Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana

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Abstract

As Earth is currently experiencing dramatic climate change, it is of critical interest to understand how species will respond to it. The chance of a species withstanding climate change is likely to depend on the diversity within the species and, particularly, whether there are sub-populations that are already adapted to extreme environments. However, most predictive studies ignore that species comprise genetically diverse individuals. We have identified genetic variants in Arabidopsis thaliana that are associated with survival of an extreme drought event—a major consequence of global warming. Subsequently, we determined how these variants are distributed across the native range of the species. Genetic alleles conferring higher drought survival showed signatures of polygenic adaptation and were more frequently found in Mediterranean and Scandinavian regions. Using geo-environmental models, we predicted that Central European, but not Mediterranean, populations might lag behind in adaptation by the end of the twenty-first century. Further analyses showed that a population decline could nevertheless be compensated by natural selection acting efficiently over standing variation or by migration of adapted individuals from populations at the margins of the species’ distribution. These findings highlight the importance of within-species genetic heterogeneity in facilitating an evolutionary response to a changing climate.

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Fig. 1: Terminal drought treatment and phenotyping of 211 accessions.
Fig. 2: Population structure and history of 762 high-quality genomes.
Fig. 3: aGWA of drought survival and environmental predictions.

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Acknowledgements

We thank R. Wedegärtner for assistance with the greenhouse drought experiment, I. Henderson for the recombination map, and the Petrov, Coop, Ross-Ibarra, Gaut, Schmitt, Weigel and Burbano laboratories for discussions. We thank J. Lasky, X. Picó, A. Hancock, H. Thomassen, T. Mitchell-Olds, J. Mujica, P. Lang and D. Seymour for comments. This work was supported by the President’s Fund of the Max Planck Society, project ‘Darwin’ to H.A.B., as well as central Max Planck Society funds and the European Research Council (AdG IMMUNEMESIS) to D.W.

Author information

M.E.-A. conceived and designed the project. G.W. and F.V. helped with and advised on image phenotyping and F.V. provided additional phenotypes. M.E.-A. and W.D. performed chromosome painter analyses. M.E.-A. performed the drought experiment, processed the image data, and designed and carried out the statistical analyses. D.W. and H.A.B. advised and oversaw the project. M.E.-A. wrote the first draft and, together with H.A.B. and D.W., wrote the final manuscript with input from all authors.

Correspondence to Detlef Weigel.

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Supplementary Information

Supplementary Methods and Supplementary Figures 1–17.

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Supplementary Tables 1–12.

Supplementary Video 1

19-frame time series of green-segmented images for one exemplary tray.

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Exposito-Alonso, M., Vasseur, F., Ding, W. et al. Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana . Nat Ecol Evol 2, 352–358 (2018) doi:10.1038/s41559-017-0423-0

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