The population genetics of structural variants in grapevine domestication

Abstract

Structural variants (SVs) are a largely unexplored feature of plant genomes. Little is known about the type and size of SVs, their distribution among individuals and, especially, their population dynamics. Understanding these dynamics is critical for understanding both the contributions of SVs to phenotypes and the likelihood of identifying them as causal genetic variants in genome-wide associations. Here, we identify SVs and study their evolutionary genomics in clonally propagated grapevine cultivars and their outcrossing wild progenitors. To catalogue SVs, we assembled the highly heterozygous Chardonnay genome, for which one in seven genes is hemizygous based on SVs. Using an integrative comparison between Chardonnay and Cabernet Sauvignon genomes by whole-genome, long-read and short-read alignment, we extended SV detection to population samples. We found that strong purifying selection acts against SVs but particularly against inversion and translocation events. SVs nonetheless accrue as recessive heterozygotes in clonally propagated lineages. They also define outlier regions of genomic divergence between wild and cultivated grapevines, suggesting roles in domestication. Outlier regions include the sex-determination region and the berry colour locus, where independent large, complex inversions have driven convergent phenotypic evolution.

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Fig. 1: Structural heterozygosity in Char04 and comparisons of structural variation between Char04 and Cab08.
Fig. 2: SVs are strongly deleterious and under purifying selection.
Fig. 3: Population genetics of SVs associated with grapevine domestication.
Fig. 4: Haplotypes of the sex region and the evolution of sex in grapevine.
Fig. 5: Convergent evolution of inversions associated with white berries.

Data availability

Raw SMRT reads for were deposited to the SRA at the NCBI under the BioProject ID PRJNA550461. Genome assembly and annotation of genes and transposable elements are available at https://zenodo.org/record/3337377#.XS0i9ZOpG_M. VCFs and custom scripts are available on request.

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Acknowledgements

We are grateful for the technical assistance of R. Gaut and R. Figueroa-Balderas, the services of the High Performance Computing Cluster and the Genomics High Throughput Facility at UC Irvine, and the comments of A. Muyle, D. Seymour, D. Koenig, T. Batarseh, G. Martin, P. Morrell and J. Ross-Ibarra. This work was supported by seed funding from UC Irvine, NSF grant no. 1542703 to B.S.G., NSF grant no. 1741627 to B.S.G. and D.C. and support to D.C. by J. Lohr Vineyards and Wines, E. & J. Gallo Winery and the Louis P. Martini Endowment in Viticulture.

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Y.Z., D.C. and B.S.G. designed the research. Y.Z., D.C. and B.S.G. wrote the manuscript. Y.Z., A.M., M.M., E.S. and Y.L. performed the analyses. T.B. provided data.

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Correspondence to Dario Cantu or Brandon S. Gaut.

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Peer review information: Nature Plants thanks Briana Gross and other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Zhou, Y., Minio, A., Massonnet, M. et al. The population genetics of structural variants in grapevine domestication. Nat. Plants 5, 965–979 (2019). https://doi.org/10.1038/s41477-019-0507-8

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