Super pangenome of Vitis empowers identification of downy mildew resistance genes for grapevine improvement

Abstract

Grapevine (Vitis) is one of the oldest domesticated fruit crops with great cultural and economic importance. Here we assembled and annotated haplotype-resolved genomes of 72 global Vitis accessions including 25 wild and 47 cultivated grapevines, among which genomes for 60 grapevines are newly released. Haplotype-aware phylogenomics disentangled the mysterious hybridization history of grapevines, revealing the enormous genetic diversity of the Vitis genus. Pangenomic analysis reveals that European cultivars, more susceptible to the destructive disease downy mildew (DM), have a smaller repertoire of resistance genes in the NLR family encoding the TIR-NBARC-LRR domain. Through extensive structural variation (SV) characterization, phenotyping, DM-infection transcriptome profiling of 113 Vitis accessions, and SV–expression quantitative trait loci analysis, we have identified over 63 SVs and their relevant genes significantly associated with DM resistance, exemplified by a lysine histidine transporter, VvLHT8. This haplotype-resolved super pangenome of the Vitis genus will accelerate breeding and enrich our understanding of the evolution and biology of grapevines. Super pangenome of the Vitis genus assembled from haplotype-resolved genomes of 72 global Vitis accessions characterizes the landscape of structural variants (SVs) and identifies SV–expression quantitative trait loci for downy mildew resistance.