Origin and evolution of grapevine genomes

Grapevines (Vitis) belonging to grape family (Vitaceae) are symbolic fruit crops pivotal to human civilization. The evolutionary history of grapevines divergent from other Vitaceae plants remains mysterious, requiring a family-wide whole-genome phylogenomic analysis. Here, weconduct chromosome-level phylogenomics to investigate the origin and evolution of grapevines using 29 genome assemblies of five genera Vitis, Parthenocissus, Ampelopsis, Tetrastigma, and Cissus, 27 of which arenewly releasedin this study. Phylogenomic and macrosynteny analysis unaminously support Ampelopsis as a neighboring lineage to Parthenocissus, a long controversy likely caused by introgression and incomplete lineage sorting. Ancestral genome reconstruction delineatesthe major chromosome rearrangement eventsin Vitaceae karyotype evolution, revealing a novel mechanism,"Fusion-Cyclizing-Fission" (FCF),underlying Cissus karyotypeformation. Pan-3D genome analysis highlights the contributions of structural variants (SVs) to the variation of A/B compartments and topologically associated domains (TAD),revealing a strong purifying selection of SVs at TAD boundaries. We further demonstrate that Helitrontransposons mediate proliferation and regulation of grapevine NLR immune-receptor genes biasedly enriched in specific ancestral chromosomes. Importantly, we discover anNLRgene VbRpv35from wild grapevine V. bellula resistant to downy mildew (DM), whose heterologous expression in V. vinifera confersenhanced DM resistance. Taken together, we provide phylogenomic insight into the origin and evolutionof grapevines and valuable resources for grapevine improvement and understanding angiosperm evolution.