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

Title: Population structure in the model grass Brachypodium distachyon is highly correlated with flowering differences across broad geographic areas

Abstract

The small, annual grass Brachypodium distachyon (L.) Beauv., a close relative of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.), is a powerful model system for cereals and bioenergy grasses. Genome-wide association studies (GWAS) of natural variation can elucidate the genetic basis of complex traits but have been so far limited in B. distachyon by the lack of large numbers of well-characterized and sufficiently diverse accessions. Here, we report on genotyping-by-sequencing (GBS) of 84 B. distachyon, seven B. hybridum, and three B. stacei accessions with diverse geographic origins including Albania, Armenia, Georgia, Italy, Spain, and Turkey. Over 90,000 high-quality single-nucleotide polymorphisms (SNPs) distributed across the Bd21 reference genome were identified. Our results confirm the hybrid nature of the B. hybridum genome, which appears as a mosaic of B. distachyon-like and B. stacei-like sequences. Analysis of more than 50,000 SNPs for the B. distachyon accessions revealed three distinct, genetically defined populations. Surprisingly, these genomic profiles are associated with differences in flowering time rather than with broad geographic origin. High levels of differentiation in loci associated with floral development support the differences in flowering phenology between B. distachyon populations. Genome-wide association studies combining genotypic and phenotypic data also suggest the presencemore » of one or more photoperiodism, circadian clock, and vernalization genes in loci associated with flowering time variation within B. distachyon populations. As a result, our characterization elucidates genes underlying population differences, expands the germplasm resources available for Brachypodium, and illustrates the feasibility and limitations of GWAS in this model grass.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [3];  [1];  [4];  [5];  [1];  [1]
  1. Univ. of Massachusetts, Amherst, MA (United States)
  2. ETSIA, Technical Univ. of Madrid, Madrid (Spain)
  3. The Ohio State Univ.-Lima, Lima, OH (United States)
  4. Univ. of Florence, Florence (Italy)
  5. Univ. di Palermo, Palermo (Italy)
Publication Date:
Research Org.:
Univ. of California, San Diego, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1312966
Grant/Contract Number:  
SC0006621
Resource Type:
Accepted Manuscript
Journal Name:
The Plant Genome
Additional Journal Information:
Journal Volume: 9; Journal Issue: 2; Journal ID: ISSN 1940-3372
Publisher:
Alliance of Crop, Soil, and Environmental Science Societies
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS

Citation Formats

Tyler, Ludmila, Lee, Scott J., Young, Nelson D., DeIulio, Gregory A., Benavente, Elena, Reagon, Michael, Sysopha, Jessica, Baldini, Riccardo M., Troia, Angelo, Hazen, Samuel P., and Caicedo, Ana L. Population structure in the model grass Brachypodium distachyon is highly correlated with flowering differences across broad geographic areas. United States: N. p., 2016. Web. doi:10.3835/plantgenome2015.08.0074.
Tyler, Ludmila, Lee, Scott J., Young, Nelson D., DeIulio, Gregory A., Benavente, Elena, Reagon, Michael, Sysopha, Jessica, Baldini, Riccardo M., Troia, Angelo, Hazen, Samuel P., & Caicedo, Ana L. Population structure in the model grass Brachypodium distachyon is highly correlated with flowering differences across broad geographic areas. United States. doi:10.3835/plantgenome2015.08.0074.
Tyler, Ludmila, Lee, Scott J., Young, Nelson D., DeIulio, Gregory A., Benavente, Elena, Reagon, Michael, Sysopha, Jessica, Baldini, Riccardo M., Troia, Angelo, Hazen, Samuel P., and Caicedo, Ana L. Fri . "Population structure in the model grass Brachypodium distachyon is highly correlated with flowering differences across broad geographic areas". United States. doi:10.3835/plantgenome2015.08.0074. https://www.osti.gov/servlets/purl/1312966.
@article{osti_1312966,
title = {Population structure in the model grass Brachypodium distachyon is highly correlated with flowering differences across broad geographic areas},
author = {Tyler, Ludmila and Lee, Scott J. and Young, Nelson D. and DeIulio, Gregory A. and Benavente, Elena and Reagon, Michael and Sysopha, Jessica and Baldini, Riccardo M. and Troia, Angelo and Hazen, Samuel P. and Caicedo, Ana L.},
abstractNote = {The small, annual grass Brachypodium distachyon (L.) Beauv., a close relative of wheat (Triticum aestivum L.) and barley (Hordeum vulgare L.), is a powerful model system for cereals and bioenergy grasses. Genome-wide association studies (GWAS) of natural variation can elucidate the genetic basis of complex traits but have been so far limited in B. distachyon by the lack of large numbers of well-characterized and sufficiently diverse accessions. Here, we report on genotyping-by-sequencing (GBS) of 84 B. distachyon, seven B. hybridum, and three B. stacei accessions with diverse geographic origins including Albania, Armenia, Georgia, Italy, Spain, and Turkey. Over 90,000 high-quality single-nucleotide polymorphisms (SNPs) distributed across the Bd21 reference genome were identified. Our results confirm the hybrid nature of the B. hybridum genome, which appears as a mosaic of B. distachyon-like and B. stacei-like sequences. Analysis of more than 50,000 SNPs for the B. distachyon accessions revealed three distinct, genetically defined populations. Surprisingly, these genomic profiles are associated with differences in flowering time rather than with broad geographic origin. High levels of differentiation in loci associated with floral development support the differences in flowering phenology between B. distachyon populations. Genome-wide association studies combining genotypic and phenotypic data also suggest the presence of one or more photoperiodism, circadian clock, and vernalization genes in loci associated with flowering time variation within B. distachyon populations. As a result, our characterization elucidates genes underlying population differences, expands the germplasm resources available for Brachypodium, and illustrates the feasibility and limitations of GWAS in this model grass.},
doi = {10.3835/plantgenome2015.08.0074},
journal = {The Plant Genome},
number = 2,
volume = 9,
place = {United States},
year = {2016},
month = {4}
}

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

Citation Metrics:
Cited by: 5 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

A protocol for Agrobacterium-mediated transformation of Brachypodium distachyon community standard line Bd21
journal, April 2009

  • Alves, Sílvia C.; Worland, Barbara; Thole, Vera
  • Nature Protocols, Vol. 4, Issue 5
  • DOI: 10.1038/nprot.2009.30

LOSITAN: A workbench to detect molecular adaptation based on a F st -outlier method
journal, July 2008


Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines
journal, March 2010

  • Atwell, Susanna; Huang, Yu S.; Vilhjálmsson, Bjarni J.
  • Nature, Vol. 465, Issue 7298
  • DOI: 10.1038/nature08800

A Pseudo-Response Regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.)
journal, July 2007

  • Beales, James; Turner, Adrian; Griffiths, Simon
  • Theoretical and Applied Genetics, Vol. 115, Issue 5
  • DOI: 10.1007/s00122-007-0603-4

Genome-wide association studies in plants: the missing heritability is in the field
journal, January 2011

  • Brachi, Benjamin; Morris, Geoffrey P.; Borevitz, Justin O.
  • Genome Biology, Vol. 12, Issue 10
  • DOI: 10.1186/gb-2011-12-10-232

TASSEL: software for association mapping of complex traits in diverse samples
journal, June 2007


Brachypodium as a Model for the Grasses: Today and the Future
journal, July 2011

  • Brkljacic, Jelena; Grotewold, Erich; Scholl, Randy
  • Plant Physiology, Vol. 157, Issue 1
  • DOI: 10.1104/pp.111.179531

BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Evolution and taxonomic split of the model grass Brachypodium distachyon
journal, January 2012

  • Catalán, Pilar; Müller, Jochen; Hasterok, Robert
  • Annals of Botany, Vol. 109, Issue 2
  • DOI: 10.1093/aob/mcr294

Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation
journal, October 2008


Targeting environmental adaptation in the monocot model Brachypodium distachyon: a multi-faceted approach
journal, January 2014


Auxin regulates distal stem cell differentiation in Arabidopsis roots
journal, June 2010

  • Ding, Z.; Friml, J.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 26
  • DOI: 10.1073/pnas.1000672107

Brachypodium distachyon . A New Model System for Functional Genomics in Grasses
journal, December 2001

  • Draper, John; Mur, Luis A. J.; Jenkins, Glyn
  • Plant Physiology, Vol. 127, Issue 4
  • DOI: 10.1104/pp.010196

agriGO: a GO analysis toolkit for the agricultural community
journal, April 2010

  • Du, Zhou; Zhou, Xin; Ling, Yi
  • Nucleic Acids Research, Vol. 38, Issue suppl_2
  • DOI: 10.1093/nar/gkq310

A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species
journal, May 2011


Detecting the number of clusters of individuals using the software structure: a simulation study
journal, July 2005


Inference of population structure using multilocus genotype data: dominant markers and null alleles: TECHNICAL ARTICLE
journal, March 2007


Confidence Limits on Phylogenies: an Approach Using the Bootstrap
journal, July 1985


Validation of microsatellite markers for cytotype discrimination in the model grass Brachypodium distachyon
journal, July 2012

  • Giraldo, Patricia; Rodríguez-Quijano, Marta; Vázquez, José F.
  • Genome, Vol. 55, Issue 7
  • DOI: 10.1139/g2012-039

Brachypodium: a promising hub between model species and cereals
journal, September 2014

  • Girin, Thomas; David, Laure C.; Chardin, Camille
  • Journal of Experimental Botany, Vol. 65, Issue 19
  • DOI: 10.1093/jxb/eru376

The iPlant Collaborative: Cyberinfrastructure for Plant Biology
journal, January 2011

  • Goff, Stephen A.; Vaughn, Matthew; McKay, Sheldon
  • Frontiers in Plant Science, Vol. 2
  • DOI: 10.3389/fpls.2011.00034

Analysis of saccharification in Brachypodium distachyon stems under mild conditions of hydrolysis
journal, January 2008

  • Gomez, Leonardo D.; Bristow, Jennifer K.; Statham, Emily R.
  • Biotechnology for Biofuels, Vol. 1, Issue 1
  • DOI: 10.1186/1754-6834-1-15

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

The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana
journal, September 2007

  • Gremski, K.; Ditta, G.; Yanofsky, M. F.
  • Development, Vol. 134, Issue 20
  • DOI: 10.1242/dev.011510

Laying the Cytotaxonomic Foundations of a New Model Grass, Brachypodium distachyon (L.) Beauv.
journal, January 2004


Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses
journal, April 2010


Genome-wide association studies of 14 agronomic traits in rice landraces
journal, October 2010

  • Huang, Xuehui; Wei, Xinghua; Sang, Tao
  • Nature Genetics, Vol. 42, Issue 11
  • DOI: 10.1038/ng.695

Inferring weak population structure with the assistance of sample group information
journal, September 2009


Dendroscope: An interactive viewer for large phylogenetic trees
journal, November 2007

  • Huson, Daniel H.; Richter, Daniel C.; Rausch, Christian
  • BMC Bioinformatics, Vol. 8, Issue 1
  • DOI: 10.1186/1471-2105-8-460

Painting the chromosomes of Brachypodium—current status and future prospects
journal, June 2011


FT Protein Acts as a Long-Range Signal in Arabidopsis
journal, June 2007


Activation Tagging of the Floral Inducer FT
journal, December 1999


Recombination and linkage disequilibrium in Arabidopsis thaliana
journal, August 2007

  • Kim, Sung; Plagnol, Vincent; Hu, Tina T.
  • Nature Genetics, Vol. 39, Issue 9
  • DOI: 10.1038/ng2115

A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers
journal, August 1993


The development of Arabidopsis as a model plant
journal, March 2010


Biological conversion assay using Clostridium phytofermentans to estimate plant feedstock quality
journal, January 2012

  • Lee, Scott J.; Warnick, Thomas A.; Pattathil, Sivakumar
  • Biotechnology for Biofuels, Vol. 5, Issue 1
  • DOI: 10.1186/1754-6834-5-5

Involvement of brassinosteroid signals in the floral-induction network of Arabidopsis
journal, August 2010

  • Li, J.; Li, Y.; Chen, S.
  • Journal of Experimental Botany, Vol. 61, Issue 15
  • DOI: 10.1093/jxb/erq241

A DNA Barcoding Method to Discriminate between the Model Plant Brachypodium distachyon and Its Close Relatives B. stacei and B. hybridum (Poaceae)
journal, December 2012


Environmental niche variation and evolutionary diversification of the Brachypodium distachyon grass complex species in their native circum-Mediterranean range
journal, July 2015

  • Lopez-Alvarez, D.; Manzaneda, A. J.; Rey, P. J.
  • American Journal of Botany, Vol. 102, Issue 7
  • DOI: 10.3732/ajb.1500128

The bZIP Transcription Factor PERIANTHIA: A Multifunctional Hub for Meristem Control
journal, January 2011

  • Maier, Annette T.; Stehling-Sun, Sandra; Offenburger, Sarah-Lena
  • Frontiers in Plant Science, Vol. 2
  • DOI: 10.3389/fpls.2011.00079

SEPALLATA gene diversification: brave new whorls
journal, September 2005


Range of cell-wall alterations enhance saccharification in Brachypodium distachyon mutants
journal, September 2014

  • Marriott, Poppy E.; Sibout, Richard; Lapierre, Catherine
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 40
  • DOI: 10.1073/pnas.1414020111

The Extent of Linkage Disequilibrium in Rice ( Oryza sativa L.)
journal, October 2007


Unlocking Triticeae genomics to sustainably feed the future
journal, November 2013

  • Mochida, K.; Shinozaki, K.
  • Plant and Cell Physiology, Vol. 54, Issue 12
  • DOI: 10.1093/pcp/pct163

Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution
journal, June 2009

  • Mosquna, A.; Katz, A.; Decker, E. L.
  • Development, Vol. 136, Issue 14
  • DOI: 10.1242/dev.035048

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


PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, Together Play Essential Roles Close to the Circadian Clock of Arabidopsis thaliana
journal, May 2005

  • Nakamichi, Norihito; Kita, Masanori; Ito, Shogo
  • Plant and Cell Physiology, Vol. 46, Issue 5
  • DOI: 10.1093/pcp/pci086

AINTEGUMENTA Contributes to Organ Polarity and Regulates Growth of Lateral Organs in Combination with YABBY Genes
journal, May 2006


Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development
journal, January 2014


Genome-wide association studies for agronomical traits in a world wide spring barley collection
journal, January 2012


Population Structure and Eigenanalysis
journal, January 2006


Principal components analysis corrects for stratification in genome-wide association studies
journal, July 2006

  • Price, Alkes L.; Patterson, Nick J.; Plenge, Robert M.
  • Nature Genetics, Vol. 38, Issue 8
  • DOI: 10.1038/ng1847

Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon
journal, December 2013

  • Ream, Thomas S.; Woods, Daniel P.; Schwartz, Christopher J.
  • Plant Physiology, Vol. 164, Issue 2
  • DOI: 10.1104/pp.113.232678

MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor
journal, March 2010

  • Schlereth, Alexandra; Möller, Barbara; Liu, Weilin
  • Nature, Vol. 464, Issue 7290
  • DOI: 10.1038/nature08836

LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems: LOM genes control meristem maintenance
journal, October 2010


Natural Variation of Flowering Time and Vernalization Responsiveness in Brachypodium distachyon
journal, February 2010

  • Schwartz, Christopher J.; Doyle, Mark R.; Manzaneda, Antonio J.
  • BioEnergy Research, Vol. 3, Issue 1
  • DOI: 10.1007/s12155-009-9069-3

The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis
journal, February 2008


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


Universal primers for amplification of three non-coding regions of chloroplast DNA
journal, November 1991

  • Taberlet, Pierre; Gielly, Ludovic; Pautou, Guy
  • Plant Molecular Biology, Vol. 17, Issue 5
  • DOI: 10.1007/BF00037152

MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods
journal, May 2011

  • Tamura, K.; Peterson, D.; Peterson, N.
  • Molecular Biology and Evolution, Vol. 28, Issue 10
  • DOI: 10.1093/molbev/msr121

Genome-wide association study of leaf architecture in the maize nested association mapping population
journal, January 2011

  • Tian, Feng; Bradbury, Peter J.; Brown, Patrick J.
  • Nature Genetics, Vol. 43, Issue 2
  • DOI: 10.1038/ng.746

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

Agrobacterium-mediated transformation of the temperate grass Brachypodium distachyon (genotype Bd21) for T-DNA insertional mutagenesis
journal, April 2008


Agrobacterium-mediated transformation and inbred line development in the model grass Brachypodium distachyon
journal, January 2006

  • Vogel, John P.; Garvin, David F.; Leong, Oymon M.
  • Plant Cell, Tissue and Organ Culture, Vol. 84, Issue 2
  • DOI: 10.1007/s11240-005-9023-9

High-efficiency Agrobacterium-mediated transformation of Brachypodium distachyon inbred line Bd21-3
journal, November 2007


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


Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes
journal, December 2011

  • Xu, Xun; Liu, Xin; Ge, Song
  • Nature Biotechnology, Vol. 30, Issue 1
  • DOI: 10.1038/nbt.2050

Genetic Characterization and Linkage Disequilibrium Estimation of a Global Maize Collection Using SNP Markers
journal, December 2009


Hd1 , a Major Photoperiod Sensitivity Quantitative Trait Locus in Rice, Is Closely Related to the Arabidopsis Flowering Time Gene CONSTANS
journal, December 2000

  • Yano, Masahiro; Katayose, Yuichi; Ashikari, Motoyuki
  • The Plant Cell, Vol. 12, Issue 12
  • DOI: 10.1105/tpc.12.12.2473

A unified mixed-model method for association mapping that accounts for multiple levels of relatedness
journal, December 2005

  • Yu, Jianming; Pressoir, Gael; Briggs, William H.
  • Nature Genetics, Vol. 38, Issue 2
  • DOI: 10.1038/ng1702

Early-Flowering Mutants of Arabidopsis thaliana
journal, January 1992

  • Zagotta, Mt; Shannon, S.; Jacobs, C.
  • Functional Plant Biology, Vol. 19, Issue 4
  • DOI: 10.1071/PP9920411

Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley
journal, February 2012

  • Zakhrabekova, S.; Gough, S. P.; Braumann, I.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 11
  • DOI: 10.1073/pnas.1113009109

Mixed linear model approach adapted for genome-wide association studies
journal, March 2010

  • Zhang, Zhiwu; Ersoz, Elhan; Lai, Chao-Qiang
  • Nature Genetics, Vol. 42, Issue 4
  • DOI: 10.1038/ng.546

    Works referencing / citing this record: