Chromosome-level phylogenomics and genome evolution of the grape family.

Grapevines (Vitis) are pivotal fruit crops for human nutrition and civilization. The evolutionary history of grapevines in the grape family (Vitaceae) remains mysterious, requiring family-wide and whole-genome phylogenomic insights. Here we conduct evolutionary genomic analyses of Vitaceae by generating chromosome-level genome assemblies, placing Ampelopsis closer to Parthenocissus and Vitis. Karyotype evolution analysis delineates major chromosome rearrangements, highlighting overall conservation within Vitis but extensive reorganization for Tetrastigma and Cissus. Pan-3D genome analysis reveals that structural variants contribute to A/B compartment and topologically associated domain variation, exhibiting structural variant clearance at topologically associated domain boundaries. We show that Helitron transposons drive expansion and regulate expression of nucleotide-binding leucine-rich repeat disease resistance genes in Vitis, and discover a nucleotide-binding leucine-rich repeat gene VbRpv35 from wild grape Vitis bellula, whose heterologous expression enhances downy mildew resistance in Vitis vinifera. Together, we provide phylogenomic insight into grapevine genome evolution and valuable resources for improving grapevines and understanding angiosperm evolution.