skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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.

Authors:
 [1]; ORCiD logo [2];  [3]; ORCiD logo [4];  [5];  [1];  [6];  [6];  [1];  [7]; ORCiD logo [1];  [1]; ORCiD logo [8];  [1];  [1]; ORCiD logo [8]; ORCiD logo [9];  [10]; ORCiD logo [3]; ORCiD logo [7] more »; ORCiD logo [1];  [1]; ORCiD logo [11]; ORCiD logo [12];  [5]; ORCiD logo [13]; ORCiD logo [14] « less
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. Estacion Experimental de Aula Dei-CSIC, Zaragoza (Spain); Fundacion ARAID, Zaragoza (Spain); Unidad Asociada al CSIC, Zaragoza (Spain)
  3. Univ. of Wisconsin, Madison, WI (United States); United States Dept. of Energy Great Lakes Bioenergy Research Center, Madison, WI (United States)
  4. Harvard Univ., Cambridge, MA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
  5. Univ. of California, Berkeley, CA (United States)
  6. Univ. of Zurich, Zurich (Switzerland)
  7. Univ. of Massachusetts, Amherst, MA (United States)
  8. Univ. of Leuven, Leuven (Belgium)
  9. Montana State Univ., Bozeman, MT (United States)
  10. Univ. of Texas Austin, Austin, TX (United States)
  11. Aberystwyth Univ., Aberystwyth (United Kingdom)
  12. Univ. of Minnesota, St. Paul, MN (United States)
  13. Unidad Asociada al CSIC, Zaragoza (Spain); Univ. de Zaragoza-Escuela Politecnica Superior de Huesca, Huesca (Spain)
  14. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1436654
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Comparative genomics; Plant genetics; Structural variation

Citation Formats

Gordon, Sean P., Contreras-Moreira, Bruno, Woods, Daniel P., Des Marais, David L., Burgess, Diane, Shu, Shengqiang, Stritt, Christoph, Roulin, Anne C., Schackwitz, Wendy, Tyler, Ludmila, Martin, Joel, Lipzen, Anna, Dochy, Niklas, Phillips, Jeremy, Barry, Kerrie, Geuten, Koen, Budak, Hikmet, Juenger, Thomas E., Amasino, Richard, Caicedo, Ana L., Goodstein, David, Davidson, Patrick, Mur, Luis A. J., Figueroa, Melania, Freeling, Michael, Catalan, Pilar, and Vogel, John P. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. United States: N. p., 2017. Web. doi:10.1038/s41467-017-02292-8.
Gordon, Sean P., Contreras-Moreira, Bruno, Woods, Daniel P., Des Marais, David L., Burgess, Diane, Shu, Shengqiang, Stritt, Christoph, Roulin, Anne C., Schackwitz, Wendy, Tyler, Ludmila, Martin, Joel, Lipzen, Anna, Dochy, Niklas, Phillips, Jeremy, Barry, Kerrie, Geuten, Koen, Budak, Hikmet, Juenger, Thomas E., Amasino, Richard, Caicedo, Ana L., Goodstein, David, Davidson, Patrick, Mur, Luis A. J., Figueroa, Melania, Freeling, Michael, Catalan, Pilar, & Vogel, John P. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure. United States. doi:10.1038/s41467-017-02292-8.
Gordon, Sean P., Contreras-Moreira, Bruno, Woods, Daniel P., Des Marais, David L., Burgess, Diane, Shu, Shengqiang, Stritt, Christoph, Roulin, Anne C., Schackwitz, Wendy, Tyler, Ludmila, Martin, Joel, Lipzen, Anna, Dochy, Niklas, Phillips, Jeremy, Barry, Kerrie, Geuten, Koen, Budak, Hikmet, Juenger, Thomas E., Amasino, Richard, Caicedo, Ana L., Goodstein, David, Davidson, Patrick, Mur, Luis A. J., Figueroa, Melania, Freeling, Michael, Catalan, Pilar, and Vogel, John P. Tue . "Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure". United States. doi:10.1038/s41467-017-02292-8. https://www.osti.gov/servlets/purl/1436654.
@article{osti_1436654,
title = {Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure},
author = {Gordon, Sean P. and Contreras-Moreira, Bruno and Woods, Daniel P. and Des Marais, David L. and Burgess, Diane and Shu, Shengqiang and Stritt, Christoph and Roulin, Anne C. and Schackwitz, Wendy and Tyler, Ludmila and Martin, Joel and Lipzen, Anna and Dochy, Niklas and Phillips, Jeremy and Barry, Kerrie and Geuten, Koen and Budak, Hikmet and Juenger, Thomas E. and Amasino, Richard and Caicedo, Ana L. and Goodstein, David and Davidson, Patrick and Mur, Luis A. J. and Figueroa, Melania and Freeling, Michael and Catalan, Pilar and Vogel, John P.},
abstractNote = {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.},
doi = {10.1038/s41467-017-02292-8},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 29 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Analysis of Plant Pan-Genomes and Transcriptomes with GET_HOMOLOGUES-EST, a Clustering Solution for Sequences of the Same Species
journal, February 2017

  • Contreras-Moreira, Bruno; Cantalapiedra, Carlos P.; García-Pereira, María J.
  • Frontiers in Plant Science, Vol. 8
  • DOI: 10.3389/fpls.2017.00184

Diterpene synthesis in Stevia rebaudiana: recruitment and up-regulation of key enzymes from the gibberellin biosynthetic pathway
journal, August 1999


Quartet Inference from SNP Data Under the Coalescent Model
journal, August 2014


Multiple reference genomes and transcriptomes for Arabidopsis thaliana
journal, August 2011

  • Gan, Xiangchao; Stegle, Oliver; Behr, Jonas
  • Nature, Vol. 477, Issue 7365
  • DOI: 10.1038/nature10414

The microbial pan-genome
journal, December 2005

  • Medini, Duccio; Donati, Claudio; Tettelin, Hervé
  • Current Opinion in Genetics & Development, Vol. 15, Issue 6
  • DOI: 10.1016/j.gde.2005.09.006

The Standing Pool of Genomic Structural Variation in a Natural Population of Mimulus guttatus
journal, December 2013

  • Flagel, Lex E.; Willis, John H.; Vision, Todd J.
  • Genome Biology and Evolution, Vol. 6, Issue 1
  • DOI: 10.1093/gbe/evt199

Insights into the Maize Pan-Genome and Pan-Transcriptome
journal, January 2014

  • Hirsch, Candice N.; Foerster, Jillian M.; Johnson, James M.
  • The Plant Cell, Vol. 26, Issue 1
  • DOI: 10.1105/tpc.113.119982

Targeted Genomic Mapping of a Red Seed Color Gene () in Wheat
journal, January 2008


Megabase Level Sequencing Reveals Contrasted Organization and Evolution Patterns of the Wheat Gene and Transposable Element Spaces
journal, June 2010

  • Choulet, Frédéric; Wicker, Thomas; Rustenholz, Camille
  • The Plant Cell, Vol. 22, Issue 6
  • DOI: 10.1105/tpc.110.074187

Development of SSR markers and analysis of diversity in Turkish populations of Brachypodium distachyon
journal, January 2009


Following Tetraploidy in Maize, a Short Deletion Mechanism Removed Genes Preferentially from One of the Two Homeologs
journal, June 2010


Sequencing of natural strains of Arabidopsis thaliana with short reads
journal, October 2008

  • Ossowski, S.; Schneeberger, K.; Clark, R. M.
  • Genome Research, Vol. 18, Issue 12
  • DOI: 10.1101/gr.080200.108

Major haplotype divergence including multiple germin-like protein genes, at the wheat Sr2 adult plant stem rust resistance locus
journal, December 2014


GET_HOMOLOGUES, a Versatile Software Package for Scalable and Robust Microbial Pangenome Analysis
journal, October 2013

  • Contreras-Moreira, Bruno; Vinuesa, Pablo
  • Applied and Environmental Microbiology, Vol. 79, Issue 24
  • DOI: 10.1128/AEM.02411-13

High-quality draft assemblies of mammalian genomes from massively parallel sequence data
journal, December 2010

  • Gnerre, S.; MacCallum, I.; Przybylski, D.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
  • DOI: 10.1073/pnas.1017351108

A First-Generation Haplotype Map of Maize
journal, November 2009


The pangenome of an agronomically important crop plant Brassica oleracea
journal, November 2016

  • Golicz, Agnieszka A.; Bayer, Philipp E.; Barker, Guy C.
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13390

BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs
journal, June 2015


Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world
journal, October 2008

  • Koonin, E. V.; Wolf, Y. I.
  • Nucleic Acids Research, Vol. 36, Issue 21
  • DOI: 10.1093/nar/gkn668

Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers
journal, July 2008


Phytozome: a comparative platform for green plant genomics
journal, November 2011

  • Goodstein, David M.; Shu, Shengqiang; Howson, Russell
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr944

A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome
journal, July 2014


Coordination of the maize transcriptome by a conserved circadian clock
journal, January 2010


TEMP: a computational method for analyzing transposable element polymorphism in populations
journal, April 2014

  • Zhuang, Jiali; Wang, Jie; Theurkauf, William
  • Nucleic Acids Research, Vol. 42, Issue 11
  • DOI: 10.1093/nar/gku323

Inconsistency of Phylogenetic Estimates from Concatenated Data under Coalescence
journal, February 2007


Maize Inbreds Exhibit High Levels of Copy Number Variation (CNV) and Presence/Absence Variation (PAV) in Genome Content
journal, November 2009


The development of quick, robust, quantitative phenotypic assays for describing the host–nonhost landscape to stripe rust
journal, October 2015

  • Dawson, Andrew M.; Bettgenhaeuser, Jan; Gardiner, Matthew
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00876

Comparative population genomics of maize domestication and improvement
journal, June 2012

  • Hufford, Matthew B.; Xu, Xun; van Heerwaarden, Joost
  • Nature Genetics, Vol. 44, Issue 7
  • DOI: 10.1038/ng.2309

Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


The pangenome of hexaploid bread wheat
journal, April 2017

  • Montenegro, Juan D.; Golicz, Agnieszka A.; Bayer, Philipp E.
  • The Plant Journal, Vol. 90, Issue 5
  • DOI: 10.1111/tpj.13515

Selection and phenotypic characterization of a core collection of Brachypodium distachyon inbred lines
journal, January 2014

  • Tyler, Ludmila; Fangel, Jonatan U.; Fagerström, Alexandra
  • BMC Plant Biology, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2229-14-25

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Many or most genes in Arabidopsis transposed after the origin of the order Brassicales
journal, October 2008


Transcripts of two ent-copalyl diphosphate synthase genes differentially localize in rice plants according to their distinct biological roles
journal, October 2014

  • Toyomasu, Tomonobu; Usui, Masami; Sugawara, Chizu
  • Journal of Experimental Botany, Vol. 66, Issue 1
  • DOI: 10.1093/jxb/eru424

A Major QTL, Ghd8, Plays Pleiotropic Roles in Regulating Grain Productivity, Plant Height, and Heading Date in Rice
journal, March 2011

  • Yan, Wen-Hao; Wang, Peng; Chen, Hua-Xia
  • Molecular Plant, Vol. 4, Issue 2
  • DOI: 10.1093/mp/ssq070

Two Adjacent Nucleotide-Binding Site–Leucine-Rich Repeat Class Genes Are Required to Confer Pikm -Specific Rice Blast Resistance
journal, October 2008


Infection of Brachypodium distachyon by Formae Speciales of Puccinia graminis: Early Infection Events and Host-Pathogen Incompatibility
journal, February 2013


Genome-wide patterns of genetic variation among elite maize inbred lines
journal, October 2010

  • Lai, Jinsheng; Li, Ruiqiang; Xu, Xun
  • Nature Genetics, Vol. 42, Issue 11
  • DOI: 10.1038/ng.684

Structural variation and genome complexity: is dispensable really dispensable?
journal, April 2014


Deletion in a gene associated with grain size increased yields during rice domestication
journal, July 2008

  • Shomura, Ayahiko; Izawa, Takeshi; Ebana, Kaworu
  • Nature Genetics, Vol. 40, Issue 8
  • DOI: 10.1038/ng.169

The genes for gibberellin biosynthesis in wheat
journal, August 2011

  • Huang, Yuanyuan; Yang, Wenlong; Pei, Zhong
  • Functional & Integrative Genomics, Vol. 12, Issue 1
  • DOI: 10.1007/s10142-011-0243-2

De novo assembly of soybean wild relatives for pan-genome analysis of diversity and agronomic traits
journal, September 2014

  • Li, Ying-hui; Zhou, Guangyu; Ma, Jianxin
  • Nature Biotechnology, Vol. 32, Issue 10
  • DOI: 10.1038/nbt.2979

Natural Variation in Maize Defense against Insect Herbivores
journal, January 2012

  • Meihls, L. N.; Kaur, H.; Jander, G.
  • Cold Spring Harbor Symposia on Quantitative Biology, Vol. 77, Issue 0
  • DOI: 10.1101/sqb.2012.77.014662

CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes
journal, March 2007


A multiple resistance locus on chromosome arm 3BS in wheat confers resistance to stem rust (Sr2), leaf rust (Lr27) and powdery mildew
journal, May 2011


Improved maize reference genome with single-molecule technologies
journal, June 2017

  • Jiao, Yinping; Peluso, Paul; Shi, Jinghua
  • Nature, Vol. 546, Issue 7659
  • DOI: 10.1038/nature22971

Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice
journal, August 2006


Population Structure in the Model Grass Is Highly Correlated with Flowering Differences across Broad Geographic Areas
journal, January 2016


Whole-genome sequencing of multiple Arabidopsis thaliana populations
journal, August 2011

  • Cao, Jun; Schneeberger, Korbinian; Ossowski, Stephan
  • Nature Genetics, Vol. 43, Issue 10
  • DOI: 10.1038/ng.911

Exploiting the Brachypodium Tool Box in cereal and grass research
journal, May 2011


Genome Reduction Uncovers a Large Dispensable Genome and Adaptive Role for Copy Number Variation in Asexually Propagated Solanum tuberosum
journal, January 2016

  • Hardigan, Michael A.; Crisovan, Emily; Hamilton, John P.
  • The Plant Cell, Vol. 28, Issue 2
  • DOI: 10.1105/tpc.15.00538

DTH8 Suppresses Flowering in Rice, Influencing Plant Height and Yield Potential Simultaneously
journal, June 2010

  • Wei, Xiangjin; Xu, Junfeng; Guo, Hongnian
  • Plant Physiology, Vol. 153, Issue 4
  • DOI: 10.1104/pp.110.156943

Conservation of telomere protein complexes: shuffling through evolution
journal, October 2009

  • Linger, Benjamin R.; Price, Carolyn M.
  • Critical Reviews in Biochemistry and Molecular Biology, Vol. 44, Issue 6
  • DOI: 10.3109/10409230903307329

QTLs for resistance to the false brome rust Puccinia brachypodii in the model grass Brachypodium distachyon L.
journal, February 2012

  • Barbieri, Mirko; Marcel, Thierry C.; Niks, Rients E.
  • Genome, Vol. 55, Issue 2
  • DOI: 10.1139/g2012-001

Genome diversity in Brachypodium distachyon: deep sequencing of highly diverse inbred lines
journal, July 2014

  • Gordon, Sean P.; Priest, Henry; Des Marais, David L.
  • The Plant Journal, Vol. 79, Issue 3
  • DOI: 10.1111/tpj.12569

    Works referencing / citing this record:

    Computational aspects underlying genome to phenome analysis in plants
    journal, January 2019

    • Bolger, Anthony M.; Poorter, Hendrik; Dumschott, Kathryn
    • The Plant Journal, Vol. 97, Issue 1
    • DOI: 10.1111/tpj.14179

    Extreme copy number variation at a tRNA ligase gene affecting phenology and fitness in yellow monkeyflowers
    journal, December 2018

    • Nelson, Thomas C.; Monnahan, Patrick J.; McIntosh, Mariah K.
    • Molecular Ecology, Vol. 28, Issue 6
    • DOI: 10.1111/mec.14904

    The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor
    journal, May 2019


    A strategy for building and using a human reference pangenome
    journal, January 2019


    The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor
    journal, May 2019


    Extreme copy number variation at a tRNA ligase gene affecting phenology and fitness in yellow monkeyflowers
    journal, December 2018

    • Nelson, Thomas C.; Monnahan, Patrick J.; McIntosh, Mariah K.
    • Molecular Ecology, Vol. 28, Issue 6
    • DOI: 10.1111/mec.14904

    Computational aspects underlying genome to phenome analysis in plants
    journal, January 2019

    • Bolger, Anthony M.; Poorter, Hendrik; Dumschott, Kathryn
    • The Plant Journal, Vol. 97, Issue 1
    • DOI: 10.1111/tpj.14179

    A strategy for building and using a human reference pangenome
    journal, January 2019