Genome‐wide scans of selection highlight the impact of biotic and abiotic constraints in natural populations of the model grass Brachypodium distachyon

Bourgeois, Yann; Stritt, Christoph; Walser, Jean‐Claude; Gordon, Sean P.; Vogel, John P.; Roulin, Anne C.

doi:10.1111/tpj.14042

Title: Genome‐wide scans of selection highlight the impact of biotic and abiotic constraints in natural populations of the model grass Brachypodium distachyon

Journal Article · Sat Sep 01 00:00:00 EDT 2018 · The Plant Journal

DOI:https://doi.org/10.1111/tpj.14042· OSTI ID:1468356

Bourgeois, Yann ^[1]; Stritt, Christoph ^[2]; Walser, Jean‐Claude ^[3]; Gordon, Sean P. ^[4];

^[4]; Roulin, Anne C. ^[2]

New York University Abu Dhabi PO Box 129188 Saadiyat Island, Abu Dhabi United Arab Emirates
Institute of Plant and Microbial Biology University of Zürich Zollikerstrasse 107 8008 Zürich Switzerland
Genetic Diversity Centre ETH Zürich Universitätstrasse 16 Zurich Switzerland
DOE Joint Genome Institute Walnut Creek CA 94598 USA

Summary Grasses are essential plants for ecosystem functioning. Quantifying the selective pressures that act on natural variation in grass species is therefore essential regarding biodiversity maintenance. In this study, we investigate the selection pressures that act on two distinct populations of the grass model Brachypodium distachyon without prior knowledge about the traits under selection. We took advantage of whole‐genome sequencing data produced for 44 natural accessions of B. distachyon and used complementary genome‐wide selection scans ( GWSS ) methods to detect genomic regions under balancing and positive selection. We show that selection is shaping genetic diversity at multiple temporal and spatial scales in this species, and affects different genomic regions across the two populations. Gene ontology annotation of candidate genes reveals that pathogens may constitute important factors of positive and balancing selection in B. distachyon . We eventually cross‐validated our results with quantitative trait locus data available for leaf‐rust resistance in this species and demonstrate that, when paired with classical trait mapping, GWSS can help pinpointing candidate genes for further molecular validation. Thanks to a near base‐perfect reference genome and the large collection of freely available natural accessions collected across its natural range, B. distachyon appears as a prime system for studies in ecology, population genomics and evolutionary biology.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: DE‐AC02‐05CH11231

OSTI ID:: 1468356

Journal Information:: The Plant Journal, Journal Name: The Plant Journal Vol. 96 Journal Issue: 2; ISSN 0960-7412

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 13 works

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References (95)

Diversity of Puccinia striiformis on Cereals and Grasses Hovmøller, Mogens S.; Sørensen, Chris K.; Walter, Stephanie Annual Review of Phytopathology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-phyto-072910-095230	journal	September 2011
Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae) Manzaneda, Antonio J.; Rey, Pedro J.; Bastida, Jesús M. New Phytologist, Vol. 193, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03988.x	journal	December 2011
Recent Activity in Expanding Populations and Purifying Selection Have Shaped Transposable Element Landscapes across Natural Accessions of the Mediterranean Grass Brachypodium distachyon Stritt, Christoph; Gordon, Sean P.; Wicker, Thomas Genome Biology and Evolution, Vol. 10, Issue 1 https://doi.org/10.1093/gbe/evx276	journal	December 2017
Evolution and Conservation of Plant NLR Functions Jacob, Florence; Vernaldi, Saskia; Maekawa, Takaki Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00297	journal	January 2013
Fast model-based estimation of ancestry in unrelated individuals Alexander, D. H.; Novembre, J.; Lange, K. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.094052.109	journal	July 2009
Environmental niche variation and evolutionary diversification of the Brachypodium distachyon grass complex species in their native circum-Mediterranean range Lopez-Alvarez, D.; Manzaneda, A. J.; Rey, P. J. American Journal of Botany, Vol. 102, Issue 7 https://doi.org/10.3732/ajb.1500128	journal	July 2015
The Plant Cell Reviews Plant Immunity: Receptor-Like Kinases, ROS-RLK Crosstalk, Quantitative Resistance, and the Growth/Defense Trade-Off Eckardt, Nancy A. The Plant Cell, Vol. 29, Issue 4 https://doi.org/10.1105/tpc.17.00289	journal	April 2017
Genome-wide analysis of signatures of selection in populations of African honey bees (Apis mellifera) using new web-based tools Fuller, Zachary L.; Niño, Elina L.; Patch, Harland M. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1712-0	journal	July 2015
Selection upon Genome Architecture: Conservation of Functional Neighborhoods with Changing Genes Al-Shahrour, Fátima; Minguez, Pablo; Marqués-Bonet, Tomás PLoS Computational Biology, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pcbi.1000953	journal	October 2010
Rapid Decline of a Grassland System and Its Ecological and Conservation Implications Ceballos, Gerardo; Davidson, Ana; List, Rurik PLoS ONE, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pone.0008562	journal	January 2010
Human influence lowers plant genetic diversity in communities with extinction debt Helm, Aveliina; Oja, Tatjana; Saar, Liina Journal of Ecology, Vol. 97, Issue 6 https://doi.org/10.1111/j.1365-2745.2009.01572.x	journal	November 2009
Genome-Wide Distribution, Organisation and Functional Characterization of Disease Resistance and Defence Response Genes across Rice Species Singh, Sangeeta; Chand, Suresh; Singh, N. K. PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0125964	journal	April 2015
Genomic variability as a driver of plant–pathogen coevolution? Karasov, Talia L.; Horton, Matthew W.; Bergelson, Joy Current Opinion in Plant Biology, Vol. 18 https://doi.org/10.1016/j.pbi.2013.12.003	journal	April 2014
Ecological genomics of local adaptation Savolainen, Outi; Lascoux, Martin; Merilä, Juha Nature Reviews Genetics, Vol. 14, Issue 11 https://doi.org/10.1038/nrg3522	journal	October 2013
Comparative analysis of the cold acclimation and freezing tolerance capacities of seven diploid Brachypodium distachyon accessions Colton-Gagnon, Katia; Ali-Benali, Mohamed Ali; Mayer, Boris F. Annals of Botany, Vol. 113, Issue 4 https://doi.org/10.1093/aob/mct283	journal	December 2013
Who believes in whole-genome scans for selection? Hermisson, J. Heredity, Vol. 103, Issue 4 https://doi.org/10.1038/hdy.2009.101	journal	August 2009
Signatures of Environmental Genetic Adaptation Pinpoint Pathogens as the Main Selective Pressure through Human Evolution Fumagalli, Matteo; Sironi, Manuela; Pozzoli, Uberto PLoS Genetics, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pgen.1002355	journal	November 2011
Size-related deterioration of semi-natural grassland fragments in Sweden Kiviniemi, Katariina; Eriksson, Ove Diversity Distributions, Vol. 8, Issue 1 https://doi.org/10.1046/j.1366-9516.2001.00125.x	journal	January 2002
Targeting environmental adaptation in the monocot model Brachypodium distachyon: a multi-faceted approach Dell’Acqua, Matteo; Zuccolo, Andrea; Tuna, Metin BMC Genomics, Vol. 15, Issue 1 https://doi.org/10.1186/1471-2164-15-801	journal	January 2014
Signatures of balancing selection are maintained at disease resistance loci following mating system evolution and a population bottleneck in the genus Capsella Gos, Gesseca; Slotte, Tanja; Wright, Stephen I. BMC Evolutionary Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2148-12-152	journal	January 2012
The Brachypodium distachyon BdWRKY36 gene confers tolerance to drought stress in transgenic tobacco plants Sun, Jiutong; Hu, Wei; Zhou, Run Plant Cell Reports, Vol. 34, Issue 1 https://doi.org/10.1007/s00299-014-1684-6	journal	September 2014
Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits Stinchcombe, J. R.; Hoekstra, H. E. Heredity, Vol. 100, Issue 2 https://doi.org/10.1038/sj.hdy.6800937	journal	February 2007
The Stripe Rust Resistance Gene Yr10 Encodes an Evolutionary-Conserved and Unique CC–NBS–LRR Sequence in Wheat Liu, Wei; Frick, Michele; Huel, Réné Molecular Plant, Vol. 7, Issue 12 https://doi.org/10.1093/mp/ssu112	journal	December 2014
Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives Wu, Qiong; Han, Ting-Shen; Chen, Xi Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1342-8	journal	November 2017
The genetic legacy of the Quaternary ice ages Hewitt, Godfrey Nature, Vol. 405, Issue 6789 https://doi.org/10.1038/35016000	journal	June 2000
Evolution of Grasses and Grassland Ecosystems Strömberg, Caroline A. E. Annual Review of Earth and Planetary Sciences, Vol. 39, Issue 1 https://doi.org/10.1146/annurev-earth-040809-152402	journal	May 2011
The genomic basis of adaptation in plants Flood, Pádraic J.; Hancock, Angela M. Current Opinion in Plant Biology, Vol. 36 https://doi.org/10.1016/j.pbi.2017.02.003	journal	April 2017
Evaluating the performance of selection scans to detect selective sweeps in domestic dogs Schlamp, Florencia; van der Made, Julian; Stambler, Rebecca Molecular Ecology, Vol. 25, Issue 1 https://doi.org/10.1111/mec.13485	journal	December 2015
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
Sambamba: fast processing of NGS alignment formats Tarasov, Artem; Vilella, Albert J.; Cuppen, Edwin Bioinformatics, Vol. 31, Issue 12 https://doi.org/10.1093/bioinformatics/btv098	journal	February 2015
Parasitism drives host genome evolution: Insights from the Pasteuria ramosa - Daphnia magna system : BRIEF COMMUNICATION Bourgeois, Yann; Roulin, Anne C.; Müller, Kristina Evolution, Vol. 71, Issue 4 https://doi.org/10.1111/evo.13209	journal	March 2017
Protein phosphorylation in plant immunity: insights into the regulation of pattern recognition receptor-mediated signaling Park, Chang-Jin; Caddell, Daniel F.; Ronald, Pamela C. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00177	journal	January 2012
The variant call format and VCFtools Danecek, P.; Auton, A.; Abecasis, G. Bioinformatics, Vol. 27, Issue 15 https://doi.org/10.1093/bioinformatics/btr330	journal	June 2011
Structure–function analysis of the NB-ARC domain of plant disease resistance proteins van Ooijen, Gerben; Mayr, Gabriele; Kasiem, Mobien M. A. Journal of Experimental Botany, Vol. 59, Issue 6 https://doi.org/10.1093/jxb/ern045	journal	April 2008
Trapping the intruder — immune receptor domain fusions provide new molecular leads for improving disease resistance in plants Krattinger, Simon G.; Keller, Beat Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0891-6	journal	February 2016
Natural variation of drought response in Brachypodium distachyon Luo, Na; Liu, Jianxiu; Yu, Xiaoqing Physiologia Plantarum, Vol. 141, Issue 1 https://doi.org/10.1111/j.1399-3054.2010.01413.x	journal	October 2010
Diversity and evolution of Rp1 rust resistance genes in four maize lines Chavan, Suchitra; Gray, Judy; Smith, Shavannor M. Theoretical and Applied Genetics, Vol. 128, Issue 5 https://doi.org/10.1007/s00122-015-2484-2	journal	March 2015
S/HIC: Robust Identification of Soft and Hard Sweeps Using Machine Learning Schrider, Daniel R.; Kern, Andrew D. PLOS Genetics, Vol. 12, Issue 3 https://doi.org/10.1371/journal.pgen.1005928	journal	March 2016
Genetic and forma specialis diversity in Blumeria graminis of cereals and its implications for host-pathogen co-evolution Wyand, Rebecca A.; Brown, James K. M. Molecular Plant Pathology, Vol. 4, Issue 3 https://doi.org/10.1046/j.1364-3703.2003.00167.x	journal	May 2003
Advantageous diversity maintained by balancing selection in humans Key, Felix M.; Teixeira, João C.; de Filippo, Cesare Current Opinion in Genetics & Development, Vol. 29 https://doi.org/10.1016/j.gde.2014.08.001	journal	December 2014
Brachypodium distachyon: making hay with a wild grass Opanowicz, Magdalena; Vain, Philippe; Draper, John Trends in Plant Science, Vol. 13, Issue 4 https://doi.org/10.1016/j.tplants.2008.01.007	journal	April 2008
Cadmium and lead contamination in vegetables collected from industrial, traffic and rural areas in Bursa Province, Turkey Mor, F.; Ceylan, S. Food Additives & Contaminants: Part A, Vol. 25, Issue 5 https://doi.org/10.1080/02652030701691531	journal	May 2008
Nonhost resistance to rust pathogens â€“ a continuation of continua Bettgenhaeuser, Jan; Gilbert, Brian; Ayliffe, Michael Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00664	journal	December 2014
QTLs for resistance to the false brome rust Puccinia brachypodii in the model grass Brachypodium distachyon L. Barbieri, Mirko; Marcel, Thierry C.; Niks, Rients E. Genome, Vol. 55, Issue 2 https://doi.org/10.1139/g2012-001	journal	February 2012
Genome-Wide Inference of Ancestral Recombination Graphs Rasmussen, Matthew D.; Hubisz, Melissa J.; Gronau, Ilan PLoS Genetics, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pgen.1004342	journal	May 2014
Molecular Signatures of Natural Selection Nielsen, Rasmus Annual Review of Genetics, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.genet.39.073003.112420	journal	December 2005
Discoal: flexible coalescent simulations with selection Kern, Andrew D.; Schrider, Daniel R. Bioinformatics, Vol. 32, Issue 24 https://doi.org/10.1093/bioinformatics/btw556	journal	August 2016
A New Approach for Using Genome Scans to Detect Recent Positive Selection in the Human Genome Tang, Kun; Thornton, Kevin R.; Stoneking, Mark PLoS Biology, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pbio.0050171	journal	June 2007
Evolutionary and ecological functional genomics Feder, Martin E.; Mitchell-Olds, Thomas Nature Reviews Genetics, Vol. 4, Issue 8 https://doi.org/10.1038/nrg1128	journal	August 2003
rehh: an R package to detect footprints of selection in genome-wide SNP data from haplotype structure Gautier, Mathieu; Vitalis, Renaud Bioinformatics, Vol. 28, Issue 8 https://doi.org/10.1093/bioinformatics/bts115	journal	March 2012
Balancing Selection and Its Effects on Sequences in Nearby Genome Regions Charlesworth, Deborah PLoS Genetics, Vol. 2, Issue 4 https://doi.org/10.1371/journal.pgen.0020064	journal	January 2006
Species-specific duplications of NBS-encoding genes in Chinese chestnut (Castanea mollissima) Zhong, Yan; Li, Yingjun; Huang, Kaihui Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16638	journal	November 2015
Circos: An information aesthetic for comparative genomics Krzywinski, M.; Schein, J.; Birol, I. Genome Research, Vol. 19, Issue 9 https://doi.org/10.1101/gr.092759.109	journal	June 2009
Evolution and Distribution of Grasses Clayton, W. D. Annals of the Missouri Botanical Garden, Vol. 68, Issue 1 https://doi.org/10.2307/2398808	journal	January 1981
Molecular genetics and evolution of disease resistance in cereals Krattinger, Simon G.; Keller, Beat New Phytologist, Vol. 212, Issue 2 https://doi.org/10.1111/nph.14097	journal	July 2016
Detecting balancing selection in genomes: limits and prospects Fijarczyk, Anna; Babik, Wiesław Molecular Ecology, Vol. 24, Issue 14 https://doi.org/10.1111/mec.13226	journal	June 2015
PopGenome: An Efficient Swiss Army Knife for Population Genomic Analyses in R Pfeifer, Bastian; Wittelsbürger, Ulrich; Ramos-Onsins, Sebastian E. Molecular Biology and Evolution, Vol. 31, Issue 7 https://doi.org/10.1093/molbev/msu136	journal	April 2014
Detecting local adaptation in widespread grassland species ? the importance of scale and local plant community Bischoff, Armin; CrÉMieux, LisÈLe; Smilauerova, Marie Journal of Ecology, Vol. 94, Issue 6 https://doi.org/10.1111/j.1365-2745.2006.01174.x	journal	November 2006
Enhancing the crops to feed the poor Huang, Jikun; Pray, Carl; Rozelle, Scott Nature, Vol. 418, Issue 6898 https://doi.org/10.1038/nature01015	journal	August 2002
Clusters of Resistance Genes in Plants Evolve by Divergent Selection and a Birth-and-Death Process Michelmore, Richard W.; Meyers, Blake C. Genome Research, Vol. 8, Issue 11 https://doi.org/10.1101/gr.8.11.1113	journal	November 1998
diploS/HIC: An Updated Approach to Classifying Selective Sweeps Kern, Andrew D.; Schrider, Daniel R. G3: Genes\|Genomes\|Genetics, Vol. 8, Issue 6 https://doi.org/10.1534/g3.118.200262	journal	April 2018
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
Southern European glacial refugia: A tale of tales Feliner, Gonzalo Nieto TAXON, Vol. 60, Issue 2 https://doi.org/10.1002/tax.602007	journal	April 2011
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research Conesa, A.; Gotz, S.; Garcia-Gomez, J. M. Bioinformatics, Vol. 21, Issue 18 https://doi.org/10.1093/bioinformatics/bti610	journal	August 2005
Origin and Domestication of the Fungal Wheat Pathogen Mycosphaerella graminicola via Sympatric Speciation Stukenbrock, E. H.; Banke, S.; Javan-Nikkhah, M. Molecular Biology and Evolution, Vol. 24, Issue 2 https://doi.org/10.1093/molbev/msl169	journal	November 2006
Post-glacial re-colonization of European biota Hewitt, Godfrey M. Biological Journal of the Linnean Society, Vol. 68, Issue 1-2 https://doi.org/10.1111/j.1095-8312.1999.tb01160.x	journal	September 1999
Using GOstats to test gene lists for GO term association Falcon, S.; Gentleman, R. Bioinformatics, Vol. 23, Issue 2 https://doi.org/10.1093/bioinformatics/btl567	journal	November 2006
Genome-wide association studies and prediction of 17 traits related to phenology, biomass and cell wall composition in the energy grass Miscanthus sinensis Slavov, Gancho T.; Nipper, Rick; Robson, Paul New Phytologist, Vol. 201, Issue 4 https://doi.org/10.1111/nph.12621	journal	December 2013
The impact of linked selection on plant genomic variation Slotte, T. Briefings in Functional Genomics, Vol. 13, Issue 4 https://doi.org/10.1093/bfgp/elu009	journal	April 2014
A Photoreceptor Contributes to the Natural Variation of Diapause Induction in Daphnia magna Roulin, Anne C.; Bourgeois, Yann; Stiefel, Urs Molecular Biology and Evolution, Vol. 33, Issue 12 https://doi.org/10.1093/molbev/msw200	journal	September 2016
The plasticity of NBS resistance genes in sorghum is driven by multiple evolutionary processes Mace, Emma; Tai, Shuaishuai; Innes, David BMC Plant Biology, Vol. 14, Issue 1 https://doi.org/10.1186/s12870-014-0253-z	journal	September 2014
The two-speed genomes of filamentous pathogens: waltz with plants Dong, Suomeng; Raffaele, Sylvain; Kamoun, Sophien Current Opinion in Genetics & Development, Vol. 35 https://doi.org/10.1016/j.gde.2015.09.001	journal	December 2015
Recognition events and host–pathogen co-evolution in gene-for-gene resistance to flax rust Dodds, Peter; Thrall, Peter Functional Plant Biology, Vol. 36, Issue 5 https://doi.org/10.1071/FP08320	journal	January 2009
Identifying targets and agents of selection: innovative methods to evaluate the processes that contribute to local adaptation Wadgymar, Susana M.; Lowry, David B.; Gould, Billie A. Methods in Ecology and Evolution, Vol. 8, Issue 6 https://doi.org/10.1111/2041-210X.12777	journal	June 2017
Comparison of a high-density genetic linkage map to genome features in the model grass Brachypodium distachyon Huo, Naxin; Garvin, David F.; You, Frank M. Theoretical and Applied Genetics, Vol. 123, Issue 3 https://doi.org/10.1007/s00122-011-1598-4	journal	May 2011
Vegetation of Eurasia from the last glacial maximum to present: Key biogeographic patterns Binney, Heather; Edwards, Mary; Macias-Fauria, Marc Quaternary Science Reviews, Vol. 157 https://doi.org/10.1016/j.quascirev.2016.11.022	journal	February 2017
A Critical Assessment of Storytelling: Gene Ontology Categories and the Importance of Validating Genomic Scans Pavlidis, Pavlos; Jensen, Jeffrey D.; Stephan, Wolfgang Molecular Biology and Evolution, Vol. 29, Issue 10 https://doi.org/10.1093/molbev/mss136	journal	July 2012
Testing for local adaptation in Avena barbata : a classic example of ecotypic divergence Latta, Robert G. Molecular Ecology, Vol. 18, Issue 18 https://doi.org/10.1111/j.1365-294X.2009.04302.x	journal	September 2009
The Scale of Population Structure in Arabidopsis thaliana Platt, Alexander; Horton, Matthew; Huang, Yu S. PLoS Genetics, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pgen.1000843	journal	February 2010
Robust and scalable inference of population history from hundreds of unphased whole genomes Terhorst, Jonathan; Kamm, John A.; Song, Yun S. Nature Genetics, Vol. 49, Issue 2 https://doi.org/10.1038/ng.3748	journal	December 2016
BEDTools: a flexible suite of utilities for comparing genomic features Quinlan, Aaron R.; Hall, Ira M. Bioinformatics, Vol. 26, Issue 6 https://doi.org/10.1093/bioinformatics/btq033	journal	January 2010
Serine/Threonine Protein Phosphatases type 2A and their roles in stress signaling País, Silvia Marina; Téllez-Iñón, María Teresa; Capiati, Daniela Andrea Plant Signaling & Behavior, Vol. 4, Issue 11 https://doi.org/10.4161/psb.4.11.9783	journal	November 2009
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
Rapid and Accurate Haplotype Phasing and Missing-Data Inference for Whole-Genome Association Studies By Use of Localized Haplotype Clustering Browning, Sharon R.; Browning, Brian L. The American Journal of Human Genetics, Vol. 81, Issue 5 https://doi.org/10.1086/521987	journal	November 2007
Glacial refugia of temperate trees in Europe: insights from species distribution modelling Svenning, Jens-Christian; Normand, Signe; Kageyama, Masa Journal of Ecology, Vol. 96, Issue 6 https://doi.org/10.1111/j.1365-2745.2008.01422.x	journal	November 2008
Determination of lead, cadmium and copper in roadside soil and plants in Elazig, Turkey Bakirdere, Sezgin; Yaman, Mehmet Environmental Monitoring and Assessment, Vol. 136, Issue 1-3 https://doi.org/10.1007/s10661-007-9695-1	journal	March 2007
Plant-Parasite Coevolution: Bridging the Gap between Genetics and Ecology Brown, James K. M.; Tellier, Aurélien Annual Review of Phytopathology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev-phyto-072910-095301	journal	September 2011
Patterns of Positive Selection in the Complete NBS-LRR Gene Family of Arabidopsis thaliana Mondragon-Palomino, M. Genome Research, Vol. 12, Issue 9 https://doi.org/10.1101/gr.159402	journal	September 2002
Which evolutionary processes influence natural genetic variation for phenotypic traits? Mitchell-Olds, Thomas; Willis, John H.; Goldstein, David B. Nature Reviews Genetics, Vol. 8, Issue 11 https://doi.org/10.1038/nrg2207	journal	November 2007
Managing water resources for crop production Wallace, J. S.; Batchelor, C. H. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 352, Issue 1356 https://doi.org/10.1098/rstb.1997.0073	journal	July 1997
Genomic signatures of selection at linked sites: unifying the disparity among species Cutter, Asher D.; Payseur, Bret A. Nature Reviews Genetics, Vol. 14, Issue 4 https://doi.org/10.1038/nrg3425	journal	March 2013
Regulation of pattern recognition receptor signalling in plants Couto, Daniel; Zipfel, Cyril Nature Reviews Immunology, Vol. 16, Issue 9 https://doi.org/10.1038/nri.2016.77	journal	August 2016
On the importance of balancing selection in plants Delph, Lynda F.; Kelly, John K. New Phytologist, Vol. 201, Issue 1 https://doi.org/10.1111/nph.12441	journal	August 2013
SweeD: Likelihood-Based Detection of Selective Sweeps in Thousands of Genomes Pavlidis, Pavlos; Živković, Daniel; Stamatakis, Alexandros Molecular Biology and Evolution, Vol. 30, Issue 9 https://doi.org/10.1093/molbev/mst112	journal	June 2013
Genome diversity in Brachypodium distachyon: deep sequencing of highly diverse inbred lines Gordon, Sean P.; Priest, Henry; Des Marais, David L. The Plant Journal, Vol. 79, Issue 3 https://doi.org/10.1111/tpj.12569	journal	July 2014

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