Browse by volume Browse by section Browse by topic Browse by conference

Section: Genomics
Topic: Genetics/Genomics, Evolution, Population biology

The demographic history of the wild crop relative Brachypodium distachyon is shaped by distinct past and present ecological niches

Minadakis, Nikolaos1 ; Williams, Hefin2 ; Horvath, Robert1 ; Caković, Danka3; Stritt, Christoph4 ; Thieme, Michael1 ; Bourgeois, Yann5, 6 ; Roulin, Anne C.1  
1 Department of Plant and Microbial Biology, University of Zurich, Zollikerstrasse 107, 8008 Zürich, Switzerland
2 Department of Life Sciences, Aberystwyth University, Aberystwyth, Wales
3 Department of Biology, University of Montenegro, Džordža Vašingtona bb, 81000 Podgorica, Montenegro
4 Swiss Tropical and Public Health Institute, Kreuzstrasse 2, 4123 Allschwil, Switzerland
5 DIADE, University of Montpellier, CIRAD, IRD, Montpellier, France
6 University House, Winston Churchill Ave, Portsmouth PO1 2UP, United Kingdom

10.24072/pcjournal.319 - Peer Community Journal, Volume 3 (2023), article no. e84.

Get full text PDF Peer reviewed and recommended by PCI

Closely related to economically important crops, the grass Brachypodium distachyon has been originally established as a pivotal species for grass genomics but more recently flourished as a model for developmental biology. Grasses encompass more than 10,000 species and cover more than 40% of the world land area from tropical to temperate regions. Given that grasses also supply about a fifth of the world's dietary protein as cereal grains, unlocking the sources of phenotypic variation in B. distachyon is hence of prime interest in fundamental and applied research in agronomy, ecology and evolution. We present here the B. distachyon diversity panel, which encompasses 332 fully sequenced accessions covering the whole species distribution from Spain to Iraq. By combining population genetics, niche modeling and landscape genomics, we suggest that B. distachyon recolonized Europe and the Middle East following the last glacial maximum. Consequently, the species faced new environmental conditions which led to clear associations between bioclimatic variables and genetic factors as well as footprints of positive selection in the genome. Altogether, this genomic resource offers a powerful alternative to Arabidopsis thaliana to investigate the genetic bases of adaptation and phenotypic plasticity in plants and more specifically in monocots.

Published online:
DOI: 10.24072/pcjournal.319
Type: Research article
Keywords: genetic diversity, local adaptation, landscape genomics, GEA, grass, Brachypodium distachyon
Minadakis, Nikolaos 1; Williams, Hefin 2; Horvath, Robert 1; Caković, Danka 3; Stritt, Christoph 4; Thieme, Michael 1; Bourgeois, Yann 5, 6; Roulin, Anne C. 1

1 Department of Plant and Microbial Biology, University of Zurich, Zollikerstrasse 107, 8008 Zürich, Switzerland
2 Department of Life Sciences, Aberystwyth University, Aberystwyth, Wales
3 Department of Biology, University of Montenegro, Džordža Vašingtona bb, 81000 Podgorica, Montenegro
4 Swiss Tropical and Public Health Institute, Kreuzstrasse 2, 4123 Allschwil, Switzerland
5 DIADE, University of Montpellier, CIRAD, IRD, Montpellier, France
6 University House, Winston Churchill Ave, Portsmouth PO1 2UP, United Kingdom
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_319,
     author = {Minadakis, Nikolaos and Williams, Hefin and Horvath, Robert and Cakovi\'c, Danka and Stritt, Christoph and Thieme, Michael and Bourgeois, Yann and Roulin, Anne C.},
     title = {The demographic history of the wild crop relative {\protect\emph{Brachypodium} distachyon} is shaped by distinct past and present ecological niches},
     journal = {Peer Community Journal},
     eid = {e84},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.319},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.319/}
}
TY  - JOUR
AU  - Minadakis, Nikolaos
AU  - Williams, Hefin
AU  - Horvath, Robert
AU  - Caković, Danka
AU  - Stritt, Christoph
AU  - Thieme, Michael
AU  - Bourgeois, Yann
AU  - Roulin, Anne C.
TI  - The demographic history of the wild crop relative Brachypodium distachyon is shaped by distinct past and present ecological niches
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.319/
DO  - 10.24072/pcjournal.319
LA  - en
ID  - 10_24072_pcjournal_319
ER  - 
%0 Journal Article
%A Minadakis, Nikolaos
%A Williams, Hefin
%A Horvath, Robert
%A Caković, Danka
%A Stritt, Christoph
%A Thieme, Michael
%A Bourgeois, Yann
%A Roulin, Anne C.
%T The demographic history of the wild crop relative Brachypodium distachyon is shaped by distinct past and present ecological niches
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.319/
%R 10.24072/pcjournal.319
%G en
%F 10_24072_pcjournal_319
Minadakis, Nikolaos; Williams, Hefin; Horvath, Robert; Caković, Danka; Stritt, Christoph; Thieme, Michael; Bourgeois, Yann; Roulin, Anne C. The demographic history of the wild crop relative Brachypodium distachyon is shaped by distinct past and present ecological niches. Peer Community Journal, Volume 3 (2023), article  no. e84. doi : 10.24072/pcjournal.319. https://peercommunityjournal.org/articles/10.24072/pcjournal.319/

Peer reviewed and recommended by PCI : 10.24072/pci.genomics.100251

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Albers, P. K.; McVean, G. Dating genomic variants and shared ancestry in population-scale sequencing data, PLOS Biology, Volume 18 (2020) no. 1 | DOI

[2] Anderson D; Burnham K. Model Selection and Multimodel Inference. A Practical Information-Theoretic Approach. 2nd ed., Springer New York, New York, NY, 2004, 488 pages | DOI

[3] Barbieri, M.; Marcel, T. C.; Niks, R. E.; Francia, E.; Pasquariello, M.; Mazzamurro, V.; Garvin, D. F.; Pecchioni, N. QTLs for resistance to the false brome rust Puccinia brachypodii in the model grass Brachypodium distachyon L., Genome, Volume 55 (2012) no. 2, pp. 152-163 | DOI

[4] Beale, C. M.; Lennon, J. J.; Gimona, A. Opening the climate envelope reveals no macroscale associations with climate in European birds, Proceedings of the National Academy of Sciences, Volume 105 (2008) no. 39, pp. 14908-14912 | DOI

[5] Benjamini, Y.; Hochberg, Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing, Journal of the Royal Statistical Society: Series B (Methodological), Volume 57 (1995) no. 1, pp. 289-300 | DOI

[6] Binney, H.; Edwards, M.; Macias-Fauria, M.; Lozhkin, A.; Anderson, P.; Kaplan, J. O.; Andreev, A.; Bezrukova, E.; Blyakharchuk, T.; Jankovska, V.; Khazina, I.; Krivonogov, S.; Kremenetski, K.; Nield, J.; Novenko, E.; Ryabogina, N.; Solovieva, N.; Willis, K.; Zernitskaya, V. Vegetation of Eurasia from the last glacial maximum to present: Key biogeographic patterns, Quaternary Science Reviews, Volume 157 (2017), pp. 80-97 | DOI

[7] Bouché, F.; Woods, D. P.; Linden, J.; Li, W.; Mayer, K. S.; Amasino, R. M.; Périlleux, C. EARLY FLOWERING 3 and Photoperiod Sensing in Brachypodium distachyon, Frontiers in Plant Science, Volume 12 (2022) | DOI

[8] Bourgeois, Y.; Stritt, C.; Walser, J.; Gordon, S. P.; Vogel, J. P.; Roulin, A. C. Genome‐wide scans of selection highlight the impact of biotic and abiotic constraints in natural populations of the model grass Brachypodium distachyon, The Plant Journal, Volume 96 (2018) no. 2, pp. 438-451 | DOI

[9] Casacuberta, J. Natural variation and adaptation in Brachypodium distachyon, Peer Community in Genomics (2023) | DOI

[10] Casimiro-Soriguer, R.; Talavera, M.; Balao, F.; Terrab, A.; Herrera, J.; Talavera, S. Phylogeny and genetic structure of Erophaca (Leguminosae), a East–West Mediterranean disjunct genus from the Tertiary, Molecular Phylogenetics and Evolution, Volume 56 (2010) no. 1, pp. 441-450 | DOI

[11] Catalán, P.; López-Álvarez, D.; Bellosta, C.; Villar, L. Updated taxonomic descriptions, iconography, and habitat preferences of Brachypodium distachyon, B. stacei, and B. hybridum (Poaceae), Anales del Jardín Botánico de Madrid, Volume 73 (2016) no. 1 | DOI

[12] Coomey, J. H.; Sibout, R.; Hazen, S. P. Grass secondary cell walls, Brachypodium distachyon as a model for discovery, New Phytologist, Volume 227 (2020) no. 6, pp. 1649-1667 | DOI

[13] Dalmais, M.; Antelme, S.; Ho-Yue-Kuang, S.; Wang, Y.; Darracq, O.; d’Yvoire, M. B.; Cézard, L.; Légée, F.; Blondet, E.; Oria, N.; Troadec, C.; Brunaud, V.; Jouanin, L.; Höfte, H.; Bendahmane, A.; Lapierre, C.; Sibout, R. A TILLING Platform for Functional Genomics in Brachypodium distachyon, PLoS ONE, Volume 8 (2013) no. 6 | DOI

[14] Danecek, P.; Auton, A.; Abecasis, G.; Albers, C. A.; Banks, E.; DePristo, M. A.; Handsaker, R. E.; Lunter, G.; Marth, G. T.; Sherry, S. T.; McVean, G.; Durbin, R. The variant call format and VCFtools, Bioinformatics, Volume 27 (2011) no. 15, pp. 2156-2158 | DOI

[15] Davis, B. A. S.; Fasel, M.; Kaplan, J. O.; Russo, E.; Burke, A. The climate and vegetation of Europe, North Africa and the Middle East during the Last Glacial Maximum (21,000 years BP) based on pollen data, Clim. Past Discuss. [preprint] , 2022 (in review, 2022) | DOI

[16] Dell’Acqua, M.; Zuccolo, A.; Tuna, M.; Gianfranceschi, L.; Pè, M. E. Targeting environmental adaptation in the monocot model Brachypodium distachyon: a multi-faceted approach, BMC Genomics, Volume 15 (2014) no. 1 | DOI

[17] Des Marais, D. L.; Lasky, J. R.; Verslues, P. E.; Chang, T. Z.; Juenger, T. E. Interactive effects of water limitation and elevated temperature on the physiology, development and fitness of diverse accessions of Brachypodium distachyon, New Phytologist, Volume 214 (2017) no. 1, pp. 132-144 | DOI

[18] Durvasula, A.; Fulgione, A.; Gutaker, R. M.; Alacakaptan, S. I.; Flood, P. J.; Neto, C.; Tsuchimatsu, T.; Burbano, H. A.; Picó, F. X.; Alonso-Blanco, C.; Hancock, A. M. African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 20, pp. 5213-5218 | DOI

[19] Elith, J.; H. Graham, C.; P. Anderson, R.; Dudík, M.; Ferrier, S.; Guisan, A.; J. Hijmans, R.; Huettmann, F.; R. Leathwick, J.; Lehmann, A.; Li, J.; G. Lohmann, L.; A. Loiselle, B.; Manion, G.; Moritz, C.; Nakamura, M.; Nakazawa, Y.; McC. M. Overton, J.; Townsend Peterson, A.; J. Phillips, S.; Richardson, K.; Scachetti-Pereira, R.; E. Schapire, R.; Soberón, J.; Williams, S.; S. Wisz, M.; E. Zimmermann, N. Novel methods improve prediction of species’ distributions from occurrence data, Ecography, Volume 29 (2006) no. 2, pp. 129-151 | DOI

[20] Elith, J.; Phillips, S. J.; Hastie, T.; Dudík, M.; Chee, Y. E.; Yates, C. J. A statistical explanation of MaxEnt for ecologists, Diversity and Distributions, Volume 17 (2011) no. 1, pp. 43-57 | DOI

[21] Evanno, G.; Regnaut, S.; Goudet, J. Detecting the number of clusters of individuals using the software structure: a simulation study, Molecular Ecology, Volume 14 (2005) no. 8, pp. 2611-2620 | DOI

[22] Exposito-Alonso, M. Seasonal timing adaptation across the geographic range of Arabidopsis thaliana, Proceedings of the National Academy of Sciences, Volume 117 (2020) no. 18, pp. 9665-9667 | DOI

[23] Exposito-Alonso, M.; Burbano, H. A.; Bossdorf, O.; Nielsen, R.; Weigel, D. Natural selection on the Arabidopsis thaliana genome in present and future climates, Nature, Volume 573 (2019) no. 7772, pp. 126-129 | DOI

[24] Feliner, G. N. Southern European glacial refugia: A tale of tales, Taxon, Volume 60 (2011) no. 2, pp. 365-372 | DOI

[25] Feliner, G. N. Patterns and processes in plant phylogeography in the Mediterranean Basin. A review, Perspectives in Plant Ecology, Evolution and Systematics, Volume 16 (2014) no. 5, pp. 265-278 | DOI

[26] Fick, S. E.; Hijmans, R. J. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas, International Journal of Climatology, Volume 37 (2017) no. 12, pp. 4302-4315 | DOI

[27] Flouri, T.; Jiao, X.; Rannala, B.; Yang, Z. Species Tree Inference with BPP Using Genomic Sequences and the Multispecies Coalescent, Molecular Biology and Evolution, Volume 35 (2018) no. 10, pp. 2585-2593 | DOI

[28] Frichot, E.; François, O. LEA: An R package for landscape and ecological association studies, Methods in Ecology and Evolution, Volume 6 (2015) no. 8, pp. 925-929 | DOI

[29] Fulgione, A.; Koornneef, M.; Roux, F.; Hermisson, J.; Hancock, A. M. Madeiran Arabidopsis thaliana Reveals Ancient Long-Range Colonization and Clarifies Demography in Eurasia, Molecular Biology and Evolution, Volume 35 (2018) no. 3, pp. 564-574 | DOI

[30] Gamba, D.; Lorts, C.; Haile, A.; Sahay, S.; Lopez, L.; Xia, T.; Takou, M.; Kulesza, E.; Elango, D.; Kerby, J.; Yifru, M.; Bulafu, C. E.; Wondimu, T.; Glowacka, K.; Lasky, J. R. The genomics and physiology of abiotic stressors associated with global elevation gradients in Arabidopsis thaliana , bioRxiv | DOI

[31] Gautier, M. Genome-Wide Scan for Adaptive Divergence and Association with Population-Specific Covariates, Genetics, Volume 201 (2015) no. 4, pp. 1555-1579 | DOI

[32] Gautier, M.; Vitalis, R. rehh : an R package to detect footprints of selection in genome-wide SNP data from haplotype structure, Bioinformatics, Volume 28 (2012) no. 8, pp. 1176-1177 | DOI

[33] Gent, P. R.; Danabasoglu, G.; Donner, L. J.; Holland, M. M.; Hunke, E. C.; Jayne, S. R.; Lawrence, D. M.; Neale, R. B.; Rasch, P. J.; Vertenstein, M.; Worley, P. H.; Yang, Z.-L.; Zhang, M. The Community Climate System Model Version 4, Journal of Climate, Volume 24 (2011) no. 19, pp. 4973-4991 | DOI

[34] Giraldo, P.; Rodríguez-Quijano, M.; Vázquez, J. F.; Carrillo, J. M.; Benavente, E. Validation of microsatellite markers for cytotype discrimination in the model grass Brachypodium distachyon, Genome, Volume 55 (2012) no. 7, pp. 523-527 | DOI

[35] Gloss, A. D.; Vergnol, A.; Morton, T. C.; Laurin, P. J.; Roux, F.; Bergelson, J. Genome-wide association mapping within a local Arabidopsis thaliana population more fully reveals the genetic architecture for defensive metabolite diversity, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 377 (2022) no. 1855 | DOI

[36] Gordon, S. P.; Contreras-Moreira, B.; Levy, J. J.; Djamei, A.; Czedik-Eysenberg, A.; Tartaglio, V. S.; Session, A.; Martin, J.; Cartwright, A.; Katz, A.; Singan, V. R.; Goltsman, E.; Barry, K.; Dinh-Thi, V. H.; Chalhoub, B.; Diaz-Perez, A.; Sancho, R.; Lusinska, J.; Wolny, E.; Nibau, C.; Doonan, J. H.; Mur, L. A. J.; Plott, C.; Jenkins, J.; Hazen, S. P.; Lee, S. J.; Shu, S.; Goodstein, D.; Rokhsar, D.; Schmutz, J.; Hasterok, R.; Catalan, P.; Vogel, J. P. Gradual polyploid genome evolution revealed by pan-genomic analysis of Brachypodium hybridum and its diploid progenitors, Nature Communications, Volume 11 (2020) no. 1 | DOI

[37] Gordon, S. P.; Contreras-Moreira, B.; Woods, D. P.; Des Marais, D. L.; Burgess, D.; Shu, S.; Stritt, C.; Roulin, A. C.; Schackwitz, W.; Tyler, L.; Martin, J.; Lipzen, A.; Dochy, N.; Phillips, J.; Barry, K.; Geuten, K.; Budak, H.; Juenger, T. E.; Amasino, R.; Caicedo, A. L.; Goodstein, D.; Davidson, P.; Mur, L. A. J.; Figueroa, M.; Freeling, M.; Catalan, P.; Vogel, J. P. Extensive gene content variation in the Brachypodium distachyon pan-genome correlates with population structure, Nature Communications, Volume 8 (2017) no. 1 | DOI

[38] Groves, R. Temperate grasslands of the southern hemisphere In: Grasses Systematics and Evolution. Jacobs SWL and Everett J, eds, CSIRO Publishing, Melbourne (2000), pp. 3781-3791 (http://hdl.handle.net/102.100.100/207809?index=1)

[39] Günther, T.; Coop, G. Robust Identification of Local Adaptation from Allele Frequencies, Genetics, Volume 195 (2013) no. 1, pp. 205-220 | DOI

[40] Haberer, G.; Kamal, N.; Bauer, E.; Gundlach, H.; Fischer, I.; Seidel, M. A.; Spannagl, M.; Marcon, C.; Ruban, A.; Urbany, C.; Nemri, A.; Hochholdinger, F.; Ouzunova, M.; Houben, A.; Schön, C.-C.; Mayer, K. F. X. European maize genomes highlight intraspecies variation in repeat and gene content, Nature Genetics, Volume 52 (2020) no. 9, pp. 950-957 | DOI

[41] Hancock, A. M.; Brachi, B.; Faure, N.; Horton, M. W.; Jarymowycz, L. B.; Sperone, F. G.; Toomajian, C.; Roux, F.; Bergelson, J. Adaptation to Climate Across the Arabidopsis thaliana Genome, Science, Volume 334 (2011) no. 6052, pp. 83-86 | DOI

[42] Hasterok, R.; Catalan, P.; Hazen, S. P.; Roulin, A. C.; Vogel, J. P.; Wang, K.; Mur, L. A. Brachypodium: 20 years as a grass biology model system; the way forward?, Trends in Plant Science, Volume 27 (2022) no. 10, pp. 1002-1016 | DOI

[43] Hermisson, J.; Pennings, P. S. Soft Sweeps, Genetics, Volume 169 (2005) no. 4, pp. 2335-2352 | DOI

[44] Horton, M. W.; Hancock, A. M.; Huang, Y. S.; Toomajian, C.; Atwell, S.; Auton, A.; Muliyati, N. W.; Platt, A.; Sperone, F. G.; Vilhjálmsson, B. J.; Nordborg, M.; Borevitz, J. O.; Bergelson, J. Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel, Nature Genetics, Volume 44 (2012) no. 2, pp. 212-216 | DOI

[45] Huo, N.; Garvin, D. F.; You, F. M.; McMahon, S.; Luo, M.-C.; Gu, Y. Q.; Lazo, G. R.; Vogel, J. P. Comparison of a high-density genetic linkage map to genome features in the model grass Brachypodium distachyon, Theoretical and Applied Genetics, Volume 123 (2011) no. 3, pp. 455-464 | DOI

[46] Hus, K.; Betekhtin, A.; Pinski, A.; Rojek-Jelonek, M.; Grzebelus, E.; Nibau, C.; Gao, M.; Jaeger, K. E.; Jenkins, G.; Doonan, J. H.; Hasterok, R. A CRISPR/Cas9-Based Mutagenesis Protocol for Brachypodium distachyon and Its Allopolyploid Relative, Brachypodium hybridum, Frontiers in Plant Science, Volume 11 (2020) | DOI

[47] International Brachypodium Initiative Genome sequencing and analysis of the model grass Brachypodium distachyon, Nature, Volume 463 (2010) no. 7282, pp. 763-768 | DOI

[48] Jayakodi, M.; Padmarasu, S.; Haberer, G.; Bonthala, V. S.; Gundlach, H.; Monat, C.; Lux, T.; Kamal, N.; Lang, D.; Himmelbach, A.; Ens, J.; Zhang, X.-Q.; Angessa, T. T.; Zhou, G.; Tan, C.; Hill, C.; Wang, P.; Schreiber, M.; Boston, L. B.; Plott, C.; Jenkins, J.; Guo, Y.; Fiebig, A.; Budak, H.; Xu, D.; Zhang, J.; Wang, C.; Grimwood, J.; Schmutz, J.; Guo, G.; Zhang, G.; Mochida, K.; Hirayama, T.; Sato, K.; Chalmers, K. J.; Langridge, P.; Waugh, R.; Pozniak, C. J.; Scholz, U.; Mayer, K. F. X.; Spannagl, M.; Li, C.; Mascher, M.; Stein, N. The barley pan-genome reveals the hidden legacy of mutation breeding, Nature, Volume 588 (2020) no. 7837, pp. 284-289 | DOI

[49] Jennings, R. P.; Singarayer, J.; Stone, E. J.; Krebs-Kanzow, U.; Khon, V.; Nisancioglu, K. H.; Pfeiffer, M.; Zhang, X.; Parker, A.; Parton, A.; Groucutt, H. S.; White, T. S.; Drake, N. A.; Petraglia, M. D. The greening of Arabia: Multiple opportunities for human occupation of the Arabian Peninsula during the Late Pleistocene inferred from an ensemble of climate model simulations, Quaternary International, Volume 382 (2015), pp. 181-199 | DOI

[50] Jiang, Y.; Wang, X.; Yu, X.; Zhao, X.; Luo, N.; Pei, Z.; Liu, H.; Garvin, D. F. Quantitative Trait Loci Associated with Drought Tolerance in Brachypodium distachyon, Frontiers in Plant Science, Volume 8 (2017) | DOI

[51] Kooyers, N. J.; Greenlee, A. B.; Colicchio, J. M.; Oh, M.; Blackman, B. K. Replicate altitudinal clines reveal that evolutionary flexibility underlies adaptation to drought stress in annual M imulus guttatus, New Phytologist, Volume 206 (2014) no. 1, pp. 152-165 | DOI

[52] Korunes, K. L.; Samuk, K. pixy : Unbiased estimation of nucleotide diversity and divergence in the presence of missing data, Molecular Ecology Resources, Volume 21 (2021) no. 4, pp. 1359-1368 | DOI

[53] Lasky, J. R.; Josephs, E. B.; Morris, G. P. Genotype–environment associations to reveal the molecular basis of environmental adaptation, The Plant Cell, Volume 35 (2023) no. 1, pp. 125-138 | DOI

[54] Lee, C.-R.; Svardal, H.; Farlow, A.; Exposito-Alonso, M.; Ding, W.; Novikova, P.; Alonso-Blanco, C.; Weigel, D.; Nordborg, M. On the post-glacial spread of human commensal Arabidopsis thaliana, Nature Communications, Volume 8 (2017) no. 1 | DOI

[55] Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM, arXiv (2013) | DOI

[56] Li, H.; Handsaker, B.; Wysoker, A.; Fennell, T.; Ruan, J.; Homer, N.; Marth, G.; Abecasis, G.; Durbin, R. The Sequence Alignment/Map format and SAMtools, Bioinformatics, Volume 25 (2009) no. 16, pp. 2078-2079 | DOI

[57] Lopez-Alvarez, D.; Manzaneda, A. J.; Rey, P. J.; Giraldo, P.; Benavente, E.; Allainguillaume, J.; Mur, L.; Caicedo, A. L.; Hazen, S. P.; Breiman, A.; Ezrati, S.; Catalan, P. Environmental niche variation and evolutionary diversification of the Brachypodium distachyon grass complex species in their native circum-Mediterranean range, American Journal of Botany, Volume 102 (2015) no. 7, pp. 1073-1088 | DOI

[58] Lovell, J. T.; MacQueen, A. H.; Mamidi, S.; Bonnette, J.; Jenkins, J.; Napier, J. D.; Sreedasyam, A.; Healey, A.; Session, A.; Shu, S.; Barry, K.; Bonos, S.; Boston, L.; Daum, C.; Deshpande, S.; Ewing, A.; Grabowski, P. P.; Haque, T.; Harrison, M.; Jiang, J.; Kudrna, D.; Lipzen, A.; Pendergast, T. H.; Plott, C.; Qi, P.; Saski, C. A.; Shakirov, E. V.; Sims, D.; Sharma, M.; Sharma, R.; Stewart, A.; Singan, V. R.; Tang, Y.; Thibivillier, S.; Webber, J.; Weng, X.; Williams, M.; Wu, G. A.; Yoshinaga, Y.; Zane, M.; Zhang, L.; Zhang, J.; Behrman, K. D.; Boe, A. R.; Fay, P. A.; Fritschi, F. B.; Jastrow, J. D.; Lloyd-Reilley, J.; Martínez-Reyna, J. M.; Matamala, R.; Mitchell, R. B.; Rouquette, F. M.; Ronald, P.; Saha, M.; Tobias, C. M.; Udvardi, M.; Wing, R. A.; Wu, Y.; Bartley, L. E.; Casler, M.; Devos, K. M.; Lowry, D. B.; Rokhsar, D. S.; Grimwood, J.; Juenger, T. E.; Schmutz, J. Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass, Nature, Volume 590 (2021) no. 7846, pp. 438-444 | DOI

[59] Lynch, M.; Ackerman, M. S.; Gout, J.-F.; Long, H.; Sung, W.; Thomas, W. K.; Foster, P. L. Genetic drift, selection and the evolution of the mutation rate, Nature Reviews Genetics, Volume 17 (2016) no. 11, pp. 704-714 | DOI

[60] López-Alvarez, D.; López-Herranz, M. L.; Betekhtin, A.; Catalán, P. A DNA Barcoding Method to Discriminate between the Model Plant Brachypodium distachyon and Its Close Relatives B. stacei and B. hybridum (Poaceae), PLoS ONE, Volume 7 (2012) no. 12 | DOI

[61] Marees, A. T.; de Kluiver, H.; Stringer, S.; Vorspan, F.; Curis, E.; Marie-Claire, C.; Derks, E. M. A tutorial on conducting genome-wide association studies: Quality control and statistical analysis, International Journal of Methods in Psychiatric Research, Volume 27 (2018) no. 2 | DOI

[62] Marks, R. A.; Amézquita, E. J.; Percival, S.; Rougon-Cardoso, A.; Chibici-Revneanu, C.; Tebele, S. M.; Farrant, J. M.; Chitwood, D. H.; VanBuren, R. A critical analysis of plant science literature reveals ongoing inequities, Proceedings of the National Academy of Sciences, Volume 120 (2023) no. 10 | DOI

[63] McKenna, A.; Hanna, M.; Banks, E.; Sivachenko, A.; Cibulskis, K.; Kernytsky, A.; Garimella, K.; Altshuler, D.; Gabriel, S.; Daly, M.; DePristo, M. A. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data, Genome Research, Volume 20 (2010) no. 9, pp. 1297-1303 | DOI

[64] McKown, K. H.; Bergmann, D. C. Stomatal development in the grasses: lessons from models and crops (and crop models), New Phytologist, Volume 227 (2020) no. 6, pp. 1636-1648 | DOI

[65] Meredith, M.; Kruschke, J. HDInterval. HDInterval: Highest (Posterior) Density Intervals, R package, 2022 (https://CRAN.R-project.org/package=HDInterval)

[66] de Miguel, M.; Rodríguez‐Quilón, I.; Heuertz, M.; Hurel, A.; Grivet, D.; Jaramillo‐Correa, J. P.; Vendramin, G. G.; Plomion, C.; Majada, J.; Alía, R.; Eckert, A. J.; González‐Martínez, S. C. Polygenic adaptation and negative selection across traits, years and environments in a long‐lived plant species (Pinus pinaster Ait., Pinaceae), Molecular Ecology, Volume 31 (2022) no. 7, pp. 2089-2105 | DOI

[67] Minadakis N; Williams H; Horvath R; Caković D; Stritt C; Thieme M; Bourgeois Y; Roulin AC Scripts for "The demographic history of the wild crop relative Brachypodium distachyon is shaped by distinct past and present ecological niches" (v1.0.0), Zenodo, 2023 | DOI

[68] Minadakis N; Williams H; Horvath R; Caković D; Stritt C; Thieme M; Bourgeois Y; Roulin AC Supplementary data for: "The demographic history of the wild crop relative Brachypodium distachyon is shaped by distinct past and present ecological niches" [Data set], Zenodo | DOI

[69] Minadakis, N.; Kaderli, L.; Horvath, R.; Bourgeois, Y.; Xu, W.; Thieme, M.; Woods, D. P.; Roulin, A. C. Polygenic architecture of flowering time and its relationship with local environments in the grass Brachypodium distachyon, bioRxiv, 2022 | DOI

[70] Mittler, R.; Zandalinas, S. I.; Fichman, Y.; Van Breusegem, F. Reactive oxygen species signalling in plant stress responses, Nature Reviews Molecular Cell Biology, Volume 23 (2022) no. 10, pp. 663-679 | DOI

[71] Moles, A. T.; Warton, D. I.; Warman, L.; Swenson, N. G.; Laffan, S. W.; Zanne, A. E.; Pitman, A.; Hemmings, F. A.; Leishman, M. R. Global patterns in plant height, Journal of Ecology, Volume 97 (2009) no. 5, pp. 923-932 | DOI

[72] Montenegro, J. D.; Golicz, A. A.; Bayer, P. E.; Hurgobin, B.; Lee, H.; Chan, C. K.; Visendi, P.; Lai, K.; Doležel, J.; Batley, J.; Edwards, D. The pangenome of hexaploid bread wheat, The Plant Journal, Volume 90 (2017) no. 5, pp. 1007-1013 | DOI

[73] Nielsen, R.; Williamson, S.; Kim, Y.; Hubisz, M. J.; Clark, A. G.; Bustamante, C. Genomic scans for selective sweeps using SNP data, Genome Research, Volume 15 (2005) no. 11, pp. 1566-1575 | DOI

[74] Nunes, T. D. G.; Zhang, D.; Raissig, M. T. Form, development and function of grass stomata, The Plant Journal, Volume 101 (2020) no. 4, pp. 780-799 | DOI

[75] Nunes, T. D.; Berg, L. S.; Slawinska, M. W.; Zhang, D.; Redt, L.; Sibout, R.; Vogel, J. P.; Laudencia-Chingcuanco, D.; Jesenofsky, B.; Lindner, H.; Raissig, M. T. Regulation of hair cell and stomatal size by a hair cell-specific peroxidase in the grass Brachypodium distachyon, Current Biology, Volume 33 (2023) no. 9 | DOI

[76] Ortiz, M.; Tremetsberger, K.; Talavera, S.; Stuessy, T.; García-Castaño, J. Population structure of Hypochaeris salzmanniana DC. (Asteraceae), an endemic species to the Atlantic coast on both sides of the Strait of Gibraltar, in relation to Quaternary sea level changes, Molecular Ecology, Volume 16 (2007) no. 3, pp. 541-552 | DOI

[77] Phillips, S. J.; Anderson, R. P.; Schapire, R. E. Maximum entropy modeling of species geographic distributions, Ecological Modelling, Volume 190 (2006) no. 3-4, pp. 231-259 | DOI

[78] Provart, N. J.; Alonso, J.; Assmann, S. M.; Bergmann, D.; Brady, S. M.; Brkljacic, J.; Browse, J.; Chapple, C.; Colot, V.; Cutler, S.; Dangl, J.; Ehrhardt, D.; Friesner, J. D.; Frommer, W. B.; Grotewold, E.; Meyerowitz, E.; Nemhauser, J.; Nordborg, M.; Pikaard, C.; Shanklin, J.; Somerville, C.; Stitt, M.; Torii, K. U.; Waese, J.; Wagner, D.; McCourt, P. 50 years of Arabidopsis research: highlights and future directions, New Phytologist, Volume 209 (2016) no. 3, pp. 921-944 | DOI

[79] Quinlan, A. R.; Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features, Bioinformatics, Volume 26 (2010) no. 6, pp. 841-842 | DOI

[80] Raissig, M. T.; Woods, D. P. The wild grass Brachypodium distachyon as a developmental model system, Emerging Model Systems in Developmental Biology (Current Topics in Developmental Biology), Volume 147, Elsevier, 2022, pp. 33-71 | DOI

[81] Rannala, B.; Yang, Z. Bayes Estimation of Species Divergence Times and Ancestral Population Sizes Using DNA Sequences From Multiple Loci, Genetics, Volume 164 (2003) no. 4, pp. 1645-1656 | DOI

[82] Ream, T. S.; Woods, D. P.; Schwartz, C. J.; Sanabria, C. P.; Mahoy, J. A.; Walters, E. M.; Kaeppler, H. F.; Amasino, R. M. Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon, Plant Physiology, Volume 164 (2014) no. 2, pp. 694-709 | DOI

[83] Rellstab, C.; Gugerli, F.; Eckert, A. J.; Hancock, A. M.; Holderegger, R. A practical guide to environmental association analysis in landscape genomics, Molecular Ecology, Volume 24 (2015) no. 17, pp. 4348-4370 | DOI

[84] Sharma, N.; Ruelens, P.; D'hauw, M.; Maggen, T.; Dochy, N.; Torfs, S.; Kaufmann, K.; Rohde, A.; Geuten, K. A Flowering Locus C Homolog Is a Vernalization-Regulated Repressor in Brachypodium and Is Cold Regulated in Wheat, Plant Physiology, Volume 173 (2017) no. 2, pp. 1301-1315 | DOI

[85] Skalska, A.; Stritt, C.; Wyler, M.; Williams, H. W.; Vickers, M.; Han, J.; Tuna, M.; Savas Tuna, G.; Susek, K.; Swain, M.; Wóycicki, R. K.; Chaudhary, S.; Corke, F.; Doonan, J. H.; Roulin, A. C.; Hasterok, R.; Mur, L. A. J. Genetic and Methylome Variation in Turkish Brachypodium Distachyon Accessions Differentiate Two Geographically Distinct Subpopulations, International Journal of Molecular Sciences, Volume 21 (2020) no. 18 | DOI

[86] Speidel, L.; Forest, M.; Shi, S.; Myers, S. R. A method for genome-wide genealogy estimation for thousands of samples, Nature Genetics, Volume 51 (2019) no. 9, pp. 1321-1329 | DOI

[87] Stritt, C.; Gimmi, E. L.; Wyler, M.; Bakali, A. H.; Skalska, A.; Hasterok, R.; Mur, L. A. J.; Pecchioni, N.; Roulin, A. C. Migration without interbreeding: Evolutionary history of a highly selfing Mediterranean grass inferred from whole genomes, Molecular Ecology, Volume 31 (2022) no. 1, pp. 70-85 | DOI

[88] Stritt, C.; Gordon, S. P.; Wicker, T.; Vogel, J. P.; Roulin, A. C. Recent Activity in Expanding Populations and Purifying Selection Have Shaped Transposable Element Landscapes across Natural Accessions of the Mediterranean Grass Brachypodium distachyon, Genome Biology and Evolution, Volume 10 (2018) no. 1, pp. 304-318 | DOI

[89] Takou, M.; Wieters, B.; Kopriva, S.; Coupland, G.; Linstädter, A.; De Meaux, J. Linking genes with ecological strategies in Arabidopsis thaliana, Journal of Experimental Botany, Volume 70 (2019) no. 4, pp. 1141-1151 | DOI

[90] Tang, K.; Thornton, K. R.; Stoneking, M. A New Approach for Using Genome Scans to Detect Recent Positive Selection in the Human Genome, PLoS Biology, Volume 5 (2007) no. 7 | DOI

[91] Vidigal, D. S.; Marques, A. C. S. S.; Willems, L. A. J.; Buijs, G.; Méndez-Vigo, B.; Hilhorst, H. W. M.; Bentsink, L.; Picó, F. X.; Alonso-Blanco, C. Altitudinal and climatic associations of seed dormancy and flowering traits evidence adaptation of annual life cycle timing in Arabidopsis thaliana, Plant, Cell & Environment, Volume 39 (2016) no. 8, pp. 1737-1748 | DOI

[92] Wadgymar, S. M.; Ogilvie, J. E.; Inouye, D. W.; Weis, A. E.; Anderson, J. T. Phenological responses to multiple environmental drivers under climate change: insights from a long‐term observational study and a manipulative field experiment, New Phytologist, Volume 218 (2018) no. 2, pp. 517-529 | DOI

[93] Walkowiak, S.; Gao, L.; Monat, C.; Haberer, G.; Kassa, M. T.; Brinton, J.; Ramirez-Gonzalez, R. H.; Kolodziej, M. C.; Delorean, E.; Thambugala, D.; Klymiuk, V.; Byrns, B.; Gundlach, H.; Bandi, V.; Siri, J. N.; Nilsen, K.; Aquino, C.; Himmelbach, A.; Copetti, D.; Ban, T.; Venturini, L.; Bevan, M.; Clavijo, B.; Koo, D.-H.; Ens, J.; Wiebe, K.; N’Diaye, A.; Fritz, A. K.; Gutwin, C.; Fiebig, A.; Fosker, C.; Fu, B. X.; Accinelli, G. G.; Gardner, K. A.; Fradgley, N.; Gutierrez-Gonzalez, J.; Halstead-Nussloch, G.; Hatakeyama, M.; Koh, C. S.; Deek, J.; Costamagna, A. C.; Fobert, P.; Heavens, D.; Kanamori, H.; Kawaura, K.; Kobayashi, F.; Krasileva, K.; Kuo, T.; McKenzie, N.; Murata, K.; Nabeka, Y.; Paape, T.; Padmarasu, S.; Percival-Alwyn, L.; Kagale, S.; Scholz, U.; Sese, J.; Juliana, P.; Singh, R.; Shimizu-Inatsugi, R.; Swarbreck, D.; Cockram, J.; Budak, H.; Tameshige, T.; Tanaka, T.; Tsuji, H.; Wright, J.; Wu, J.; Steuernagel, B.; Small, I.; Cloutier, S.; Keeble-Gagnère, G.; Muehlbauer, G.; Tibbets, J.; Nasuda, S.; Melonek, J.; Hucl, P. J.; Sharpe, A. G.; Clark, M.; Legg, E.; Bharti, A.; Langridge, P.; Hall, A.; Uauy, C.; Mascher, M.; Krattinger, S. G.; Handa, H.; Shimizu, K. K.; Distelfeld, A.; Chalmers, K.; Keller, B.; Mayer, K. F. X.; Poland, J.; Stein, N.; McCartney, C. A.; Spannagl, M.; Wicker, T.; Pozniak, C. J. Multiple wheat genomes reveal global variation in modern breeding, Nature, Volume 588 (2020) no. 7837, pp. 277-283 | DOI

[94] Wang, W.; Mauleon, R.; Hu, Z.; Chebotarov, D.; Tai, S.; Wu, Z.; Li, M.; Zheng, T.; Fuentes, R. R.; Zhang, F.; Mansueto, L.; Copetti, D.; Sanciangco, M.; Palis, K. C.; Xu, J.; Sun, C.; Fu, B.; Zhang, H.; Gao, Y.; Zhao, X.; Shen, F.; Cui, X.; Yu, H.; Li, Z.; Chen, M.; Detras, J.; Zhou, Y.; Zhang, X.; Zhao, Y.; Kudrna, D.; Wang, C.; Li, R.; Jia, B.; Lu, J.; He, X.; Dong, Z.; Xu, J.; Li, Y.; Wang, M.; Shi, J.; Li, J.; Zhang, D.; Lee, S.; Hu, W.; Poliakov, A.; Dubchak, I.; Ulat, V. J.; Borja, F. N.; Mendoza, J. R.; Ali, J.; Li, J.; Gao, Q.; Niu, Y.; Yue, Z.; Naredo, M. E. B.; Talag, J.; Wang, X.; Li, J.; Fang, X.; Yin, Y.; Glaszmann, J.-C.; Zhang, J.; Li, J.; Hamilton, R. S.; Wing, R. A.; Ruan, J.; Zhang, G.; Wei, C.; Alexandrov, N.; McNally, K. L.; Li, Z.; Leung, H. Genomic variation in 3,010 diverse accessions of Asian cultivated rice, Nature, Volume 557 (2018) no. 7703, pp. 43-49 | DOI

[95] Warren, D. L.; Glor, R. E.; Turelli, M. ENMTools: a toolbox for comparative studies of environmental niche models, Ecography (2010) | DOI

[96] Warren, D. L.; Matzke, N. J.; Cardillo, M.; Baumgartner, J. B.; Beaumont, L. J.; Turelli, M.; Glor, R. E.; Huron, N. A.; Simões, M.; Iglesias, T. L.; Piquet, J. C.; Dinnage, R. ENMTools 1.0: an R package for comparative ecological biogeography, Ecography, Volume 44 (2021) no. 4, pp. 504-511 | DOI

[97] Wei, T.; Simko, V. R package ‘corrplot’: Visualization of a Correlation Matrix. (Version 0.92), 2021 (https://github.com/taiyun/corrplot)

[98] Wieters, B.; Steige, K. A.; He, F.; Koch, E. M.; Ramos-Onsins, S. E.; Gu, H.; Guo, Y.-L.; Sunyaev, S.; de Meaux, J. Polygenic adaptation of rosette growth in Arabidopsis thaliana, PLOS Genetics, Volume 17 (2021) no. 1 | DOI

[99] Williams, H. W.; Cross, D. E.; Crump, H. L.; Drost, C. J.; Thomas, C. J. Climate suitability for European ticks: assessing species distribution models against null models and projection under AR5 climate, Parasites & Vectors, Volume 8 (2015) no. 1 | DOI

[100] Wilson, P. B.; Streich, J. C.; Murray, K. D.; Eichten, S. R.; Cheng, R.; Aitken, N. C.; Spokas, K.; Warthmann, N.; Gordon, S. P.; Accession, C.; Vogel, J. P.; Borevitz, J. O. Global Diversity of the Brachypodium Species Complex as a Resource for Genome-Wide Association Studies Demonstrated for Agronomic Traits in Response to Climate, Genetics, Volume 211 (2019) no. 1, pp. 317-331 | DOI

[101] Woods, D. P.; Ream, T. S.; Minevich, G.; Hobert, O.; Amasino, R. M. PHYTOCHROME C Is an Essential Light Receptor for Photoperiodic Flowering in the Temperate Grass, Brachypodium distachyon, Genetics, Volume 198 (2014) no. 1, pp. 397-408 | DOI

[102] Woods, D. P.; Bednarek, R.; Bouché, F.; Gordon, S. P.; Vogel, J. P.; Garvin, D. F.; Amasino, R. M. Genetic Architecture of Flowering-Time Variation in Brachypodium distachyon, Plant Physiology, Volume 173 (2017) no. 1, pp. 269-279 | DOI

[103] Woods, D. P.; Dong, Y.; Bouché, F.; Mayer, K.; Varner, L.; Ream, T. S.; Thrower, N.; Wilkerson, C.; Cartwright, A.; Sibout, R.; Laudencia‐Chingcuanco, D.; Vogel, J.; Amasino, R. M. Mutations in the predicted DNA polymerase subunit POLD3 result in more rapid flowering of Brachypodium distachyon, New Phytologist, Volume 227 (2020) no. 6, pp. 1725-1735 | DOI

[104] Woodward, A. W.; Bartel, B. Biology in Bloom: A Primer on the Arabidopsis thaliana Model System, Genetics, Volume 208 (2018) no. 4, pp. 1337-1349 | DOI

[105] Wu, Q.; Han, T.-S.; Chen, X.; Chen, J.-F.; Zou, Y.-P.; Li, Z.-W.; Xu, Y.-C.; Guo, Y.-L. Long-term balancing selection contributes to adaptation in Arabidopsis and its relatives, Genome Biology, Volume 18 (2017) no. 1 | DOI

[106] Wyler, M.; Stritt, C.; Walser, J.-C.; Baroux, C.; Roulin, A. C. Impact of Transposable Elements on Methylation and Gene Expression across Natural Accessions of Brachypodium distachyon, Genome Biology and Evolution, Volume 12 (2020) no. 11, pp. 1994-2001 | DOI

[107] Yan, W.; Wang, B.; Chan, E.; Mitchell‐Olds, T. Genetic architecture and adaptation of flowering time among environments, New Phytologist, Volume 230 (2021) no. 3, pp. 1214-1227 | DOI

[108] Yeaman, S. Evolution of polygenic traits under global vs local adaptation, Genetics, Volume 220 (2022) no. 1 | DOI

[109] Yokoyama, Y.; Lambeck, K.; De Deckker, P.; Johnston, P.; Fifield, l. K. Erratum: correction: Timing of the Last Glacial Maximum from observed sea-level minima, Nature, Volume 412 (2001) no. 6842, p. 99-99 | DOI

[110] Zhang, D.; Spiegelhalder, R. P.; Abrash, E. B.; Nunes, T. D.; Hidalgo, I.; Anleu Gil, M. X.; Jesenofsky, B.; Lindner, H.; Bergmann, D. C.; Raissig, M. T. Opposite polarity programs regulate asymmetric subsidiary cell divisions in grasses, eLife, Volume 11 (2022) | DOI

[111] Zhen, Y.; Ungerer, M. C. Clinal variation in freezing tolerance among natural accessions of Arabidopsis thaliana, New Phytologist, Volume 177 (2007) no. 2, pp. 419-427 | DOI

[112] Zheng, X.; Levine, D.; Shen, J.; Gogarten, S. M.; Laurie, C.; Weir, B. S. A high-performance computing toolset for relatedness and principal component analysis of SNP data, Bioinformatics, Volume 28 (2012) no. 24, pp. 3326-3328 | DOI

[113] Zhou, X.; Stephens, M. Genome-wide efficient mixed-model analysis for association studies, Nature Genetics, Volume 44 (2012) no. 7, pp. 821-824 | DOI

Cited by Sources: