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, we conduct 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 are newly released in 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 delineates the major chromosome rearrangement events in Vitaceae karyotype evolution, revealing a novel mechanism, "Fusion-Cyclizing-Fission" (FCF), underlying Cissus karyotype formation. 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 Helitron transposons mediate proliferation and regulation of grapevine NLR immune-receptor genes biasedly enriched in specific ancestral chromosomes. Importantly, we discover an NLR gene VbRpv35 from wild grapevine V. bellula resistant to downy mildew (DM), whose heterologous expression in V. vinifera confers enhanced DM resistance. Taken together, we provide phylogenomic insight into the origin and evolution of grapevines and valuable resources for grapevine improvement and understanding angiosperm evolution.