Global Diversity of the Brachypodium Species Complex as a Resource for Genome-Wide Association Studies Demonstrated for Agronomic Traits in Response to Climate

Wilson, Pip B.; Streich, Jared C.; Murray, Kevin D.; Eichten, Steve R.; Cheng, Riyan; Aitken, Nicola C.; Spokas, Kurt; Warthmann, Norman; Gordon, Sean P.; Vogel, John P.; Borevitz, Justin O.

doi:10.1534/genetics.118.301589

Title: Global Diversity of the Brachypodium Species Complex as a Resource for Genome-Wide Association Studies Demonstrated for Agronomic Traits in Response to Climate

Journal Article · 08 January 2019 · Genetics

DOI: https://doi.org/10.1534/genetics.118.301589 · OSTI ID:1493985

Wilson, Pip B. ^[1];

^[1]; Murray, Kevin D. ^[1]; Eichten, Steve R. ^[1]; Cheng, Riyan ^[2]; Aitken, Nicola C. ^[1]; Spokas, Kurt ^[3]; Warthmann, Norman ^[1]; Gordon, Sean P. ^[4]; Vogel, John P. ^[4];

^[1]

Australian National Univ., Canberra, ACT (Australia)
Univ. of California, San Diego, CA (United States); Australian National Univ., Canberra, ACT (Australia)
United States Department of Agriculture (USDA), St. Paul, MN (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

The development of model systems requires a detailed assessment of standing genetic variation across natural populations. The Brachypodium species complex has been promoted as a plant model for grass genomics with translation to small grain and biomass crops. To capture the genetic diversity within this species complex, thousands of Brachypodium accessions from around the globe were collected and genotyped by sequencing. Overall, 1897 samples were classified into two diploid or allopolyploid species, and then further grouped into distinct inbred genotypes. A core set of diverse B. distachyon diploid lines was selected for whole genome sequencing and high resolution phenotyping. Genome-wide association studies across simulated seasonal environments was used to identify candidate genes and pathways tied to key life history and agronomic traits under current and future climatic conditions. A total of 8, 22, and 47 QTL were identified for flowering time, early vigor, and energy traits, respectively. The results highlight the genomic structure of the Brachypodium species complex, and the diploid lines provided a resource that allows complex trait dissection within this grass model species.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Contributing Organization:: Accession Contributors

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1493985

Journal Information:: Genetics, Journal Name: Genetics Journal Issue: 1 Vol. 211; ISSN 0016-6731

Publisher:: Genetics Society of AmericaCopyright Statement

Country of Publication:: United States

Language:: English

References (129)

Genomic Diversity and Climate Adaptation in Brachypodium Wilson, Pip; Streich, Jared; Borevitz, Justin Genetics and Genomics of Brachypodium https://doi.org/10.1007/7397_2015_18	book	January 2015
Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars Wang, Minghui; Jiang, Ning; Jia, Tianye Theoretical and Applied Genetics, Vol. 124, Issue 2 https://doi.org/10.1007/s00122-011-1697-2	journal	September 2011
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method Earl, Dent A.; vonHoldt, Bridgett M. Conservation Genetics Resources, Vol. 4, Issue 2 https://doi.org/10.1007/s12686-011-9548-7	journal	October 2011
Pyramiding greater early vigour and integrated transpiration efficiency in bread wheat; trade-offs and benefits Wilson, P. B.; Rebetzke, G. J.; Condon, A. G. Field Crops Research, Vol. 183 https://doi.org/10.1016/j.fcr.2015.07.002	journal	November 2015
TraitCapture: genomic and environment modelling of plant phenomic data Brown, Tim B.; Cheng, Riyan; Sirault, Xavier RR Current Opinion in Plant Biology, Vol. 18 https://doi.org/10.1016/j.pbi.2014.02.002	journal	April 2014
Genetic dissection of seedling and early vigor in a recombinant inbred line population of rice Lu, Xun-Li; Niu, Ao-Lei; Cai, Hai-Ya Plant Science, Vol. 172, Issue 2 https://doi.org/10.1016/j.plantsci.2006.08.012	journal	February 2007
Genome-wide association studies of 14 agronomic traits in rice landraces Huang, Xuehui; Wei, Xinghua; Sang, Tao Nature Genetics, Vol. 42, Issue 11 https://doi.org/10.1038/ng.695	journal	October 2010
Genome-wide association study of leaf architecture in the maize nested association mapping population Tian, Feng; Bradbury, Peter J.; Brown, Patrick J. Nature Genetics, Vol. 43, Issue 2 https://doi.org/10.1038/ng.746	journal	January 2011
Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure Gordon, Sean P.; Contreras-Moreira, Bruno; Woods, Daniel P. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02292-8	journal	December 2017
Targeted A-to-G base editing of chloroplast DNA in plants Mok, Young Geun; Hong, Sunghyun; Bae, Su-Ji Nature Plants, Vol. 8, Issue 12 https://doi.org/10.1038/s41477-022-01279-8	journal	December 2022
SSR individual identification system construction and population genetics analysis for Chamaecyparis formosensis Huang, Chiun-Jr; Chu, Fang-Hua; Huang, Yi-Shiang Scientific Reports, Vol. 12, Issue 1 https://doi.org/10.1038/s41598-022-07870-5	journal	March 2022
Rapid recent growth and divergence of rice nuclear genomes Ma, J.; Bennetzen, J. L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 34 https://doi.org/10.1073/pnas.0403715101	journal	July 2004
Evolution and taxonomic split of the model grass Brachypodium distachyon Catalán, Pilar; Müller, Jochen; Hasterok, Robert Annals of Botany, Vol. 109, Issue 2 https://doi.org/10.1093/aob/mcr294	journal	January 2012
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data Li, H. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr509	journal	September 2011
Axe: rapid, competitive sequence read demultiplexing using a trie Murray, Kevin D.; Borevitz, Justin O. Bioinformatics, Vol. 34, Issue 22 https://doi.org/10.1093/bioinformatics/bty432	journal	June 2018
Inference of Population Structure Using Multilocus Genotype Data Pritchard, Jonathan K.; Stephens, Matthew; Donnelly, Peter Genetics, Vol. 155, Issue 2 https://doi.org/10.1093/genetics/155.2.945	journal	June 2000
Theoretical Basis of the Beavis Effect Xu, Shizhong Genetics, Vol. 165, Issue 4 https://doi.org/10.1093/genetics/165.4.2259	journal	December 2003
Breeding for high water-use efficiency Condon, A. G. Journal of Experimental Botany, Vol. 55, Issue 407 https://doi.org/10.1093/jxb/erh277	journal	September 2004
Effect of Selection for Dark Respiration Rate of Mature Leaves on Crop Yields of Lolium perenne cv. S23 Wilson, D.; Jones, J. G. Annals of Botany, Vol. 49, Issue 3 https://doi.org/10.1093/oxfordjournals.aob.a086255	journal	March 1982
Frequent Gene Movement and Pseudogene Evolution Is Common to the Large and Complex Genomes of Wheat, Barley, and Their Relatives Wicker, Thomas; Mayer, Klaus F. X.; Gundlach, Heidrun The Plant Cell, Vol. 23, Issue 5 https://doi.org/10.1105/tpc.111.086629	journal	May 2011
Linear Mixed Models Minimise False Positive Rate and Enhance Precision of Mass Univariate Vertex-Wise Analyses of Grey-Matter Couvy-Duchesne, Baptiste; Zhang, Futao; Kemper, Kathryn E. 2020 IEEE 17th International Symposium on Biomedical Imaging (ISBI) https://doi.org/10.1109/isbi45749.2020.9098719	conference	April 2020
Exploiting the Brachypodium Tool Box in cereal and grass research Mur, Luis A. J.; Allainguillaume, Joel; Catalán, Pilar New Phytologist, Vol. 191, Issue 2 https://doi.org/10.1111/j.1469-8137.2011.03748.x	journal	May 2011
Population and phylogenomic decomposition via genotyping-by-sequencing in Australian Pelargonium Nicotra, Adrienne B.; Chong, Caroline; Bragg, Jason G. Molecular Ecology, Vol. 25, Issue 9 https://doi.org/10.1111/mec.13584	journal	May 2016
Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field Poorter, Hendrik; Fiorani, Fabio; Pieruschka, Roland New Phytologist, Vol. 212, Issue 4 https://doi.org/10.1111/nph.14243	journal	October 2016
Climate Change Impacts on Global Food Security Wheeler, T.; von Braun, J. Science, Vol. 341, Issue 6145 https://doi.org/10.1126/science.1239402	journal	August 2013
Molecular, morphological, and cytological analysis of diverse Brachypodium distachyon inbred lines Filiz, E.; Ozdemir, B. S.; Budak, F. Genome, Vol. 52, Issue 10 https://doi.org/10.1139/g09-062	journal	October 2009
Validation of microsatellite markers for cytotype discrimination in the model grass Brachypodium distachyon Giraldo, Patricia; Rodríguez-Quijano, Marta; Vázquez, José F. Genome, Vol. 55, Issue 7 https://doi.org/10.1139/g2012-039	journal	July 2012
Brachypodium distachyon and Setaria viridis : Model Genetic Systems for the Grasses Brutnell, Thomas P.; Bennetzen, Jeffrey L.; Vogel, John P. Annual Review of Plant Biology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105528	journal	April 2015
Natural Variations and Genome-Wide Association Studies in Crop Plants Huang, Xuehui; Han, Bin Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-035715	journal	April 2014
QTLRel: an R Package for Genome-wide Association Studies in which Relatedness is a Concern Cheng, Riyan; Abney, Mark; Palmer, Abraham A. BMC Genetics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2156-12-66	journal	January 2011
Development of SSR markers and analysis of diversity in Turkish populations of Brachypodium distachyon Vogel, John P.; Tuna, Metin; Budak, Hikmet BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-88	journal	January 2009
Genome-wide association studies in plants: the missing heritability is in the field Brachi, Benjamin; Morris, Geoffrey P.; Borevitz, Justin O. Genome Biology, Vol. 12, Issue 10 https://doi.org/10.1186/gb-2011-12-10-232	journal	January 2011
Environmental isolation explains Iberian genetic diversity in the highly homozygous model grass Brachypodium distachyon Marques, Isabel; Shiposha, Valeriia; López-Alvarez, Diana BMC Evolutionary Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12862-017-0996-x	journal	June 2017
Modelling the genetic architecture of flowering time control in barley through nested association mapping Maurer, Andreas; Draba, Vera; Jiang, Yong BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1459-7	journal	April 2015
Enviromic-based kernels may optimize resource allocation with multi-trait multi-environment genomic prediction for tropical Maize Gevartosky, Raysa; Carvalho, Humberto Fanelli; Costa-Neto, Germano BMC Plant Biology, Vol. 23, Issue 1 https://doi.org/10.1186/s12870-022-03975-1	journal	January 2023
Using Phenomic Analysis of Photosynthetic Function for Abiotic Stress Response Gene Discovery Rungrat, Tepsuda; Awlia, Mariam; Brown, Tim The Arabidopsis Book, Vol. 14 https://doi.org/10.1199/tab.0185	journal	January 2016
Linkage and Association Mapping of Arabidopsis thaliana Flowering Time in Nature Brachi, Benjamin; Faure, Nathalie; Horton, Matt PLoS Genetics, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pgen.1000940	journal	May 2010
A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species Elshire, Robert J.; Glaubitz, Jeffrey C.; Sun, Qi PLoS ONE, Vol. 6, Issue 5, Article No. e19379 https://doi.org/10.1371/journal.pone.0019379	journal	May 2011
A DNA Barcoding Method to Discriminate between the Model Plant Brachypodium distachyon and Its Close Relatives B. stacei and B. hybridum (Poaceae) López-Alvarez, Diana; López-Herranz, Maria Luisa; Betekhtin, Alexander PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0051058	journal	December 2012
Yield Trends Are Insufficient to Double Global Crop Production by 2050 Ray, Deepak K.; Mueller, Nathaniel D.; West, Paul C. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066428	journal	June 2013
Insight into the Karyotype Evolution of Brachypodium Species Using Comparative Chromosome Barcoding Idziak, Dominika; Hazuka, Iwona; Poliwczak, Beata PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0093503	journal	March 2014
Nested Association Mapping of Stem Rust Resistance in Wheat Using Genotyping by Sequencing Bajgain, Prabin; Rouse, Matthew N.; Tsilo, Toi J. PLOS ONE, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pone.0155760	journal	May 2016
Estimating hourly incoming solar radiation from limited meteorological data Spokas, Kurt; Forcella, Frank Weed Science, Vol. 54, Issue 1 https://doi.org/10.1614/ws-05-098r.1	journal	February 2006
libqcpp: A C++14 sequence quality control library D. Murray, Kevin; O. Borevitz, Justin The Journal of Open Source Software, Vol. 2, Issue 13 https://doi.org/10.21105/joss.00232	journal	May 2017
Memory of the vernalized state in plants including the model grass Brachypodium distachyon Woods, Daniel P.; Ream, Thomas S.; Amasino, Richard M. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00099	journal	March 2014
Identification and Roles of Photosystem II Assembly, Stability, and Repair Factors in Arabidopsis Lu, Yan Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00168	journal	February 2016
GENOTYPIC DIFFERENCES IN DARK RESPIRATION OF MATURE LEAVES IN WINTER WHEAT ( Triticum aestivum L.) Winzeler, M.; McCULLOUGH, D. E.; Hunt, L. A. Canadian Journal of Plant Science, Vol. 68, Issue 3 https://doi.org/10.4141/cjps88-080	journal	July 1988
Genomic Diversity and Climate Adaptation in Brachypodium Wilson, Pip; Streich, Jared; Borevitz, Justin Genetics and Genomics of Brachypodium https://doi.org/10.1007/7397_2015_18	book	January 2015
Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars Wang, Minghui; Jiang, Ning; Jia, Tianye Theoretical and Applied Genetics, Vol. 124, Issue 2 https://doi.org/10.1007/s00122-011-1697-2	journal	September 2011
Genome-wide association study for grain yield and related traits in an elite spring wheat population grown in temperate irrigated environments Sukumaran, Sivakumar; Dreisigacker, Susanne; Lopes, Marta Theoretical and Applied Genetics, Vol. 128, Issue 2 https://doi.org/10.1007/s00122-014-2435-3	journal	December 2014
Genomic breeding for food, environment and livelihoods Rivers, John; Warthmann, Norman; Pogson, Barry J. Food Security, Vol. 7, Issue 2 https://doi.org/10.1007/s12571-015-0431-3	journal	March 2015
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method Earl, Dent A.; vonHoldt, Bridgett M. Conservation Genetics Resources, Vol. 4, Issue 2 https://doi.org/10.1007/s12686-011-9548-7	journal	October 2011
Pyramiding greater early vigour and integrated transpiration efficiency in bread wheat; trade-offs and benefits Wilson, P. B.; Rebetzke, G. J.; Condon, A. G. Field Crops Research, Vol. 183 https://doi.org/10.1016/j.fcr.2015.07.002	journal	November 2015
TraitCapture: genomic and environment modelling of plant phenomic data Brown, Tim B.; Cheng, Riyan; Sirault, Xavier RR Current Opinion in Plant Biology, Vol. 18 https://doi.org/10.1016/j.pbi.2014.02.002	journal	April 2014
Genetic dissection of seedling and early vigor in a recombinant inbred line population of rice Lu, Xun-Li; Niu, Ao-Lei; Cai, Hai-Ya Plant Science, Vol. 172, Issue 2 https://doi.org/10.1016/j.plantsci.2006.08.012	journal	February 2007
Laying the Cytotaxonomic Foundations of a New Model Grass, Brachypodium distachyon (L.) Beauv. Hasterok, Robert; Draper, John; Jenkins, Glyn Chromosome Research, Vol. 12, Issue 4 https://doi.org/10.1023/B:CHRO.0000034130.35983.99	journal	January 2004
Genome sequencing and analysis of the model grass Brachypodium distachyon Nature, Vol. 463, Issue 7282, p. 763-768 https://doi.org/10.1038/nature08747	journal	February 2010
Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines Atwell, Susanna; Huang, Yu S.; Vilhjálmsson, Bjarni J. Nature, Vol. 465, Issue 7298 https://doi.org/10.1038/nature08800	journal	March 2010
Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm Huang, Xuehui; Zhao, Yan; Wei, Xinghua Nature Genetics, Vol. 44, Issue 1 https://doi.org/10.1038/ng.1018	journal	December 2011
Genome-wide association study using whole-genome sequencing rapidly identifies new genes influencing agronomic traits in rice Yano, Kenji; Yamamoto, Eiji; Aya, Koichiro Nature Genetics, Vol. 48, Issue 8 https://doi.org/10.1038/ng.3596	journal	June 2016
Genome-wide association studies of 14 agronomic traits in rice landraces Huang, Xuehui; Wei, Xinghua; Sang, Tao Nature Genetics, Vol. 42, Issue 11 https://doi.org/10.1038/ng.695	journal	October 2010
Genome-wide association study of leaf architecture in the maize nested association mapping population Tian, Feng; Bradbury, Peter J.; Brown, Patrick J. Nature Genetics, Vol. 43, Issue 2 https://doi.org/10.1038/ng.746	journal	January 2011
Improved linear mixed models for genome-wide association studies Listgarten, Jennifer; Lippert, Christoph; Kadie, Carl M. Nature Methods, Vol. 9, Issue 6 https://doi.org/10.1038/nmeth.2037	journal	May 2012
Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure Gordon, Sean P.; Contreras-Moreira, Bruno; Woods, Daniel P. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02292-8	journal	December 2017
Genetic improvement of early vigour in wheat Rebetzke, G. J.; Richards, R. A. Australian Journal of Agricultural Research, Vol. 50, Issue 3 https://doi.org/10.1071/A98125	journal	January 1999
Quantitative trait loci on chromosome 4B for coleoptile length and early vigour in wheat (Triticum aestivum L.) Rebetzke, G. J.; Appels, R.; Morrison, A. D. Australian Journal of Agricultural Research, Vol. 52, Issue 12 https://doi.org/10.1071/AR01042	journal	January 2001
Of growing importance: combining greater early vigour and transpiration efficiency for wheat in variable rainfed environments Wilson, P. B.; Rebetzke, G. J.; Condon, A. G. Functional Plant Biology, Vol. 42, Issue 12 https://doi.org/10.1071/FP15228	journal	January 2015
Rapid recent growth and divergence of rice nuclear genomes Ma, J.; Bennetzen, J. L. Proceedings of the National Academy of Sciences, Vol. 101, Issue 34 https://doi.org/10.1073/pnas.0403715101	journal	July 2004
The more the better? The role of polyploidy in facilitating plant invasions te Beest, M.; Le Roux, J. J.; Richardson, D. M. Annals of Botany, Vol. 109, Issue 1 https://doi.org/10.1093/aob/mcr277	journal	October 2011
Evolution and taxonomic split of the model grass Brachypodium distachyon Catalán, Pilar; Müller, Jochen; Hasterok, Robert Annals of Botany, Vol. 109, Issue 2 https://doi.org/10.1093/aob/mcr294	journal	January 2012
CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure Jakobsson, M.; Rosenberg, N. A. Bioinformatics, Vol. 23, Issue 14 https://doi.org/10.1093/bioinformatics/btm233	journal	May 2007
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data Li, H. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr509	journal	September 2011
A high-performance computing toolset for relatedness and principal component analysis of SNP data Zheng, X.; Levine, D.; Shen, J. Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts606	journal	October 2012
Axe: rapid, competitive sequence read demultiplexing using a trie Murray, Kevin D.; Borevitz, Justin O. Bioinformatics, Vol. 34, Issue 22 https://doi.org/10.1093/bioinformatics/bty432	journal	June 2018
Inference of Population Structure Using Multilocus Genotype Data Pritchard, Jonathan K.; Stephens, Matthew; Donnelly, Peter Genetics, Vol. 155, Issue 2 https://doi.org/10.1093/genetics/155.2.945	journal	June 2000
Theoretical Basis of the Beavis Effect Xu, Shizhong Genetics, Vol. 165, Issue 4 https://doi.org/10.1093/genetics/165.4.2259	journal	December 2003
Breeding for high water-use efficiency Condon, A. G. Journal of Experimental Botany, Vol. 55, Issue 407 https://doi.org/10.1093/jxb/erh277	journal	September 2004
Effect of Selection for Dark Respiration Rate of Mature Leaves on Crop Yields of Lolium perenne cv. S23 Wilson, D.; Jones, J. G. Annals of Botany, Vol. 49, Issue 3 https://doi.org/10.1093/oxfordjournals.aob.a086255	journal	March 1982
Brachypodium distachyon . A New Model System for Functional Genomics in Grasses Draper, John; Mur, Luis A. J.; Jenkins, Glyn Plant Physiology, Vol. 127, Issue 4 https://doi.org/10.1104/pp.010196	journal	December 2001
Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon Ream, Thomas S.; Woods, Daniel P.; Schwartz, Christopher J. Plant Physiology, Vol. 164, Issue 2 https://doi.org/10.1104/pp.113.232678	journal	December 2013
Brachypodium distachyon. A New Model System for Functional Genomics in Grasses Draper, J. PLANT PHYSIOLOGY, Vol. 127, Issue 4 https://doi.org/10.1104/pp.127.4.1539	journal	December 2001
Natural Variation in Brachypodium Links Vernalization and Flowering Time Loci as Major Flowering Determinants Bettgenhaeuser, Jan; Corke, Fiona M. K.; Opanowicz, Magdalena Plant Physiology, Vol. 173, Issue 1 https://doi.org/10.1104/pp.16.00813	journal	September 2016
Genetic Architecture of Flowering-Time Variation in Brachypodium distachyon Woods, Daniel P.; Bednarek, Ryland; Bouché, Frédéric Plant Physiology, Vol. 173, Issue 1 https://doi.org/10.1104/pp.16.01178	journal	October 2016
Frequent Gene Movement and Pseudogene Evolution Is Common to the Large and Complex Genomes of Wheat, Barley, and Their Relatives Wicker, Thomas; Mayer, Klaus F. X.; Gundlach, Heidrun The Plant Cell, Vol. 23, Issue 5 https://doi.org/10.1105/tpc.111.086629	journal	May 2011
Detecting the number of clusters of individuals using the software structure: a simulation study Evanno, G.; Regnaut, S.; Goudet, J. Molecular Ecology, Vol. 14, Issue 8 https://doi.org/10.1111/j.1365-294X.2005.02553.x	journal	July 2005
Genomic diversity in switchgrass (Panicum virgatum): from the continental scale to a dune landscape: GENOMIC DIVERSITY IN SWITCHGRASS Morris, Geoffrey P.; Grabowski, Paul P.; Borevitz, Justin O. Molecular Ecology, Vol. 20, Issue 23 https://doi.org/10.1111/j.1365-294X.2011.05335.x	journal	November 2011
Exploiting the Brachypodium Tool Box in cereal and grass research Mur, Luis A. J.; Allainguillaume, Joel; Catalán, Pilar New Phytologist, Vol. 191, Issue 2 https://doi.org/10.1111/j.1469-8137.2011.03748.x	journal	May 2011
genalex 6: genetic analysis in Excel. Population genetic software for teaching and research Peakall, Rod; Smouse, Peter E. Molecular Ecology Notes, Vol. 6, Issue 1 https://doi.org/10.1111/j.1471-8286.2005.01155.x	journal	March 2006
Population and phylogenomic decomposition via genotyping-by-sequencing in Australian Pelargonium Nicotra, Adrienne B.; Chong, Caroline; Bragg, Jason G. Molecular Ecology, Vol. 25, Issue 9 https://doi.org/10.1111/mec.13584	journal	May 2016
Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field Poorter, Hendrik; Fiorani, Fabio; Pieruschka, Roland New Phytologist, Vol. 212, Issue 4 https://doi.org/10.1111/nph.14243	journal	October 2016
Climate Change Impacts on Global Food Security Wheeler, T.; von Braun, J. Science, Vol. 341, Issue 6145 https://doi.org/10.1126/science.1239402	journal	August 2013
Two Sides of a Coin: a Zika Virus Mutation Selected in Pregnant Rhesus Macaques Promotes Fetal Infection in Mice but at a Cost of Reduced Fitness in Nonpregnant Macaques and Diminished Transmissibility by Vectors Lemos, Danilo; Stuart, Jackson B.; Louie, William Journal of Virology, Vol. 94, Issue 24 https://doi.org/10.1128/jvi.01605-20	journal	September 2020
Molecular, morphological, and cytological analysis of diverse Brachypodium distachyon inbred lines Filiz, E.; Ozdemir, B. S.; Budak, F. Genome, Vol. 52, Issue 10 https://doi.org/10.1139/G09-062	journal	October 2009
Validation of microsatellite markers for cytotype discrimination in the model grass Brachypodium distachyon Giraldo, Patricia; Rodríguez-Quijano, Marta; Vázquez, José F. Genome, Vol. 55, Issue 7 https://doi.org/10.1139/g2012-039	journal	July 2012
Brachypodium distachyon and Setaria viridis : Model Genetic Systems for the Grasses Brutnell, Thomas P.; Bennetzen, Jeffrey L.; Vogel, John P. Annual Review of Plant Biology, Vol. 66, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105528	journal	April 2015
Natural Variations and Genome-Wide Association Studies in Crop Plants Huang, Xuehui; Han, Bin Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-035715	journal	April 2014
QTLRel: an R Package for Genome-wide Association Studies in which Relatedness is a Concern Cheng, Riyan; Abney, Mark; Palmer, Abraham A. BMC Genetics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2156-12-66	journal	January 2011
Development of SSR markers and analysis of diversity in Turkish populations of Brachypodium distachyon Vogel, John P.; Tuna, Metin; Budak, Hikmet BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-88	journal	January 2009
Genome-wide association studies in plants: the missing heritability is in the field Brachi, Benjamin; Morris, Geoffrey P.; Borevitz, Justin O. Genome Biology, Vol. 12, Issue 10 https://doi.org/10.1186/gb-2011-12-10-232	journal	January 2011
Environmental isolation explains Iberian genetic diversity in the highly homozygous model grass Brachypodium distachyon Marques, Isabel; Shiposha, Valeriia; López-Alvarez, Diana BMC Evolutionary Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12862-017-0996-x	journal	June 2017
Modelling the genetic architecture of flowering time control in barley through nested association mapping Maurer, Andreas; Draba, Vera; Jiang, Yong BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1459-7	journal	April 2015
The combination of gas-phase fluorophore technology and automation to enable high-throughput analysis of plant respiration Scafaro, Andrew P.; Negrini, A. Clarissa A.; O’Leary, Brendan Plant Methods, Vol. 13, Issue 1 https://doi.org/10.1186/s13007-017-0169-3	journal	March 2017
AdapterRemoval v2: rapid adapter trimming, identification, and read merging Schubert, Mikkel; Lindgreen, Stinus; Orlando, Ludovic BMC Research Notes, Vol. 9, Issue 1 https://doi.org/10.1186/s13104-016-1900-2	journal	February 2016
Using Phenomic Analysis of Photosynthetic Function for Abiotic Stress Response Gene Discovery Rungrat, Tepsuda; Awlia, Mariam; Brown, Tim The Arabidopsis Book, Vol. 14 https://doi.org/10.1199/tab.0185	journal	January 2016
Linkage and Association Mapping of Arabidopsis thaliana Flowering Time in Nature Brachi, Benjamin; Faure, Nathalie; Horton, Matt PLoS Genetics, Vol. 6, Issue 5 https://doi.org/10.1371/journal.pgen.1000940	journal	May 2010
Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses Higgins, Janet A.; Bailey, Paul C.; Laurie, David A. PLoS ONE, Vol. 5, Issue 4 https://doi.org/10.1371/journal.pone.0010065	journal	April 2010
A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species Elshire, Robert J.; Glaubitz, Jeffrey C.; Sun, Qi PLoS ONE, Vol. 6, Issue 5, Article No. e19379 https://doi.org/10.1371/journal.pone.0019379	journal	May 2011
A DNA Barcoding Method to Discriminate between the Model Plant Brachypodium distachyon and Its Close Relatives B. stacei and B. hybridum (Poaceae) López-Alvarez, Diana; López-Herranz, Maria Luisa; Betekhtin, Alexander PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0051058	journal	December 2012
Yield Trends Are Insufficient to Double Global Crop Production by 2050 Ray, Deepak K.; Mueller, Nathaniel D.; West, Paul C. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0066428	journal	June 2013
Insight into the Karyotype Evolution of Brachypodium Species Using Comparative Chromosome Barcoding Idziak, Dominika; Hazuka, Iwona; Poliwczak, Beata PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0093503	journal	March 2014
Nested Association Mapping of Stem Rust Resistance in Wheat Using Genotyping by Sequencing Bajgain, Prabin; Rouse, Matthew N.; Tsilo, Toi J. PLOS ONE, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pone.0155760	journal	May 2016
Estimating hourly incoming solar radiation from limited meteorological data Spokas, Kurt; Forcella, Frank Weed Science, Vol. 54, Issue 1 https://doi.org/10.1614/WS-05-098R.1	journal	February 2006
libqcpp: A C++14 sequence quality control library D. Murray, Kevin; O. Borevitz, Justin The Journal of Open Source Software, Vol. 2, Issue 13 https://doi.org/10.21105/joss.00232	journal	May 2017
Visual Quantification of Wheat Development1 Haun, J. R. Agronomy Journal, Vol. 65, Issue 1 https://doi.org/10.2134/agronj1973.00021962006500010035x	journal	January 1973
QTL for Fatty Acid Composition of Maize Kernel Oil in Illinois High Oil × B73 Backcross-Derived Lines Wassom, James J.; Mikkelineni, Venugopal; Bohn, Martin O. Crop Science, Vol. 48, Issue 1 https://doi.org/10.2135/cropsci2007.04.0208	journal	January 2008
Development of Genetic and Genomic Research Resources for , a New Model System for Grass Crop Research Garvin, David F.; Gu, Yong-Qiang; Hasterok, Robert Crop Science, Vol. 48, Issue Supplement_1 https://doi.org/10.2135/cropsci2007.06.0332tpg	journal	January 2008
Supplemental Material for Wilson et al., 2018 Wilson, Pip; Streich, Jared C.; Murray, Kevin Figshare https://doi.org/10.25386/genetics.7345160	collection	January 2018
Memory of the vernalized state in plants including the model grass Brachypodium distachyon Woods, Daniel P.; Ream, Thomas S.; Amasino, Richard M. Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00099	journal	March 2014
Identification and Roles of Photosystem II Assembly, Stability, and Repair Factors in Arabidopsis Lu, Yan Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00168	journal	February 2016
QTL Hotspots for Early Vigor and Related Traits under Dry Direct-Seeded System in Rice (Oryza sativa L.) Singh, Uma M.; Yadav, Shailesh; Dixit, Shilpi Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00286	journal	March 2017
Population Structure in the Model Grass Is Highly Correlated with Flowering Differences across Broad Geographic Areas Tyler, Ludmila; Lee, Scott J.; Young, Nelson D. The Plant Genome, Vol. 9, Issue 2 https://doi.org/10.3835/plantgenome2015.08.0074	journal	January 2016
Updated taxonomic descriptions, iconography, and habitat preferences of Brachypodium distachyon, B. stacei, and B. hybridum (Poaceae) [Updated taxonomic descriptions, iconography, and habitat preferences of Brachypodium distachyon, B. stacei, and B. hybridum (Poaceae)] Catalán, Pilar; López-Álvarez, Diana; Bellosta, Cristina Anales del Jardín Botánico de Madrid, Vol. 73, Issue 1 https://doi.org/10.3989/ajbm.2428	journal	March 2016
GENOTYPIC DIFFERENCES IN DARK RESPIRATION OF MATURE LEAVES IN WINTER WHEAT ( Triticum aestivum L.) Winzeler, M.; McCULLOUGH, D. E.; Hunt, L. A. Canadian Journal of Plant Science, Vol. 68, Issue 3 https://doi.org/10.4141/cjps88-080	journal	July 1988
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data Li, Heng arXiv https://doi.org/10.48550/arxiv.1203.6372	text	January 2012
Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure Gordon, Sean P.; Contreras-Moreira, Bruno; Woods, Daniel P. Nature Publishing Group https://doi.org/10.5167/uzh-148888	text	January 2017
Frequent gene movement and pseudogene evolution is common to the large and complex genomes of wheat, barley, and their relatives Wicker, Thomas; Mayer, K. F. X.; Gundlach, H. American Society of Plant Physiologists https://doi.org/10.5167/uzh-53887	text	January 2011
The combination of gas-phase fluorophore technology and automation to enable high-throughput analysis of plant respiration Scafaro, Andrew; Negrini, A.; OâLeary, Brendan figshare https://doi.org/10.6084/m9.figshare.c.3723052.v1	collection	January 2017
Environmental isolation explains Iberian genetic diversity in the highly homozygous model grass Brachypodium distachyon Marques, Isabel; Shiposha, Valeriia; Lรณpez-Alvarez, Diana Figshare https://doi.org/10.6084/m9.figshare.c.3804565.v1	collection	January 2017

Cited By (2)

Extending the Genotype in Brachypodium by Including DNA Methylation Reveals a Joint Contribution with Genetics on Adaptive Traits Eichten, Steven R.; Srivastava, Akanksha; Reddiex, Adam J. G3 Genes\|Genomes\|Genetics, Vol. 10, Issue 5 https://doi.org/10.1534/g3.120.401189	journal	May 2020
Genetic Variation for Seed Metabolite Levels in Brachypodium distachyon Onda, Yoshihiko; Inoue, Komaki; Sawada, Yuji International Journal of Molecular Sciences, Vol. 20, Issue 9 https://doi.org/10.3390/ijms20092348	journal	May 2019

Linked Research (2)

Similar Records

Genetic Architecture of Flowering-Time Variation in Brachypodium distachyon

Journal Article · 2016 · Plant Physiology (Bethesda) · OSTI ID:1379644

Woods, Daniel P.; Bednarek, Ryland; Bouché, Frédéric; +4 more

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

Journal Article · 2016 · The Plant Genome · OSTI ID:1312966

Tyler, Ludmila; Lee, Scott J.; Young, Nelson D.; +8 more

Cell wall composition and biomass recalcitrance differences within a genotypically diverse set of Brachypodium distachyon inbred lines

Journal Article · 2016 · Frontiers in Plant Science · OSTI ID:1285953

Cass, Cynthia L.; Lavell, Anastasiya A.; Santoro, Nicholas; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES