1932

Abstract

The genetics model system (L.) Heynh. lives across a vast geographic range with contrasting climates, in response to which it has evolved diverse life histories and phenotypic adaptations. In the last decade, the cataloging of worldwide populations, DNA sequencing of whole genomes, and conducting of outdoor field experiments have transformed it into a powerful evolutionary ecology system to understand the genomic basis of adaptation. Here, we summarize new insights on following the coordinated efforts of the 1001 Genomes Project, the latest reconstruction of biogeographic and demographic history, and the systematic genomic mapping of trait natural variation through 15 years of genome-wide association studies. We then put this in the context of local adaptation across climates by summarizing insights from 73 outdoor common garden experiments conducted to date. We conclude by highlighting how molecular and genomic knowledge of adaptation can help us to understand species’ (mal)adaptation under ongoing climate change.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-071123-095146
2025-05-20
2025-06-16
Loading full text...

Full text loading...

/deliver/fulltext/arplant/76/1/annurev-arplant-071123-095146.html?itemId=/content/journals/10.1146/annurev-arplant-071123-095146&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    1001 Genomes Consort. 2016.. 1,135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana. . Cell 166:(2):48191
    [Crossref] [Google Scholar]
  2. 2.
    Abdellaoui A, Yengo L, Verweij KJH, Visscher PM. 2023.. 15 years of GWAS discovery: realizing the promise. . Am. J. Hum. Genet. 110:(2):17994
    [Crossref] [Google Scholar]
  3. 3.
    Ågren J, Oakley CG, McKay JK, Lovell JT, Schemske DW. 2013.. Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana. . PNAS 110:(52):2107782
    [Crossref] [Google Scholar]
  4. 4.
    Ågren J, Schemske DW. 2012.. Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. . New Phytol. 194:(4):111222
    [Crossref] [Google Scholar]
  5. 5.
    Alonso-Blanco C, Aarts MGM, Bentsink L, Keurentjes JJB, Reymond M, et al. 2009.. What has natural variation taught us about plant development, physiology, and adaptation?. Plant Cell 21:(7):187796
    [Crossref] [Google Scholar]
  6. 6.
    Alonso-Blanco C, Bentsink L, Hanhart CJ, Blankestijn-de Vries H, Koornneef M. 2003.. Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. . Genetics 164:(2):71129
    [Crossref] [Google Scholar]
  7. 7.
    Alonso-Blanco C, Koornneef M. 2000.. Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. . Trends Plant Sci. 5:(1):2229
    [Crossref] [Google Scholar]
  8. 8.
    Alonso-Blanco C, Méndez-Vigo B, Koornneef M. 2005.. From phenotypic to molecular polymorphisms involved in naturally occurring variation of plant development. . Int. J. Dev. Biol. 49:(5–6):71732
    [Crossref] [Google Scholar]
  9. 9.
    Alonso-Blanco C, Méndez-Vigo B, Xavier Picó F. 2021.. Analyses of natural variation: field experiments and nucleotide diversity for your favorite gene. . Methods Mol. Biol. 2200::93112
    [Crossref] [Google Scholar]
  10. 10.
    Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, et al. 2003.. Genome-wide insertional mutagenesis of Arabidopsis thaliana. . Science 301:(5633):65357
    [Crossref] [Google Scholar]
  11. 11.
    Arabidopsis Genome Initiat. 2000.. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. . Nature 408:(6814):796815
    [Crossref] [Google Scholar]
  12. 12.
    Arteaga N, Méndez-Vigo B, Fuster-Pons A, Savic M, Murillo-Sánchez A, et al. 2022.. Differential environmental and genomic architectures shape the natural diversity for trichome patterning and morphology in different Arabidopsis organs. . Plant Cell Environ. 45:(10):301835
    [Crossref] [Google Scholar]
  13. 13.
    Arteaga N, Savic M, Méndez-Vigo B, Fuster-Pons A, Torres-Pérez R, et al. 2021.. MYB transcription factors drive evolutionary innovations in Arabidopsis fruit trichome patterning. . Plant Cell 33:(3):54865
    [Crossref] [Google Scholar]
  14. 14.
    Atwell S, Huang YS, Vilhjálmsson BJ, Willems G, Horton M, et al. 2010.. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. . Nature 465:(7298):62731
    [Crossref] [Google Scholar]
  15. 15.
    Auge GA, Blair LK, Burghardt LT, Coughlan J, Edwards B, et al. 2015.. Secondary dormancy dynamics depends on primary dormancy status in Arabidopsis thaliana. . Seed Sci. Res. 25:(2):23046
    [Crossref] [Google Scholar]
  16. 16.
    Baskin CC, Baskin JM. 1998.. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. San Diego, CA:: Academic Press
    [Google Scholar]
  17. 17.
    Baskin JM, Baskin CC. 1997.. Methods of breaking seed dormancy in the endangered species Iliamna corei (Sherff) Sherff (Malvaceae), with special attention to heating. . Nat. Areas J. 17:(4):31323
    [Google Scholar]
  18. 18.
    Bazakos C, Hanemian M, Trontin C, Jiménez-Gómez JM, Loudet O. 2017.. New strategies and tools in quantitative genetics: how to go from the phenotype to the genotype. . Annu. Rev. Plant Biol. 68::43555
    [Crossref] [Google Scholar]
  19. 19.
    Bentsink L, Jowett J, Hanhart CJ, Koornneef M. 2006.. Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. . PNAS 103:(45):1704247
    [Crossref] [Google Scholar]
  20. 20.
    Bergelson J, Roux F. 2010.. Towards identifying genes underlying ecologically relevant traits in Arabidopsis thaliana. . Nat. Rev. Genet. 11:(12):86779
    [Crossref] [Google Scholar]
  21. 21.
    Bergelson J, Stahl E, Dudek S, Kreitman M. 1998.. Genetic variation within and among populations of Arabidopsis thaliana. . Genetics 148:(3):131123
    [Crossref] [Google Scholar]
  22. 22.
    Bewley JD. 1997.. Seed germination and dormancy. . Plant Cell 9:(7):105566
    [Crossref] [Google Scholar]
  23. 23.
    Bhaskara GB, Lasky JR, Razzaque S, Zhang L, Haque T, et al. 2022.. Natural variation identifies new effectors of water-use efficiency in Arabidopsis. . PNAS 119:(33):e2205305119
    [Crossref] [Google Scholar]
  24. 24.
    Bomblies K, Yant L, Laitinen RA, Kim S-T, Hollister JD, et al. 2010.. Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. . PLOS Genet. 6:(3):e1000890
    [Crossref] [Google Scholar]
  25. 25.
    Bontrager M, Usui T, Lee-Yaw JA, Anstett DN, Branch HA, et al. 2021.. Adaptation across geographic ranges is consistent with strong selection in marginal climates and legacies of range expansion. . Evolution 75:(6):131633
    [Crossref] [Google Scholar]
  26. 26.
    Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, et al. 2010.. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. . PLOS Genet. 6:(5):e1000940
    [Crossref] [Google Scholar]
  27. 27.
    Brennan AC, Méndez-Vigo B, Haddioui A, Martínez-Zapater JM, Picó FX, Alonso-Blanco C. 2014.. The genetic structure of Arabidopsis thaliana in the south-western Mediterranean range reveals a shared history between North Africa and southern Europe. . BMC Plant Biol. 14::17
    [Crossref] [Google Scholar]
  28. 28.
    Burghardt LT, Metcalf CJE, Wilczek AM, Schmitt J, Donohue K. 2015.. Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes. . Am. Nat. 185:(2):21227
    [Crossref] [Google Scholar]
  29. 29.
    Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MD. 2004.. Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. . PNAS 101:(44):1567075
    [Crossref] [Google Scholar]
  30. 30.
    Callahan HS, Pigliucci M. 2002.. Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana. . Ecology 83:(7):196580
    [Crossref] [Google Scholar]
  31. 31.
    Cao J, Schneeberger K, Ossowski S, Günther T, Bender S, et al. 2011.. Whole-genome sequencing of multiple Arabidopsis thaliana populations. . Nat. Genet. 43:(10):95663
    [Crossref] [Google Scholar]
  32. 32.
    Capblancq T, Fitzpatrick MC, Bay RA, Exposito-Alonso M, Keller SR. 2020.. Genomic prediction of (mal)adaptation across current and future climatic landscapes. . Annu. Rev. Ecol. Evol. Syst. 51::24569
    [Crossref] [Google Scholar]
  33. 33.
    Chew YH, Wilczek AM, Williams M, Welch SM, Schmitt J, Halliday KJ. 2012.. An augmented Arabidopsis phenology model reveals seasonal temperature control of flowering time. . New Phytol. 194:(3):65465
    [Crossref] [Google Scholar]
  34. 34.
    Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, et al. 2007.. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. . Science 317:(5836):33842
    [Crossref] [Google Scholar]
  35. 35.
    Clausen J, Keck DD, Hiesey WM. 1941.. Regional differentiation in plant species. . Am. Nat. 75:(758):23150
    [Crossref] [Google Scholar]
  36. 36.
    Clauss MJ, Venable DL. 2000.. Seed germination in desert annuals: an empirical test of adaptive bet hedging. . Am. Nat. 155:(2):16886
    [Crossref] [Google Scholar]
  37. 37.
    Debieu M, Tang C, Stich B, Sikosek T, Effgen S, et al. 2013.. Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana. . PLOS ONE 8:(5):e61075
    [Crossref] [Google Scholar]
  38. 38.
    Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, et al. 2016.. The global spectrum of plant form and function. . Nature 529:(7585):16771
    [Crossref] [Google Scholar]
  39. 39.
    Dittberner H, Korte A, Mettler-Altmann T, Weber APM, Monroe G, de Meaux J. 2018.. Natural variation in stomata size contributes to the local adaptation of water-use efficiency in Arabidopsis thaliana. . Mol. Ecol. 27:(20):405265
    [Crossref] [Google Scholar]
  40. 40.
    Dittmar EL, Oakley CG, Ågren J, Schemske DW. 2014.. Flowering time QTL in natural populations of Arabidopsis thaliana and implications for their adaptive value. . Mol. Ecol. 23:(17):4291303
    [Crossref] [Google Scholar]
  41. 41.
    Donohue K, Dorn L, Griffith C, Kim E, Aguilera A, et al. 2005.. The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. . Evolution 59:(4):75870
    [Google Scholar]
  42. 42.
    Duncan S, Holm S, Questa J, Irwin J, Grant A, Dean C. 2015.. Seasonal shift in timing of vernalization as an adaptation to extreme winter. . eLife 4::e06620
    [Crossref] [Google Scholar]
  43. 43.
    Durvasula A, Fulgione A, Gutaker RM, Alacakaptan SI, Flood PJ, et al. 2017.. African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana. . PNAS 114:(20):521318
    [Crossref] [Google Scholar]
  44. 44.
    Exposito-Alonso M. 2020.. Seasonal timing adaptation across the geographic range of Arabidopsis thaliana. . PNAS 117:(18):966567
    [Crossref] [Google Scholar]
  45. 45.
    Exposito-Alonso M. 2023.. Understanding local plant extinctions before it is too late: bridging evolutionary genomics with global ecology. . New Phytol. 237:(6):200511
    [Crossref] [Google Scholar]
  46. 46.
    Exposito-Alonso M, 500 Genomes Field Exp. Team, Burbano HA, Bossdorf O, Nielsen R, Weigel D. 2019.. Natural selection on the Arabidopsis thaliana genome in present and future climates. . Nature 573:(7772):12629
    [Crossref] [Google Scholar]
  47. 47.
    Exposito-Alonso M, Becker C, Schuenemann VJ, Reiter E, Setzer C, et al. 2018a.. The rate and potential relevance of new mutations in a colonizing plant lineage. . PLOS Genet. 14:(2):e1007155
    [Crossref] [Google Scholar]
  48. 48.
    Exposito-Alonso M, Brennan AC, Alonso-Blanco C, Picó FX. 2018b.. Spatio-temporal variation in fitness responses to contrasting environments in Arabidopsis thaliana. . Evolution 72:(8):157086
    [Crossref] [Google Scholar]
  49. 49.
    Exposito-Alonso M, Vasseur F, Ding W, Wang G, Burbano HA, Weigel D. 2018c.. Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana. . Nat. Ecol. Evol. 2:(2):35258
    [Crossref] [Google Scholar]
  50. 50.
    Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, Wilczek AM. 2011.. A map of local adaptation in Arabidopsis thaliana. . Science 334:(6052):8689
    [Crossref] [Google Scholar]
  51. 51.
    Fournier-Level A, Taylor MA, Paril JF, Martínez-Berdeja A, Stitzer MC, et al. 2022.. Adaptive significance of flowering time variation across natural seasonal environments in Arabidopsis thaliana. . New Phytol. 234:(2):71934
    [Crossref] [Google Scholar]
  52. 52.
    Fournier-Level A, Wilczek AM, Cooper MD, Roe JL, Anderson J, et al. 2013.. Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana. . Mol. Ecol. 22:(13):355266
    [Crossref] [Google Scholar]
  53. 53.
    Frachon L, Libourel C, Villoutreix R, Carrère S, Glorieux C, et al. 2017.. Intermediate degrees of synergistic pleiotropy drive adaptive evolution in ecological time. . Nat. Ecol. Evol. 1:(10):155161
    [Crossref] [Google Scholar]
  54. 54.
    François O, Blum MGB, Jakobsson M, Rosenberg NA. 2008.. Demographic history of European populations of Arabidopsis thaliana. . PLOS Genet. 4:(5):e1000075
    [Crossref] [Google Scholar]
  55. 55.
    Fulgione A, Koornneef M, Roux F, Hermisson J, Hancock AM. 2018.. Madeiran Arabidopsis thaliana reveals ancient long-range colonization and clarifies demography in Eurasia. . Mol. Biol. Evol. 35:(3):56474
    [Crossref] [Google Scholar]
  56. 56.
    Fulgione A, Neto C, Elfarargi AF, Tergemina E, Ansari S, et al. 2022.. Parallel reduction in flowering time from de novo mutations enable evolutionary rescue in colonizing lineages. . Nat. Commun. 13:(1):1461
    [Crossref] [Google Scholar]
  57. 57.
    Gan X, Stegle O, Behr J, Steffen JG, Drewe P, et al. 2011.. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. . Nature 477:(7365):41923
    [Crossref] [Google Scholar]
  58. 58.
    Gibson G. 2011.. Rare and common variants: twenty arguments. . Nat. Rev. Genet. 13:(2):13545
    [Crossref] [Google Scholar]
  59. 59.
    Griffith C, Kim E, Donohue K. 2004.. Life-history variation and adaptation in the historically mobile plant Arabidopsis thaliana (Brassicaceae) in North America. . Am. J. Bot. 91:(6):83749
    [Crossref] [Google Scholar]
  60. 60.
    Grillo MA, Li C, Hammond M, Wang L, Schemske DW. 2013.. Genetic architecture of flowering time differentiation between locally adapted populations of Arabidopsis thaliana. . New Phytol. 197:(4):132131
    [Crossref] [Google Scholar]
  61. 61.
    Grime JP, Pierce S. 2012.. The Evolutionary Strategies that Shape Ecosystems. Hoboken, NJ:: Wiley
    [Google Scholar]
  62. 62.
    Grimm DG, Roqueiro D, Salome P, Kleeberger S, Greshake B, et al. 2016.. easyGWAS: a cloud-based platform for comparing the results of genome-wide association studies. . Plant Cell 29:(1):519
    [Crossref] [Google Scholar]
  63. 63.
    Hagmann J, Becker C, Müller J, Stegle O, Meyer RC, et al. 2015.. Century-scale methylome stability in a recently diverged Arabidopsis thaliana lineage. . PLOS Genet. 11:(1):e1004920
    [Crossref] [Google Scholar]
  64. 64.
    Hamilton JA, Okada M, Korves T, Schmitt J. 2015.. The role of climate adaptation in colonization success in Arabidopsis thaliana. . Mol. Ecol. 24:(9):225363
    [Crossref] [Google Scholar]
  65. 65.
    Hampe A, Petit RJ. 2005.. Conserving biodiversity under climate change: the rear edge matters. . Ecol. Lett. 8:(5):46167
    [Crossref] [Google Scholar]
  66. 66.
    Hancock AM, Brachi B, Faure N, Horton MW, Jarymowycz LB, et al. 2011.. Adaptation to climate across the Arabidopsis thaliana genome. . Science 334:(6052):8386
    [Crossref] [Google Scholar]
  67. 67.
    Harper JL. 1977.. Population Biology of Plants. London:: Academic
    [Google Scholar]
  68. 68.
    Henderson IR, Dean C. 2004.. Control of Arabidopsis flowering: the chill before the bloom. . Development 131:(16):382938
    [Crossref] [Google Scholar]
  69. 69.
    Hepworth J, Antoniou-Kourounioti RL, Bloomer RH, Selga C, Berggren K, et al. 2018.. Absence of warmth permits epigenetic memory of winter in Arabidopsis. . Nat. Commun. 9:(1):639
    [Crossref] [Google Scholar]
  70. 70.
    Hereford J. 2009.. A quantitative survey of local adaptation and fitness trade-offs. . Am. Nat. 173:(5):57988
    [Crossref] [Google Scholar]
  71. 71.
    Hoffmann MH. 2002.. Biogeography of Arabidopsis thaliana (L.) Heynh. (Brassicaceae). . J. Biogeogr. 29:(1):12534
    [Crossref] [Google Scholar]
  72. 72.
    Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S, et al. 2012.. Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. . Nat. Genet. 44:(2):21216
    [Crossref] [Google Scholar]
  73. 73.
    IPBES (Intergov. Sci. Policy Platf. Biodivers. Ecosyst. Serv.). 2019.. Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. Bonn, Ger.:: IPBES
    [Google Scholar]
  74. 74.
    Juenger TE, Mckay JK, Hausmann N, Keurentjes JJB, Sen S, et al. 2005.. Identification and characterization of QTL underlying whole-plant physiology in Arabidopsis thaliana: δ13C, stomatal conductance and transpiration efficiency. . Plant Cell Environ. 28:(6):697708
    [Crossref] [Google Scholar]
  75. 75.
    Kang M, Wu H, Liu H, Liu W, Zhu M, et al. 2023.. The pan-genome and local adaptation of Arabidopsis thaliana. . Nat. Commun. 14::6259
    [Crossref] [Google Scholar]
  76. 76.
    Karasov TL, Kniskern JM, Gao L, DeYoung BJ, Ding J, et al. 2014.. The long-term maintenance of a resistance polymorphism through diffuse interactions. . Nature 512:(7515):43640
    [Crossref] [Google Scholar]
  77. 77.
    Kasulin L, Rowan B, León RJC, Schuenemann VJ, Weigel D, Botto JF. 2017.. A single haplotype hyposensitive to light and requiring strong vernalization dominates Arabidopsis thaliana populations in Patagonia, Argentina. . Mol. Ecol. 26:(13):3389404
    [Crossref] [Google Scholar]
  78. 78.
    Katz E, Knapp A, Lensink M, Keller CK, Stefani J, et al. 2022.. Genetic variation underlying differential ammonium and nitrate responses in Arabidopsis thaliana. . Plant Cell 34:(12):4696713
    [Crossref] [Google Scholar]
  79. 79.
    Kawakatsu T, Huang S-SC, Jupe F, Sasaki E, Schmitz RJ, et al. 2016.. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. . Cell 166:(2):492505
    [Crossref] [Google Scholar]
  80. 80.
    Kim S, Plagnol V, Hu TT, Toomajian C, Clark RM, et al. 2007.. Recombination and linkage disequilibrium in Arabidopsis thaliana. . Nat. Genet. 39:(9):115155
    [Crossref] [Google Scholar]
  81. 81.
    Kingsolver JG, Diamond SE, Siepielski AM, Carlson SM. 2012.. Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. . Evol. Ecol. 26:(5):110118
    [Crossref] [Google Scholar]
  82. 82.
    Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, et al. 2001.. The strength of phenotypic selection in natural populations. . Am. Nat. 157:(3):24561
    [Crossref] [Google Scholar]
  83. 83.
    Koch MA, Matschinger M. 2007.. Evolution and genetic differentiation among relatives of Arabidopsis thaliana. . PNAS 104:(15):627277
    [Crossref] [Google Scholar]
  84. 84.
    Koornneef M, Alonso-Blanco C, Vreugdenhil D. 2004.. Naturally occurring genetic variation in Arabidopsis thaliana. . Annu. Rev. Plant Biol. 55::14172
    [Crossref] [Google Scholar]
  85. 85.
    Korves TM, Schmid KJ, Caicedo AL, Mays C, Stinchcombe JR, et al. 2007.. Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. . Am. Nat. 169:(5):E14157
    [Crossref] [Google Scholar]
  86. 86.
    Kronholm I, Picó FX, Alonso-Blanco C, Goudet J, de Meaux J. 2012.. Genetic basis of adaptation in Arabidopsis thaliana: local adaptation at the seed dormancy QTL DOG1. . Evolution 66:(7):2287302
    [Crossref] [Google Scholar]
  87. 87.
    Lande R, Arnold SJ. 1983.. The measurement of selection on correlated characters. . Evolution 37:(6):121026
    [Crossref] [Google Scholar]
  88. 88.
    Lang PLM, Erberich JM, Lopez L, Weiß CL, Amador G, et al. 2024.. Century-long timelines of herbarium genomes predict plant stomatal response to climate change. . Nat. Ecol. Evol. 8::164153
    [Crossref] [Google Scholar]
  89. 89.
    LaRue T, Lindner H, Srinivas A, Exposito-Alonso M, Lobet G, Dinneny JR. 2022.. Uncovering natural variation in root system architecture and growth dynamics using a robotics-assisted phenomics platform. . eLife 11::e76968
    [Crossref] [Google Scholar]
  90. 90.
    Lee C-R, Svardal H, Farlow A, Exposito-Alonso M, Ding W, et al. 2017.. On the post-glacial spread of human commensal Arabidopsis thaliana. . Nat. Commun. 8::14458
    [Crossref] [Google Scholar]
  91. 91.
    Lee TA, Nobori T, Illouz-Eliaz N, Xu J, Jow B, et al. 2023.. A single-nucleus atlas of seed-to-seed development in Arabidopsis. . bioRxiv 2023.03.23.533992. https://www.biorxiv.org/content/10.1101/2023.03.23.533992v1
  92. 92.
    Leimu R, Fischer M. 2008.. A meta-analysis of local adaptation in plants. . PLOS ONE 3:(12):e4010
    [Crossref] [Google Scholar]
  93. 93.
    Leventhal L, Ruffley M, Exposito-Alonso M. 2025.. Climate Change Evolution Experiment: data from Arabidopsis thaliana Common Garden at Carnegie Institution for Science at Stanford University (0.0) [Data set]. . Zenodo. https://doi.org/10.5281/zenodo.14728818
    [Google Scholar]
  94. 94.
    Lian Q, Huettel B, Walkemeier B, Mayjonade B, Lopez-Roques C, et al. 2024.. A pan-genome of 69 Arabidopsis thaliana accessions reveals a conserved genome structure throughout the global species range. . Nat. Genet. 56:(5):98291
    [Crossref] [Google Scholar]
  95. 95.
    Linhart YB, Grant MC. 1996.. Evolutionary significance of local genetic differentiation in plants. . Annu. Rev. Ecol. Syst. 27::23777
    [Crossref] [Google Scholar]
  96. 96.
    Long Q, Rabanal FA, Meng D, Huber CD, Farlow A, et al. 2013.. Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. . Nat. Genet. 45:(8):88490
    [Crossref] [Google Scholar]
  97. 97.
    Lopez-Arboleda WA, Reinert S, Nordborg M, Korte A. 2021.. Global genetic heterogeneity in adaptive traits. . Mol. Biol. Evol. 38:(11):482231
    [Crossref] [Google Scholar]
  98. 98.
    Ludlow MM. 1989.. Strategies of response to water stress. . In Structural and Functional Responses to Environmental Stresses, ed. KH Kreeb, H Richter, TM Hinkley , pp. 26981 The Hague, Neth:.: SBP Acad. Publ.
    [Google Scholar]
  99. 99.
    Manzano-Piedras E, Marcer A, Alonso-Blanco C, Picó FX. 2014.. Deciphering the adjustment between environment and life history in annuals: lessons from a geographically-explicit approach in Arabidopsis thaliana. . PLOS ONE 9:(2):e87836
    [Crossref] [Google Scholar]
  100. 100.
    Martínez-Berdeja A, Stitzer MC, Taylor MA, Okada M, Ezcurra E, et al. 2020.. Functional variants of DOG1 control seed chilling responses and variation in seasonal life-history strategies in Arabidopsis thaliana. . PNAS 117:(5):252634
    [Crossref] [Google Scholar]
  101. 101.
    Mauricio R, Rausher MD, Burdick DS. 1997.. Variation in the defense strategies of plants: Are resistance and tolerance mutually exclusive?. Ecology 78:(5):130111
    [Crossref] [Google Scholar]
  102. 102.
    McKay JK, Richards JH, Nemali KS, Sen S, Mitchell-Olds T, et al. 2008.. Genetics of drought adaptation in Arabidopsis thaliana II. QTL analysis of a new mapping population, KAS-1 × TSU-1. . Evolution 62:(12):301426
    [Crossref] [Google Scholar]
  103. 103.
    Méndez-Vigo B, Castilla AR, Gómez R, Marcer A, Alonso-Blanco C, Picó FX. 2022.. Spatiotemporal dynamics of genetic variation at the quantitative and molecular levels within a natural Arabidopsis thaliana population. . J. Ecol. 110:(11):270116
    [Crossref] [Google Scholar]
  104. 104.
    Méndez-Vigo B, Gomaa NH, Alonso-Blanco C, Picó XF. 2013.. Among- and within-population variation in flowering time of Iberian Arabidopsis thaliana estimated in field and glasshouse conditions. . New Phytol. 197:(4):133243
    [Crossref] [Google Scholar]
  105. 105.
    Méndez-Vigo B, Picó FX, Ramiro M, Martínez-Zapater JM, Alonso-Blanco C. 2011.. Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. . Plant Physiol. 157:(4):194255
    [Crossref] [Google Scholar]
  106. 106.
    Mitchell-Olds T. 1996.. Genetic constraints on life-history evolution: quantitative-trait loci influencing growth and flowering in Arabidopsis thaliana. . Evolution 50:(1):14045
    [Google Scholar]
  107. 107.
    Mojica JP, Mullen J, Lovell JT, Monroe JG, Paul JR, et al. 2016.. Genetics of water use physiology in locally adapted Arabidopsis thaliana. . Plant Sci. 251::1222
    [Crossref] [Google Scholar]
  108. 108.
    Montesinos-Navarro A, Picó FX, Tonsor SJ. 2012.. Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana. . Evolution 66:(11):341731
    [Crossref] [Google Scholar]
  109. 109.
    Mosleh Arany A, de Jong TJ, van der Meijden E. 2009.. Herbivory and local genetic differentiation in natural populations of Arabidopsis thaliana (Brassicaceae). . Plant Ecol. 201:(2):65159
    [Crossref] [Google Scholar]
  110. 110.
    Murren CJ, Denning W, Pigliucci M. 2005.. Relationships between vegetative and life history traits and fitness in a novel field environment: impacts of herbivores. . Evol. Ecol. 19:(6):583601
    [Crossref] [Google Scholar]
  111. 111.
    Nasser J, Bergman DT, Fulco CP, Guckelberger P, Doughty BR, et al. 2021.. Genome-wide enhancer maps link risk variants to disease genes. . Nature 593:(7858):23843
    [Crossref] [Google Scholar]
  112. 112.
    Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, et al. 2002.. The extent of linkage disequilibrium in Arabidopsis thaliana. . Nat. Genet. 30:(2):19093
    [Crossref] [Google Scholar]
  113. 113.
    Oakley CG, Ågren J, Atchison RA, Schemske DW. 2014.. QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs. . Mol. Ecol. 23:(17):430415
    [Crossref] [Google Scholar]
  114. 114.
    O'Malley RC, Huang S-SC, Song L, Lewsey MG, Bartlett A, et al. 2016.. Cistrome and epicistrome features shape the regulatory DNA landscape. . Cell 165:(5):128092. Erratum . 2016.. Cell 166:(6):1598
    [Google Scholar]
  115. 115.
    Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D. 2008.. Sequencing of natural strains of Arabidopsis thaliana with short reads. . Genome Res. 18:(12):202433
    [Crossref] [Google Scholar]
  116. 116.
    Picó FX. 2012.. Demographic fate of Arabidopsis thaliana cohorts of autumn- and spring-germinated plants along an altitudinal gradient. . J. Ecol. 100:(4):100918
    [Crossref] [Google Scholar]
  117. 117.
    Pigliucci M. 2002.. Ecology and evolutionary biology of Arabidopsis. . Arabidopsis Book 1::e0003
    [Crossref] [Google Scholar]
  118. 118.
    Piskurewicz U, Iwasaki M, Susaki D, Megies C, Kinoshita T, Lopez-Molina L. 2016.. Dormancy-specific imprinting underlies maternal inheritance of seed dormancy in Arabidopsis thaliana. . eLife 5::e19573
    [Crossref] [Google Scholar]
  119. 119.
    Platt A, Horton M, Huang YS, Li Y, Anastasio AE, et al. 2010.. The scale of population structure in Arabidopsis thaliana. . PLOS Genet. 6:(2):e1000843
    [Crossref] [Google Scholar]
  120. 120.
    Postma FM, Ågren J. 2016.. Early life stages contribute strongly to local adaptation in Arabidopsis thaliana. . PNAS 113:(27):759095
    [Crossref] [Google Scholar]
  121. 121.
    Postma FM, Ågren J. 2018.. Among-year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana. . Mol. Ecol. 27:(11):2498511
    [Crossref] [Google Scholar]
  122. 122.
    Provart NJ, Alonso J, Assmann SM, Bergmann D, Brady SM, et al. 2016.. 50 years of Arabidopsis research: highlights and future directions. . New Phytol. 209:(3):92144
    [Crossref] [Google Scholar]
  123. 123.
    Przybylska MS, Violle C, Vile D, Scheepens JF, Lacombe B, et al. 2023.. AraDiv: a dataset of functional traits and leaf hyperspectral reflectance of Arabidopsis thaliana. . Sci. Data 10::314
    [Crossref] [Google Scholar]
  124. 124.
    Rabanal FA, Gräff M, Lanz C, Fritschi K, Llaca V, et al. 2022.. Pushing the limits of HiFi assemblies reveals centromere diversity between two Arabidopsis thaliana genomes. . Nucleic Acids Res. 50:(21):1230927
    [Crossref] [Google Scholar]
  125. 125.
    Ratcliffe D. 1961.. Adaptation to habitat in a group of annual plants. . J. Ecol. 49:(1):187203
    [Crossref] [Google Scholar]
  126. 126.
    Rédei GP. 1975.. Arabidopsis as a genetic tool. . Annu. Rev. Genet. 9::11127
    [Crossref] [Google Scholar]
  127. 127.
    Rédei GP. 1992.. A heuristic glance at the past of Arabidopsis genetics. . In Methods in Arabidopsis Research, ed. C Koncz, N-H Chua, J Schell , pp. 115. Singapore:: World Sci.
    [Google Scholar]
  128. 128.
    Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, et al. 2003.. The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. . Nucleic Acids Res. 31:(1):22428
    [Crossref] [Google Scholar]
  129. 129.
    Rodríguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB. 2017.. Engineering quantitative trait variation for crop improvement by genome editing. . Cell 171:(2):47080.e8
    [Crossref] [Google Scholar]
  130. 130.
    Ruffley M, Lutz U, Leventhal L, Hateley S, Yuan W, 2024.. Selection constraints of plant adaptation can be relaxed by gene editing. . bioRxiv 2023.10.16.562583. https://www.biorxiv.org/content/10.1101/2023.10.16.562583v2
  131. 131.
    Sajeev N, Koornneef M, Bentsink L. 2024.. A commitment for life: decades of unraveling the molecular mechanisms behind seed dormancy and germination. . Plant Cell 36:(5):135876
    [Crossref] [Google Scholar]
  132. 132.
    Samis KE, Murren CJ, Bossdorf O, Donohue K, Fenster CB, et al. 2012.. Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana. . Ecol. Evol. 2:(6):116280
    [Crossref] [Google Scholar]
  133. 133.
    Samis KE, Stinchcombe JR, Murren CJ. 2019.. Population climatic history predicts phenotypic responses in novel environments for Arabidopsis thaliana in North America. . Am. J. Bot. 106:(8):106880
    [Crossref] [Google Scholar]
  134. 134.
    Sasaki E, Köcher T, Filiault DL, Nordborg M. 2021.. Revisiting a GWAS peak in Arabidopsis thaliana reveals possible confounding by genetic heterogeneity. . Heredity 127:(3):24552
    [Crossref] [Google Scholar]
  135. 135.
    Sato Y, Shimizu-Inatsugi R, Yamazaki M, Shimizu KK, Nagano AJ. 2019.. Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana. . BMC Plant Biol. 19::163
    [Crossref] [Google Scholar]
  136. 136.
    Schiffels S, Durbin R. 2014.. Inferring human population size and separation history from multiple genome sequences. . Nat. Genet. 46:(8):91925
    [Crossref] [Google Scholar]
  137. 137.
    Schmitt J, Niles J, Wulff RD. 1992.. Norms of reaction of seed traits to maternal environments in Plantago lanceolata. . Am. Nat. 139:(3):45166
    [Crossref] [Google Scholar]
  138. 138.
    Schmitz RJ, Schultz MD, Urich MA, Nery JR, Pelizzola M, et al. 2013.. Patterns of population epigenomic diversity. . Nature 495:(7440):19398
    [Crossref] [Google Scholar]
  139. 139.
    Schultz ST, Lynch M, Willis JH. 1999.. Spontaneous deleterious mutation in Arabidopsis thaliana. . PNAS 96:(20):1139398
    [Crossref] [Google Scholar]
  140. 140.
    Seren Ü, Grimm D, Fitz J, Weigel D, Nordborg M, et al. 2017.. AraPheno: a public database for Arabidopsis thaliana phenotypes. . Nucleic Acids Res. 45:(D1):D105459
    [Crossref] [Google Scholar]
  141. 141.
    Seren Ü, Vilhjálmsson BJ, Horton MW, Meng D, Forai P, et al. 2012.. GWAPP: a web application for genome-wide association mapping in Arabidopsis. . Plant Cell 24:(12):4793805
    [Crossref] [Google Scholar]
  142. 142.
    Sharbel TF, Haubold B, Mitchell-Olds T. 2000.. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. . Mol. Ecol. 9:(12):210918
    [Crossref] [Google Scholar]
  143. 143.
    Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, et al. 2005.. Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. . Plant Physiol. 138:(2):116373
    [Crossref] [Google Scholar]
  144. 144.
    Simons YB, Bullaughey K, Hudson RR, Sella G. 2018.. A population genetic interpretation of GWAS findings for human quantitative traits. . PLOS Biol. 16:(3):e2002985
    [Crossref] [Google Scholar]
  145. 145.
    Singh A, Roy S. 2017.. High altitude population of Arabidopsis thaliana is more plastic and adaptive under common garden than controlled condition. . BMC Ecol. 17:(1):39
    [Crossref] [Google Scholar]
  146. 146.
    Somerville C, Koornneef M. 2002.. A fortunate choice: the history of Arabidopsis as a model plant. . Nat. Rev. Genet. 3:(11):88389
    [Crossref] [Google Scholar]
  147. 147.
    Somssich M. 2019.. A short history of Arabidopsis thaliana (L.) Heynh. Columbia-0. . PeerJ Prepr. 7:e26931v5
    [Google Scholar]
  148. 148.
    Song S, He H, Gühl K, van Bolderen-Veldkamp M, Buijs G, et al. 2021.. DELAY OF GERMINATION 6, encoding the ANAC060 transcription factor, inhibits seed dormancy. . bioRxiv 2021.05.03.442418. https://www.biorxiv.org/content/10.1101/2021.05.03.442418v1.full
  149. 149.
    Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, et al. 2004.. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. . PNAS 101:(13):471217
    [Crossref] [Google Scholar]
  150. 150.
    Stuttmann J, Barthel K, Martin P, Ordon J. 2021.. Highly efficient multiplex editing: one-shot generation of 8× Nicotiana benthamiana and 12× Arabidopsis mutants. . Plant J. 106:(1):822
    [Crossref] [Google Scholar]
  151. 151.
    Tabas-Madrid D, Méndez-Vigo B, Arteaga N, Marcer A, Pascual-Montano A, et al. 2018.. Genome-wide signatures of flowering adaptation to climate temperature: Regional analyses in a highly diverse native range of Arabidopsis thaliana. . Plant Cell Environ. 41:(8):180620
    [Crossref] [Google Scholar]
  152. 152.
    Taylor MA, Cooper MD, Sellamuthu R, Braun P, Migneault A, et al. 2017.. Interacting effects of genetic variation for seed dormancy and flowering time on phenology, life history, and fitness of experimental Arabidopsis thaliana populations over multiple generations in the field. . New Phytol. 216:(1):291302
    [Crossref] [Google Scholar]
  153. 153.
    Tergemina E, Elfarargi AF, Flis P, Fulgione A, Göktay M, et al. 2022.. A two-step adaptive walk rewires nutrient transport in a challenging edaphic environment. . Sci. Adv. 8:(20):eabm9385
    [Crossref] [Google Scholar]
  154. 154.
    Todesco M, Balasubramanian S, Hu TT, Traw MB, Horton M, et al. 2010.. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. . Nature 465:(7298):63236
    [Crossref] [Google Scholar]
  155. 155.
    Togninalli M, Seren Ü, Meng D, Fitz J, Nordborg M, et al. 2018.. The AraGWAS Catalog: a curated and standardized Arabidopsis thaliana GWAS catalog. . Nucleic Acids Res. 46:(D1):D115056
    [Crossref] [Google Scholar]
  156. 156.
    Toledo B, Marcer A, Méndez-Vigo B, Alonso-Blanco C, Picó FX. 2019.. An ecological history of the relict genetic lineage of Arabidopsis thaliana. . Environ. Exp. Bot. 170::103800
    [Crossref] [Google Scholar]
  157. 157.
    Turesson G. 1925.. The plant species in relation to habitat and climate. . Hereditas 6:(2):147236
    [Crossref] [Google Scholar]
  158. 158.
    Vasseur F, Bresson J, Wang G, Schwab R, Weigel D. 2018.. Image-based methods for phenotyping growth dynamics and fitness components in Arabidopsis thaliana. . Plant Methods 14::63
    [Crossref] [Google Scholar]
  159. 159.
    Vasseur F, Sartori K, Baron E, Fort F, Kazakou E, et al. 2018.. Climate as a driver of adaptive variations in ecological strategies in Arabidopsis thaliana. . Ann. Bot. 122:(6):93545
    [Google Scholar]
  160. 160.
    Vidigal DS, Marques ACSS, Willems LAJ, Buijs G, Méndez-Vigo B, et al. 2016.. Altitudinal and climatic associations of seed dormancy and flowering traits evidence adaptation of annual life cycle timing in Arabidopsis thaliana. . Plant Cell Environ. 39:(8):173748
    [Crossref] [Google Scholar]
  161. 161.
    Visscher PM, Wray NR, Zhang Q, Sklar P, McCarthy MI, et al. 2017.. 10 years of GWAS discovery: biology, function, and translation. . Am. J. Hum. Genet. 101:(1):522
    [Crossref] [Google Scholar]
  162. 162.
    Voichek Y, Weigel D. 2020.. Identifying genetic variants underlying phenotypic variation in plants without complete genomes. . Nat. Genet. 52::53440
    [Crossref] [Google Scholar]
  163. 163.
    Warthmann N, Fitz J, Weigel D. 2007.. MSQT for choosing SNP assays from multiple DNA alignments. . Bioinformatics 23:(20):278487
    [Crossref] [Google Scholar]
  164. 164.
    Weigel D. 2012.. Natural variation in Arabidopsis: from molecular genetics to ecological genomics. . Plant Physiol. 158:(1):222
    [Crossref] [Google Scholar]
  165. 165.
    Weigel D, Mott R. 2009.. The 1001 Genomes Project for Arabidopsis thaliana. . Genome Biol. 10:(5):107
    [Crossref] [Google Scholar]
  166. 166.
    Weigel D, Nordborg M. 2015.. Population genomics for understanding adaptation in wild plant species. . Annu. Rev. Genet. 49::31538
    [Crossref] [Google Scholar]
  167. 167.
    Westerman JM, Lawrence MJ. 1970.. Genotype-environment interaction and developmental regulation in Arabidopsis thaliana I. Inbred lines; description. . Heredity 25:(4):60927
    [Crossref] [Google Scholar]
  168. 168.
    Wilczek AM, Cooper MD, Korves TM, Schmitt J. 2014.. Lagging adaptation to warming climate in Arabidopsis thaliana. . PNAS 111:(22):790613
    [Crossref] [Google Scholar]
  169. 169.
    Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, et al. 2009.. Effects of genetic perturbation on seasonal life history plasticity. . Science 323:(5916):93034
    [Crossref] [Google Scholar]
  170. 170.
    Wu X, Jiang W, Fragoso C, Huang J, Zhou G, et al. 2022.. Prioritized candidate causal haplotype blocks in plant genome-wide association studies. . PLOS Genet. 18:(10):e1010437
    [Crossref] [Google Scholar]
  171. 171.
    Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, et al. 2006.. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. . Nat. Genet. 38:(2):2038
    [Crossref] [Google Scholar]
  172. 172.
    Zhou X, Carbonetto P, Stephens M. 2013.. Polygenic modeling with Bayesian sparse linear mixed models. . PLOS Genet. 9:(2):e1003264
    [Crossref] [Google Scholar]
  173. 173.
    Zhu H, Li C, Gao C. 2020.. Applications of CRISPR-Cas in agriculture and plant biotechnology. . Nat. Rev. Mol. Cell Biol. 21:(11):66177
    [Crossref] [Google Scholar]
  174. 174.
    Zou Y-P, Hou X-H, Wu Q, Chen J-F, Li Z-W, et al. 2017.. Adaptation of Arabidopsis thaliana to the Yangtze River basin. . Genome Biol. 18:(1):239
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-arplant-071123-095146
Loading
/content/journals/10.1146/annurev-arplant-071123-095146
Loading

Data & Media loading...

Supplemental Materials

Supplemental Materials

Supplemental Materials

Supplemental Materials

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error