Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure

Sean P. Gordon; Bruno Contreras-Moreira; Daniel P. Woods; David L. Des Marais; Diane Burgess; Shengqiang Shu; Christoph Stritt; Anne C. Roulin; Wendy Schackwitz; Ludmila Tyler; Joel Martin; Anna Lipzen; Niklas Dochy; Jeremy Phillips; Kerrie Barry; Koen Geuten; Hikmet Budak; Thomas E. Juenger; Richard Amasino; Ana L. Caicedo; David Goodstein; Patrick Davidson; Luis A.J. Mur; Melania Figueroa; Michael Freeling; Pilar Catalan; John P. Vogel

doi:10.1038/s41467-017-02292-8

Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure

Sean P. Gordon
, Bruno Contreras-Moreira
, Daniel P. Woods
, David L. Des Marais
, Diane Burgess
, Shengqiang Shu
, Christoph Stritt
, Anne C. Roulin
, Wendy Schackwitz
, Ludmila Tyler
, Joel Martin
, Anna Lipzen
, Niklas Dochy
, Jeremy Phillips
, Kerrie Barry
, Koen Geuten
, Hikmet Budak
, Thomas E. Juenger
, Richard Amasino
, Ana L. Caicedo

David Goodstein, Patrick Davidson, Luis A.J. Mur, Melania Figueroa, Michael Freeling, Pilar Catalan, John P. Vogel

Plant Pathology

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

284 Scopus citations

Abstract

While prokaryotic pan-genomes have been shown to contain many more genes than any individual organism, the prevalence and functional significance of differentially present genes in eukaryotes remains poorly understood. Whole-genome de novo assembly and annotation of 54 lines of the grass Brachypodium distachyon yield a pan-genome containing nearly twice the number of genes found in any individual genome. Genes present in all lines are enriched for essential biological functions, while genes present in only some lines are enriched for conditionally beneficial functions (e.g., defense and development), display faster evolutionary rates, lie closer to transposable elements and are less likely to be syntenic with orthologous genes in other grasses. Our data suggest that differentially present genes contribute substantially to phenotypic variation within a eukaryote species, these genes have a major influence in population genetics, and transposable elements play a key role in pan-genome evolution.

Original language	English (US)
Article number	2184
Journal	Nature communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-02292-8
State	Published - Dec 1 2017

Bibliographical note

Funding Information:
IOS–1258126), and the Great Lakes Bioenergy Research Center (Department of Energy Biological and Environmental Research Office of Science grant no. DE– FCO2–07ER64494). TEJ and DLDM were supported by NSF PGRP grant IOS-0922457. We thank Jason Stajich for advice on dN/dS software. P.C. and B.C.M. were funded by Spanish MINECO (CGL2012-39953-C02-01 and CGL2016-79790-P). B.C.M. was partially funded by DGA—Obra Social La Caixa (grant number GA-LC-059-2011) and Spanish MINECO (AGL2013-48756-R, CSIC13-4E-2490). PC was partially funded by Spanish Aragon Government-European Social Fund (Bioflora). BCM and PC thankfully acknowledge the resources from the supercomputer "Memento" and assistance provided by BIFI-ZCAM. M.F. acknowledges the University of Minnesota Experimental Station USDA-NIFA Hatch/Figueroa project MIN-22-058.

Funding Information:
The work conducted by the US DOE Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231. D.P. W. and R.A. were funded in part by the National Science Foundation (grant no.

Publisher Copyright:
© 2017 The Author(s).

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Gordon, S. P., Contreras-Moreira, B., Woods, D. P., Des Marais, D. L., Burgess, D., Shu, S., Stritt, C., Roulin, A. C., Schackwitz, W., Tyler, L., Martin, J., Lipzen, A., Dochy, N., Phillips, J., Barry, K., Geuten, K., Budak, H., Juenger, T. E., Amasino, R., ... Vogel, J. P. (2017). Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. Nature communications, 8(1), Article 2184. https://doi.org/10.1038/s41467-017-02292-8

Gordon, SP, Contreras-Moreira, B, Woods, DP, Des Marais, DL, Burgess, D, Shu, S, Stritt, C, Roulin, AC, Schackwitz, W, Tyler, L, Martin, J, Lipzen, A, Dochy, N, Phillips, J, Barry, K, Geuten, K, Budak, H, Juenger, TE, Amasino, R, Caicedo, AL, Goodstein, D, Davidson, P, Mur, LAJ, Figueroa, M, Freeling, M, Catalan, P & Vogel, JP 2017, 'Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure', Nature communications, vol. 8, no. 1, 2184. https://doi.org/10.1038/s41467-017-02292-8

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title = "Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure",

abstract = "While prokaryotic pan-genomes have been shown to contain many more genes than any individual organism, the prevalence and functional significance of differentially present genes in eukaryotes remains poorly understood. Whole-genome de novo assembly and annotation of 54 lines of the grass Brachypodium distachyon yield a pan-genome containing nearly twice the number of genes found in any individual genome. Genes present in all lines are enriched for essential biological functions, while genes present in only some lines are enriched for conditionally beneficial functions (e.g., defense and development), display faster evolutionary rates, lie closer to transposable elements and are less likely to be syntenic with orthologous genes in other grasses. Our data suggest that differentially present genes contribute substantially to phenotypic variation within a eukaryote species, these genes have a major influence in population genetics, and transposable elements play a key role in pan-genome evolution.",

author = "Gordon, \{Sean P.\} and Bruno Contreras-Moreira and Woods, \{Daniel P.\} and \{Des Marais\}, \{David L.\} and Diane Burgess and Shengqiang Shu and Christoph Stritt and Roulin, \{Anne C.\} and Wendy Schackwitz and Ludmila Tyler and Joel Martin and Anna Lipzen and Niklas Dochy and Jeremy Phillips and Kerrie Barry and Koen Geuten and Hikmet Budak and Juenger, \{Thomas E.\} and Richard Amasino and Caicedo, \{Ana L.\} and David Goodstein and Patrick Davidson and Mur, \{Luis A.J.\} and Melania Figueroa and Michael Freeling and Pilar Catalan and Vogel, \{John P.\}",

note = "Funding Information: IOS–1258126), and the Great Lakes Bioenergy Research Center (Department of Energy Biological and Environmental Research Office of Science grant no. DE– FCO2–07ER64494). TEJ and DLDM were supported by NSF PGRP grant IOS-0922457. We thank Jason Stajich for advice on dN/dS software. P.C. and B.C.M. were funded by Spanish MINECO (CGL2012-39953-C02-01 and CGL2016-79790-P). B.C.M. was partially funded by DGA—Obra Social La Caixa (grant number GA-LC-059-2011) and Spanish MINECO (AGL2013-48756-R, CSIC13-4E-2490). PC was partially funded by Spanish Aragon Government-European Social Fund (Bioflora). BCM and PC thankfully acknowledge the resources from the supercomputer {"}Memento{"} and assistance provided by BIFI-ZCAM. M.F. acknowledges the University of Minnesota Experimental Station USDA-NIFA Hatch/Figueroa project MIN-22-058. Funding Information: The work conducted by the US DOE Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231. D.P. W. and R.A. were funded in part by the National Science Foundation (grant no. Publisher Copyright: {\textcopyright} 2017 The Author(s).",

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doi = "10.1038/s41467-017-02292-8",

language = "English (US)",

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T1 - Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure

AU - Gordon, Sean P.

AU - Contreras-Moreira, Bruno

AU - Woods, Daniel P.

AU - Des Marais, David L.

AU - Burgess, Diane

AU - Shu, Shengqiang

AU - Stritt, Christoph

AU - Roulin, Anne C.

AU - Schackwitz, Wendy

AU - Tyler, Ludmila

AU - Martin, Joel

AU - Lipzen, Anna

AU - Dochy, Niklas

AU - Phillips, Jeremy

AU - Barry, Kerrie

AU - Geuten, Koen

AU - Budak, Hikmet

AU - Juenger, Thomas E.

AU - Amasino, Richard

AU - Caicedo, Ana L.

AU - Goodstein, David

AU - Davidson, Patrick

AU - Mur, Luis A.J.

AU - Figueroa, Melania

AU - Freeling, Michael

AU - Catalan, Pilar

AU - Vogel, John P.

N1 - Funding Information: IOS–1258126), and the Great Lakes Bioenergy Research Center (Department of Energy Biological and Environmental Research Office of Science grant no. DE– FCO2–07ER64494). TEJ and DLDM were supported by NSF PGRP grant IOS-0922457. We thank Jason Stajich for advice on dN/dS software. P.C. and B.C.M. were funded by Spanish MINECO (CGL2012-39953-C02-01 and CGL2016-79790-P). B.C.M. was partially funded by DGA—Obra Social La Caixa (grant number GA-LC-059-2011) and Spanish MINECO (AGL2013-48756-R, CSIC13-4E-2490). PC was partially funded by Spanish Aragon Government-European Social Fund (Bioflora). BCM and PC thankfully acknowledge the resources from the supercomputer "Memento" and assistance provided by BIFI-ZCAM. M.F. acknowledges the University of Minnesota Experimental Station USDA-NIFA Hatch/Figueroa project MIN-22-058. Funding Information: The work conducted by the US DOE Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract no. DE-AC02-05CH11231. D.P. W. and R.A. were funded in part by the National Science Foundation (grant no. Publisher Copyright: © 2017 The Author(s).

PY - 2017/12/1

Y1 - 2017/12/1

N2 - While prokaryotic pan-genomes have been shown to contain many more genes than any individual organism, the prevalence and functional significance of differentially present genes in eukaryotes remains poorly understood. Whole-genome de novo assembly and annotation of 54 lines of the grass Brachypodium distachyon yield a pan-genome containing nearly twice the number of genes found in any individual genome. Genes present in all lines are enriched for essential biological functions, while genes present in only some lines are enriched for conditionally beneficial functions (e.g., defense and development), display faster evolutionary rates, lie closer to transposable elements and are less likely to be syntenic with orthologous genes in other grasses. Our data suggest that differentially present genes contribute substantially to phenotypic variation within a eukaryote species, these genes have a major influence in population genetics, and transposable elements play a key role in pan-genome evolution.

AB - While prokaryotic pan-genomes have been shown to contain many more genes than any individual organism, the prevalence and functional significance of differentially present genes in eukaryotes remains poorly understood. Whole-genome de novo assembly and annotation of 54 lines of the grass Brachypodium distachyon yield a pan-genome containing nearly twice the number of genes found in any individual genome. Genes present in all lines are enriched for essential biological functions, while genes present in only some lines are enriched for conditionally beneficial functions (e.g., defense and development), display faster evolutionary rates, lie closer to transposable elements and are less likely to be syntenic with orthologous genes in other grasses. Our data suggest that differentially present genes contribute substantially to phenotypic variation within a eukaryote species, these genes have a major influence in population genetics, and transposable elements play a key role in pan-genome evolution.

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Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure

Abstract

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