Genetic structure and domestication history of the grape

Abstract

The grape is one of the earliest domesticated fruit crops and, since antiquity, it has been widely cultivated and prized for its fruit and wine. Here, we characterize genome-wide patterns of genetic variation in over 1,000 samples of the domesticated grape, Vitis vinifera subsp. vinifera, and its wild relative, V. vinifera subsp. sylvestris from the US Department of Agriculture grape germplasm collection. We find support for a Near East origin of vinifera and present evidence of introgression from local sylvestris as the grape moved into Europe. High levels of genetic diversity and rapid linkage disequilibrium (LD) decay have been maintained in vinifera, which is consistent with a weak domestication bottleneck followed by thousands of years of widespread vegetative propagation. The considerable genetic diversity within vinifera, however, is contained within a complex network of close pedigree relationships that has been generated by crosses among elite cultivars. We show that first-degree relationships are rare between wine and table grapes and among grapes from geographically distant regions. Our results suggest that although substantial genetic diversity has been maintained in the grape subsequent to domestication, there has been a limited exploration of this diversity. We propose that the adoption of vegetative propagation was a double-edged sword: Although it provided a benefit by ensuring true breeding cultivars, it also discouraged the generation of unique cultivars through crosses. The grape currently faces severe pathogen pressures, and the long-term sustainability of the grape and wine industries will rely on the exploitation of the grape's tremendous natural genetic diversity.

Fig. 1.

Clonal relationships within the USDA grape germplasm collection. (A) Number of clonal relationships was evaluated for each of the 950 vinifera accessions. Most of the accessions [551 (58%) of 950 accessions] have a clonal relationship with at least 1 other accession. (B) Degree of clonal relatedness among all 950 vinifera accessions is represented as a set of clusters. The 399 accessions that do not have a clonal relationship with another accession are shown as lone black dots. Accessions with six or fewer clonal relationships are grouped together with their clones and shown in gray. Clusters of clones with ≥7 accessions are colored, and their names are indicated in the legend. Names listed in the legend are the prime names from the Vitis International Variety Catalogue (http://www.vivc.de/).

Fig. 2.

First-degree relationships within the USDA grape germplasm collection. (A) Number of first-degree relationships was evaluated for each of the 583 unique vinifera cultivars. A total of 74.8% of the unique cultivars are related to at least 1 other cultivar by a first-degree relationship, and some cultivars have many first-degree relationships (i.e., >10; SI Appendix, Table S4). (B) Pedigree structure of vinifera is represented as a set of networks. Edges in the network represent inferred first-degree relationships. The vertices, or dots, represent grape cultivars and are colored by grape type (legend). The sample size of each grape type is shown in parentheses. Lone dots represent cultivars with no first-degree relatives in the dataset. Note that one single interconnected network is clearly visible and includes 384 (58.3%) of the 583 unique cultivars that are interconnected by a series of first-degree relationships.

Fig. 3.

Network of first-degree relationships among common grape cultivars. Solid vertices represent likely parent-offspring relationships. Dotted vertices represent sibling relationships or equivalent. Arrows point from parents to offspring for inferred trios (details are provided in Materials and Methods).

Fig. 4.

Visualization of genetic relationships among sylvestris and vinifera. PC axis 1 (PC1) and PC2 were calculated from 59 sylvestris samples, and 570 vinifera samples were subsequently projected onto these axes. The proportion of the variance explained by each PC is shown in parentheses along each axis. The vinifera samples are represented by circles, and their origins are indicated in the legend. The countries or regions of origin of the sylvestris samples are represented by two-letter codes provided in the legend.