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. 2021 Dec 21;12(1):7240.
doi: 10.1038/s41467-021-27487-y.

The genomes of 204 Vitis vinifera accessions reveal the origin of European wine grapes

Affiliations

The genomes of 204 Vitis vinifera accessions reveal the origin of European wine grapes

Gabriele Magris et al. Nat Commun. .

Abstract

In order to elucidate the still controversial processes that originated European wine grapes from its wild progenitor, here we analyse 204 genomes of Vitis vinifera and show that all analyses support a single domestication event that occurred in Western Asia and was followed by numerous and pervasive introgressions from European wild populations. This admixture generated the so-called international wine grapes that have diffused from Alpine countries worldwide. Across Europe, marked differences in genomic diversity are observed in local varieties that are traditionally cultivated in different wine producing countries, with Italy and France showing the largest diversity. Three genomic regions of reduced genetic diversity are observed, presumably as a consequence of artificial selection. In the lowest diversity region, two candidate genes that gained berry-specific expression in domesticated varieties may contribute to the change in berry size and morphology that makes the fruit attractive for human consumption and adapted for winemaking.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Split and admixture events in groups defined by population structure in the WGS panel (a) and by geographic distribution in the diversity panel (b).
a Maximum likelihood (ML) tree with four groups of cultivated varieties (Supplementary Fig. 10) and four groups of wild accessions (Supplementary Fig. 7). Ancestry composition and group sizes are illustrated in Supplementary Fig. 10. b ML tree with nine groups of cultivated varieties and seven populations of sylvestris. Ancestry composition, group sizes, explained variance and the description of sylvestrissylvestris admixture are given in Supplementary Fig. 22. a, b Migration events are indicated by colored arrows. The color scale shows the migration weight. The scale bar shows ten times the average standard error of the estimated entries in the sample covariance matrix. Bold lines indicate the sylvestris branches of the tree. Trees represent random trees and numbers represent bootstrap support values above 70% (100 iterations) before adding migrations. Support for the migration events and the resulting predictive model is given in Supplementary Figs. 20 and  22c, Supplementary Table 1, and Supplementary Data 2.
Fig. 2
Fig. 2. Chromosomal patterns of gene flow from western sylvestris into table grapes generating Alpine wine grapes.
a Dots represent adjusted fd values in 100 Kb windows of non-repetitive DNA. Lines represent cubic smoothing splines of the values. b Diagram of 100 Kb chromosomal windows (in red) that show phylogenetic tree topologies with shorter genetic distance between Alpine wine grapes and western sylvestris than between Alpine wine grapes and any other cultivated group. Red triangles in a and constricted regions in b indicate the location of centromeric repeats. Source data are provided as a Source Data file.
Fig. 3
Fig. 3. Principal component analysis (PCA) in the WGS panel (a) and in the diversity panel (b).
a PCA of 204 V. vinifera whole genome resequenced genotypes based on 7.9 M SNPs. b PCA of 1445 V. vinifera genotypes based on a subset of 6357 pre-ascertained SNPs in the diversity panel and in common with the WGS panel. Sequenced samples are indicated as open (cultivated varieties) and solid (wild accessions) squares. Additional cultivated varieties are indicated as gray crosses in b. Samples with uncertain assignment in their literature reports are reported as “faux sauvage”: 1, sylvestris FR B00ERBY; 2, KE–06; 3, Vigne sauvage faux “Mouchouses 1”; 4, “Tighzirt 1”; 5, “Fethiye 58 64” and collectively indicated as solid circles in b. The 2-letter codes (αβ) indicate countries of origin: CH Switzerland, DE Germany, DZ Algeria, ES Spain, FR France, GE Georgia, GR Greece, HU Hungary, IT Italy, MA Morocco, SK Slovakia, TN Tunisia, TR Turkey. Source data are provided as a Source Data file.
Fig. 4
Fig. 4. Ancestry versus geography.
Continental patterns of ancestry components in cultivated (a) and wild (b) grapevines and nationwide patterns of wine grape ancestry in the top five wine–producing countries in Europe (c, d). Colors represent W2 ancestry (blue), C1 ancestry (orange), C2 ancestry (gray), and W1 ancestry (yellow). Each ancestry component is plotted separately (a, b). Intensity of the main ancestry component is plotted (c). Overlay of all ancestry components is plotted (d). The collection site of wild accessions is indicated by black dots (b). The most representative site of cultivation of each variety is indicate by black dots (c, d). Abbreviations of top wine-producing countries: Italy IT, France FR, Spain ES, Germany DE, Portugal PT. Source data are provided as a Source Data file.
Fig. 5
Fig. 5. Selective sweep on chromosome 17 and allele specific expression (ASE) of the LRR–receptor kinase VIT_217s0000g05570.
a Chromosomal plot of haplotype diversity. Haplotype diversity was calculated in blocks of five consecutive variant sites and plotted as the average of 50 consecutive blocks (blue dots) and a cubic smoothing spline (black line). The scale indicates Mb. The yellow background indicate the interval magnified in b. b V2.1 gene models (exons in blue), manually curated gene predictions (green) in the isopiperitenol/carveol dehydrogenase gene cluster (gene IDs 7 → 11), annotated transposable elements (light gray). c Frequency of 19 haplotypes shown in Supplementary Fig. 38 in 196 grapevine accessions. d Genotype frequency in 121 cultivated varieties. e VIT_217s0000g05570 (gene 6 in b) gene phylogeny. Numbers indicate the proportion of bootstrap trees supporting that clade. f ASE of the LRR–receptor kinase VIT_217s0000g05570 alleles in representative varieties of 15 haplotypic combinations, in softening berries (lower panel) and leaves (upper panel). The asterisks indicate statistically significant ASE levels (p-value <0.05) according to a Stouffer’s meta-analysis with weight and direction effect using n = 2 biologically independent samples. Cumulative expression is reported for each haplotypic combination lacking exonic SNPs in VIT_217s0000g05570 (H1-A/H1-G, H1-A/H10, H1-A/AX) and for a control variety homozygous for the H1-A haplotype. Gene expression for three haplotype combinations (H1-A/H10, H1-A/H6, H1-A/H4) was quantified in leaves of three different representative varieties (Tschvediansis Tetra, Picolit, Lambrusco Grasparossa) with the same genotype with respect to those used for berry gene expression. Source data of gene expression are provided as a Source Data file.
Fig. 6
Fig. 6. Association analysis between SNPs and seed-to-berry ratio at the onset of berry ripening.
a Association between a A → T mutation in the VIT_217s0000g05570 gene, which recapitulate the increase in berry–specific expression of the kinase, and seed-to-berry ratio in hard berries prior to softening, soft berries collected over the same bunch and their average (as a proxy for the end of the first phase of berry growth). Box-plots show 88 accessions (green dots) sorted by their genotype at the SNP_chr17:6,079,793. Accessions with missing AA, AT, TT genotypes were classified based on their alternate/alternate, alternate/reference and reference/reference genotypes, respectively, at the variant sites chr17:6,080,166; 6,079,793; 6,080,193; 6,080,258; 6,080,447; 6,080,449, which are all in LD with chr17: 6,079,793 in the H1-A haplotype. b Variation in soluble solids concentration in the same berries and accessions as in a. Red dots indicate values in hard berries of sylvestris V395. Yellow dots indicate values in eastern feral grapes. Cyan dots indicate values in Berzamino and Gordin Verde. Boxes indicate the first and third quartiles, the horizontal line within the boxes indicates the median and the whiskers indicate ±1.5 × interquartile range. Source data are provided as a Source Data file.

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