Evolutionary genomics of grape (Vitis vinifera ssp. vinifera) domestication
Edited by Andrew G. Clark, Cornell University, Ithaca, NY, and approved September 25, 2017 (received for review June 5, 2017)
Significance
We generated genomic data to estimate the population history of grapes, the most economically important horticultural crop in the world. Domesticated grapes experienced a protracted, 22,000-y population decline prior to domestication; we hypothesize that this decline reflects low-intensity cultivation by humans prior to domestication. Domestication altered the mating system of grapes. The sex determination region is detectable as a region of heightened genetic divergence between wild and cultivated accessions. Based on gene expression analyses, we propose candidate genes that alter sex determination. Finally, grapes contain more deleterious mutations in heterozygous states than do their wild ancestors. The accumulation of deleterious mutations is due in part to clonal propagation, which shelters deleterious recessive mutations.
Abstract
We gathered genomic data from grapes (Vitis vinifera ssp. vinifera), a clonally propagated perennial crop, to address three ongoing mysteries about plant domestication. The first is the duration of domestication; archaeological evidence suggests that domestication occurs over millennia, but genetic evidence indicates that it can occur rapidly. We estimated that our wild and cultivated grape samples diverged ∼22,000 years ago and that the cultivated lineage experienced a steady decline in population size (Ne) thereafter. The long decline may reflect low-intensity management by humans before domestication. The second mystery is the identification of genes that contribute to domestication phenotypes. In cultivated grapes, we identified candidate-selected genes that function in sugar metabolism, flower development, and stress responses. In contrast, candidate-selected genes in the wild sample were limited to abiotic and biotic stress responses. A genomic region of high divergence corresponded to the sex determination region and included a candidate male sterility factor and additional genes with sex-specific expression. The third mystery concerns the cost of domestication. Annual crops accumulate putatively deleterious variants, in part due to strong domestication bottlenecks. The domestication of perennial crops differs from that of annuals in several ways, including the intensity of bottlenecks, and it is not yet clear if they accumulate deleterious variants. We found that grape accessions contained 5.2% more deleterious variants than wild individuals, and these were more often in a heterozygous state. Using forward simulations, we confirm that clonal propagation leads to the accumulation of recessive deleterious mutations but without decreasing fitness.
Data Availability
Data deposition: The sequence reported in this paper has been deposited in the National Center for Biotechnology Information Sequence Read Archive (NCBI SRA) database (accession no. PRJNA388292).
Acknowledgments
We thank R. Gaut and R. Figueroa-Balderas for generating the data and sampling; two anonymous reviewers, D. Seymour, Q. Liu, K. Roessler, and E. Solares provided comments. Y.Z. is supported by the International Postdoctoral Exchange Fellowship Program, J.S. is supported by the National Science Foundation Graduate Research Fellowships Program, and B.S.G. is supported by the Borchard Foundation. D.C. is supported by J. Lohr Vineyards and Wines, E. & J. Gallo Winery, and the Louis P. Martini Endowment.
Supporting Information
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Cover image: Pictured is a developing Arabidopsis thaliana lateral root labeled with a fluorescent transcriptional reporter, with cell outlines shown in blue. Yujuan Du and Ben Scheres found that the PLETHORA transcription factors PLT3, PLT5, and PLT7 regulate the initiation of cell divisions at the start of Arabidopsis lateral root development. According to the authors, PLETHORA transcription factors are key molecular triggers for the establishment of new meristems and tissue differentiation associated with a new growth axis. See the article by Yujuan Du and Ben Scheres on pages 11709–11714. Image courtesy of Yujuan Du.
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Copyright
Copyright © 2017 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
Data Availability
Data deposition: The sequence reported in this paper has been deposited in the National Center for Biotechnology Information Sequence Read Archive (NCBI SRA) database (accession no. PRJNA388292).
Submission history
Published online: October 17, 2017
Published in issue: October 31, 2017
Keywords
Acknowledgments
We thank R. Gaut and R. Figueroa-Balderas for generating the data and sampling; two anonymous reviewers, D. Seymour, Q. Liu, K. Roessler, and E. Solares provided comments. Y.Z. is supported by the International Postdoctoral Exchange Fellowship Program, J.S. is supported by the National Science Foundation Graduate Research Fellowships Program, and B.S.G. is supported by the Borchard Foundation. D.C. is supported by J. Lohr Vineyards and Wines, E. & J. Gallo Winery, and the Louis P. Martini Endowment.
Notes
This article is a PNAS Direct Submission.
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The authors declare no conflict of interest.
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