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It remains a major challenge to identify the genes and mutations that lead to plant sexual differentiation. Here, we study the structure and evolution of the sex-determining region (SDR) in Vitis species. We report an improved, chromosome-scale Cabernet Sauvignon genome sequence and the phased assembly of nine wild and cultivated grape genomes. By resolving twenty Vitis SDR haplotypes, we compare male, female, and hermaphrodite haplotype structures and identify sex-linked regions. Coupled with gene expression data, we identify a candidate male-sterility mutation in the VviINP1 gene and potential female-sterility function associated with the transcription factor VviYABBY3 . Our data suggest that dioecy has been lost during domestication through a rare recombination event between male and female haplotypes. This work significantly advances the understanding of the genetic basis of sex determination in Vitis and provides the information necessary to rapidly identify sex types in grape breeding programs.

Wild grapevine ( Vitis vinifera subsp. sylvestris ) is widely recognized as an important source of resistance or tolerance genes for diseases and environmental stresses. Recent studies revealed partial resistance to powdery mildew ( Erysiphe necator, PM) in V. sylvestris from Central Asia. Here, we report resistance to PM of V. sylvestris collected from different regions of Croatia and in seedling populations established from in situ V. sylvestris accessions. Ninety-one in situ individuals and 67  V. sylvestris seedlings were evaluated for PM resistance according to OIV 455 descriptor. Three SSR markers (SC47-18, SC8-071-0014, and UDV-124) linked to PM resistance locus Ren1 were used to decipher allelic structure. Nine seedlings showed resistance in in vivo evaluations while leaf disk assays revealed three PM-resistant accessions. One V. vinifera cultivar used as a control for PM evaluations also showed high phenotypic resistance. Based on the presence of one or two resistance alleles that are linked to the Ren1 locus, 32 resistant seedlings and 41 resistant in situ genotypes were identified in the investigated set. Eight seedlings showed consistent phenotypic PM resistance, of which seven carried one or two alleles at the tested markers. This study provides the first evidence of PM resistance present within the eastern Adriatic V. sylvestris germplasm.

Background Introgressive hybridization can reassort genetic variants into beneficial combinations, permitting adaptation to new ecological niches. To evaluate evolutionary patterns and dynamics that contribute to introgression, we investigate six wild Vitis species that are native to the Southwestern United States and useful for breeding grapevine ( V. vinifera ) rootstocks. Results By creating a reference genome assembly from one wild species, V. arizonica , and by resequencing 130 accessions, we focus on identifying putatively introgressed regions (pIRs) between species. We find six species pairs with signals of introgression between them, comprising up to ~ 8% of the extant genome for some pairs. The pIRs tend to be gene poor, located in regions of high recombination and enriched for genes implicated in disease resistance functions. To assess potential pIR function, we explore SNP associations to bioclimatic variables and to bacterial levels after infection with the causative agent of Pierce’s disease ( Xylella fastidiosa ). pIRs are enriched for SNPs associated with both climate and bacterial levels, suggesting that introgression is driven by adaptation to biotic and abiotic stressors. Conclusions Altogether, this study yields insights into the genomic extent of introgression, potential pressures that shape adaptive introgression, and the evolutionary history of economically important wild relatives of a critical crop.

Diversified reproductive systems can be observed in the plant kingdom and applied in crop breeding; however, their impacts on crop genomic variation and breeding remain unclear. Grapevine ( Vitis vinifera L.), a widely planted fruit tree, underwent a shift from dioecism to monoecism during domestication and involves crossing, self-pollination, and clonal propagation for its cultivation. In this study, we discover that the reproductive types, namely, crossing, selfing, and cloning, dramatically impact genomic landscapes and grapevine breeding based on comparative genomic and population genetics of wild grapevine and a complex pedigree of Pinot Noir. The impacts are widely divergent, which show interesting patterns of genomic purging and the Hill-Robertson interference. Selfing reduces genomic heterozygosity, while cloning increases it, resulting in a “double U-shaped” site frequency spectrum (SFS). Crossing and cloning conceal while selfing purges most deleterious and structural burdens. Moreover, the close leakage of large-effect deleterious and structural variations in repulsion phases maintains heterozygous genomic regions in 4.3% of the grapevine genome after successive selfing for nine generations. Our study provides new insights into the genetic basis of clonal propagation and genomic breeding of clonal crops by purging deleterious variants while integrating beneficial variants through various reproductive systems. Effects of reproductive systems on crop genomic variation and breeding remain unclear. Here, the authors report that reproductive types impact genomic landscapes and grapevine breeding based on comparative genomic and population genetic analyses of wild grapevine and a complex pedigree of Pinot Noir.

Background The mountainous region between the Caucasus and China is considered to be the center of domestication for grapevine. Despite the importance of Central Asia in the history of grape growing, information about the extent and distribution of grape genetic variation in this region is limited in comparison to wild and cultivated grapevines from around the Mediterranean basin. The principal goal of this work was to survey the genetic diversity and relationships among wild and cultivated grape germplasm from the Caucasus, Central Asia, and the Mediterranean basin collectively to understand gene flow, possible domestication events and adaptive introgression. Results A total of 1378 wild and cultivated grapevines collected around the Mediterranean basin and from Central Asia were tested with a set of 20 nuclear SSR markers. Genetic data were analyzed (Cluster analysis, Principal Coordinate Analysis and STRUCTURE) to identify groups, and the results were validated by Nei’s genetic distance, pairwise F ST analysis and assignment tests. All of these analyses identified three genetic groups: G1, wild accessions from Croatia, France, Italy and Spain; G2, wild accessions from Armenia, Azerbaijan and Georgia; and G3, cultivars from Spain, France, Italy, Georgia, Iran, Pakistan and Turkmenistan, which included a small group of wild accessions from Georgia and Croatia. Wild accessions from Georgia clustered with cultivated grape from the same area ( proles pontica ), but also with Western Europe ( proles occidentalis ), supporting Georgia as the ancient center of grapevine domestication. In addition, cluster analysis indicated that Western European wild grapes grouped with cultivated grapes from the same area, suggesting that the cultivated proles occidentalis contributed more to the early development of wine grapes than the wild vines from Eastern Europe. Conclusions The analysis of genetic relationships among the tested genotypes provided evidence of genetic relationships between wild and cultivated accessions in the Mediterranean basin and Central Asia. The genetic structure indicated a considerable amount of gene flow, which limited the differentiation between the two subspecies. The results also indicated that grapes with mixed ancestry occur in the regions where wild grapevines were domesticated.

Pierce’s disease (PD) caused by the bacterium Xylella fastidiosa is a deadly disease of grapevines. This study used 20 SSR markers to genotype 326 accessions of grape species collected from the southeastern and southwestern United States, Mexico and Costa Rica. Two hundred sixty-six of these accessions, and an additional 12 PD resistant hybrid cultivars developed from southeastern US grape species, were evaluated for PD resistance. Disease resistance was evaluated by quantifying the level of bacteria in stems and measuring PD symptoms on the canes and leaves. Both Bayesian clustering and principal coordinate analyses identified two groups with an east-west divide: group 1 consisted of grape species from the southeastern US and Mexico, and group 2 consisted of accessions collected from the southwestern US and Mexico. The Sierra Madre Oriental mountain range appeared to be a phylogeographic barrier. The state of Texas was identified as a potential hybridization zone. The hierarchal STRUCTURE analysis on each group showed clustering of unique grape species. An east-west divide was also observed for PD resistance. With the exception of Vitis candicans and V . cinerea accessions collected from Mexico, all other grape species as well as the resistant southeastern hybrid cultivars were susceptible to the disease. Southwestern US grape accessions from drier desert regions showed stronger resistance to the disease. Strong PD resistance was observed within three distinct genetic clusters of V . arizonica which is adapted to drier environments and hybridizes freely with other species across its wide range.

Multiple grape powdery mildew (PM) genetic resistance ( R ) loci have been found in wild grape species. Little is known about the defense responses associated with each R locus. In this study, we compare the defense mechanisms associated with PM resistance in interspecific crosses segregating for a single R locus from Muscadinia rotundifolia ( Run1 , Run1.2b , Run2.1 , Run2.2 ) , Vitis cinerea ( Ren2 ) , V. romanetii ( Ren4D and Ren4U ), and the interspecific hybrid Villard blanc ( Ren3 ). By combining optical microscopy, visual scoring, and biomass estimation, we show that the eight R loci confer resistance by limiting infection at different stages. We assessed the defense mechanisms triggered in response to PM at 1 and 5 days post-inoculation (dpi) via RNA sequencing. To account for the genetic differences between species, we developed for each accession a diploid synthetic reference transcriptome by incorporating into the PN40024 reference homozygous and heterozygous sequence variants and de novo assembled transcripts. Most of the R loci exhibited a higher number of differentially expressed genes (DEGs) associated with PM resistance at 1 dpi compared to 5 dpi, suggesting that PM resistance is mostly associated with an early transcriptional reprogramming. Comparison of the PM resistance-associated DEGs showed a limited overlap between pairs of R loci, and nearly half of the DEGs were specific to a single R locus. The largest overlap of PM resistance-associated DEGs was found between Ren3 + , Ren4D + , and Ren4U + genotypes at 1 dpi, and between Ren4U + and Run1 + accessions at 5 dpi. The Ren3 + , Ren4D + , and Ren4U + were also found to have the highest number of R locus-specific DEGs in response to PM. Both shared and R locus-specific DEGs included genes from different defense-related categories, indicating that the presence of E. necator triggered distinct transcriptional responses in the eight R loci.

Grape Phylloxera, Daktulosphaira vitifoliae, is a gall-forming insect that feeds on the leaves and roots of many Vitis species. The roots of the cultivated V. vinifera cultivars and hybrids are highly susceptible to grape phylloxera feeding damage. The native range of this insect covers most of North America, and it is particularly abundant in the eastern and central United States. Phylloxera was introduced from North America to almost all grape-growing regions across five of the temperate zone continents. It devastated vineyards in each of these regions causing large-scale disruptions to grape growers, wine makers and national economies. In order to understand the population diversity of grape phylloxera in its native range, more than 500 samples from 19 States and 34 samples from the introduced range (northern California, Europe and South America) were genotyped with 32 simple sequence repeat markers. STRUCTURE, a model based clustering method identified five populations within these samples. The five populations were confirmed by a neighbor-joining tree and principal coordinate analysis (PCoA). These populations were distinguished by their Vitis species hosts and their geographic locations. Samples collected from California, Europe and South America traced back to phylloxera sampled in the northeastern United States on V. riparia, with some influence from phylloxera collected along the Atlantic Coast and Central Plains on V. vulpina. Reproductive statistics conclusively confirmed that sexual reproduction is common in the native range and is combined with cyclical parthenogenesis. Native grape phylloxera populations were identified to be under Hardy-Weinberg equilibrium. The identification of admixed samples between many of these populations indicates that shared environments facilitate sexual reproduction between different host associated populations to create new genotypes of phylloxera. This study also found that assortative mating might occur across the sympatric range of the V. vulpina west and V. cinerea populations.

Cultivated grapevines ( Vitis vinifera ) lack resistance to powdery mildew (PM) with few exceptions. Resistance to this pathogen within V. vinifera has been reported in earlier studies and identified as the Ren1 locus in two Central Asian table grape accessions. Other PM-resistant cultivated varieties and accessions of the wild ancestor V. vinifera subsp. sylvestris were soon identified raising questions regarding the origin of the resistance. In this study, F1 breeding populations were developed with a PM susceptible V. vinifera subsp. vinifera breeding line and a PM-resistant subsp. sylvestris accession. Genotyping was carried out with five Ren1 locus linked SSR markers. A PM resistance locus explaining up to 96% of the phenotypic variation was identified in the same genomic position, where the Ren1 locus was previously reported. New SSR marker alleles linked with the resistance locus were identified. We report results of PM resistance in multiple accessions of subsp. sylvestris collected as seed lots or cuttings from five countries in the Caucasus and Central Asia. A total of 20 females from 11 seed lots and 19 males from nine seed lots collected from Georgia, Armenia, and Azerbaijan were resistant to PM. Three male and one female plant collected as cuttings from Afghanistan and Iran were also resistant to PM. Allelic analysis of markers linked with the Ren1 locus in conjunction with disease evaluation data found a high diversity of allelic haplotypes, which are only possible via recombination events occurring over a long time period. Sequence analysis of two alleles of the SSR marker that cosegregates with the resistance found SNPs that were present in the wild progenitor and in cultivated forms. Variable levels of PM resistance among the tested accessions were also observed. These lines of evidence suggest that the powdery mildew fungus may have been present in Asia for a longer time than currently thought, giving the wild progenitor V. vinifera subsp. sylvestris time to coevolve with and develop resistance to this pathogen.

This is the first report evaluating the genetic diversity of Mexican grape species utilizing DNA-based markers to understand the distribution of grape species, and patterns of hybridization. The study utilized accessions maintained in three collections in Mexico, one in the USA and recently collected germplasm. Fifteen SSR markers were used to develop a fingerprint database to identify unique germplasm. Two different clustering analyses without prior population assignment, were used to identify groups that were verified by a Discriminant Analysis of Principal Components and a Principal Coordinate Analysis. Genetic diversity estimates were made across and within groups to validate the results obtained from the clustering analyses. Multiple clustering analyses and diversity parameters supported six genetic groups representing different geographic regions. The Northeastern group was the most diverse with a geographic range extending to Eastern and Central Mexico, while the Coahuila group was the least diverse. Vitis arizonica Engelm. and Vitis cinerea Engelm. ex Millardet were the most abundant species with many hybrid forms. We provide evidence that wild grape species in Mexico follow the physical barriers of mountain ranges like the Sierra Madre Oriental with an east–west divide and the Trans-Mexican Volcanic Belt as a corridor for gene flow among different grape species. Additional collections are required to fully understand the extent of hybridization and to clarify hybrid zones.