Trust PhD studentship to J.L.D.L. and BBSRC grant BB/K006320/1 to R.E.C.S. and A.C., by a Wellcome Trust grant (RG 093735/Z/10/Z) and ERC Starting Grant 260809 to M.R. (M.R. is a Wellcome Trust Research Career Development and Wellcome-Beit Prize Fellow), by Czech Science Foundation grant P305/12/P040 and Charles University grant UNCE 204013 to M.P. and by Cancer Research UK to L.J. and J.H. Publisher Copyright: © 2015 Nature America, Inc. All rights reserved.

PY - 2015/2/25

Y1 - 2015/2/25

N2 - Natural variation within species reveals aspects of genome evolution and function. The fission yeast Schizosaccharomyces pombe is an important model for eukaryotic biology, but researchers typically use one standard laboratory strain. To extend the usefulness of this model, we surveyed the genomic and phenotypic variation in 161 natural isolates. We sequenced the genomes of all strains, finding moderate genetic diversity (π = 3 × 10 -3 substitutions/site) and weak global population structure. We estimate that dispersal of S. pombe began during human antiquity (∼340 BCE), and ancestors of these strains reached the Americas at ∼1623 CE. We quantified 74 traits, finding substantial heritable phenotypic diversity. We conducted 223 genome-wide association studies, with 89 traits showing at least one association. The most significant variant for each trait explained 22% of the phenotypic variance on average, with indels having larger effects than SNPs. This analysis represents a rich resource to examine genotype-phenotype relationships in a tractable model.

AB - Natural variation within species reveals aspects of genome evolution and function. The fission yeast Schizosaccharomyces pombe is an important model for eukaryotic biology, but researchers typically use one standard laboratory strain. To extend the usefulness of this model, we surveyed the genomic and phenotypic variation in 161 natural isolates. We sequenced the genomes of all strains, finding moderate genetic diversity (π = 3 × 10 -3 substitutions/site) and weak global population structure. We estimate that dispersal of S. pombe began during human antiquity (∼340 BCE), and ancestors of these strains reached the Americas at ∼1623 CE. We quantified 74 traits, finding substantial heritable phenotypic diversity. We conducted 223 genome-wide association studies, with 89 traits showing at least one association. The most significant variant for each trait explained 22% of the phenotypic variance on average, with indels having larger effects than SNPs. This analysis represents a rich resource to examine genotype-phenotype relationships in a tractable model.

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JO - Nature Genetics

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The genomic and phenotypic diversity of Schizosaccharomyces pombe

Abstract

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