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Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations

Abstract

Forest trees are dominant components of terrestrial ecosystems that have global ecological and economic importance. Despite distributions that span wide environmental gradients, many tree populations are locally adapted, and mechanisms underlying this adaptation are poorly understood. Here we use a combination of whole-genome selection scans and association analyses of 544 Populus trichocarpa trees to reveal genomic bases of adaptive variation across a wide latitudinal range. Three hundred ninety-seven genomic regions showed evidence of recent positive and/or divergent selection and enrichment for associations with adaptive traits that also displayed patterns consistent with natural selection. These regions also provide unexpected insights into the evolutionary dynamics of duplicated genes and their roles in adaptive trait variation.

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Figure 1: Geographic locations and genetic structure of the 544 P. trichocarpa individuals sequenced.
Figure 2: Phenotypic evidence of climate-driven selection in P. trichocarpa.
Figure 3: Unique and shared genomic regions among five selection scans.
Figure 4: The selection outliers have a stronger association signal with adaptive traits than that expected by chance.
Figure 5: A region of chromosome 10 shows an abundance of bud flush association and strong evidence of selection from multiple selection scans.
Figure 6: A region of chromosome 8 shows multiple strong bud flush associations and evidence of positive selection.

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Acknowledgements

We thank the members of BioEnergy Science Center for their varied contributions to this work, and especially those involved in the collection, propagation and maintenance of the common gardens, including G. Howe, A. Groover, R. Stettler, J. Johnson and the staff at Mt. Jefferson Farms and Greenwood Resources. We thank the West Virginia University High Performance Computing facility, in particular N. Gregg and M. Carlise. P. balsamifera transcriptomes were provided by M. Olson (Texas Tech University). This work was supported by funding from the BioEnergy Science Center, a US Department of Energy (DOE) Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. A.M.B. acknowledges support from the Virginia Agricultural Experiment Station and the McIntire Stennis Program of the National Institute of Food and Agriculture, US Department of Agriculture.

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G.A.T., S.P.D., G.T.S. and L.M.E. conceived and designed the study. All authors performed measurements. L.G., J.M. and W.S. performed sequencing. L.M.E., S.P.D., G.T.S., E. R.-M., J.M., P.R., W.M. and W.S. performed analyses. L.M.E., S.P.D. and A.M.B. drafted the manuscript. All authors read, revised, and approved the manuscript.

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Correspondence to Stephen P DiFazio.

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Supplementary Figures 1–18 and Supplementary Note. (PDF 12507 kb)

Supplementary Tables 1–12, 14 and 15 (XLSX 2709 kb)

Supplementary Table 13

List of SNPs and their associated P values for phenotypic associations as determined by the emmax mixed model analysis. The nearest predicted gene is listed, as well as annotations of predicted SNP effects for those that fall within genes, as determined by the SNPeff program. When a SNP lies within two or more genes, additional distance to gene and gene model columns are added before the snpEFF annotation column. (XLSX 5856 kb)

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Evans, L., Slavov, G., Rodgers-Melnick, E. et al. Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nat Genet 46, 1089–1096 (2014). https://doi.org/10.1038/ng.3075

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