Genomic and ecological drivers of parallel arid adaptation in tree grapes (Vitaceae)

Abstract

Understanding plant adaptation is critical under intensifying global aridification. Succulence, a key drought-resistance innovation, has evolved repeatedly across plant lineages, yet its intrinsic genomic drivers remain underexplored. Integrating comprehensive evidence from genomics, ecology, and morphology, we investigate adaptation to aridity in the tree grape genus, Cyphostemma (Vitaceae), whose species span environmental gradients from rainforests to deserts and exhibit wide genomic and phenotypic variation. Utilising genome assemblies of representative Cyphostemma species, we demonstrate that specific long terminal repeat retrotransposon (LTR-RT) lineages thrived through the radiation of Cyphostemma and led to substantial intron expansion, a phenomenon rarely studied in eudicots. The intronic LTR-RT insertions likely enhanced tolerance of genome structural changes, facilitating succulence evolution. Genomes of succulents were further expanded by intergenic LTR-RTs, which exhibit recurrent evolutionary advantages in arid and seasonal habitats. Our study reveals how genomic landscapes are shaped by both intrinsic LTR-RT dynamics and extrinsic environmental forces. Critically, we suggest that stochastic dynamics of LTR-RT communities enhance genomic evolvability, enabling adaptive evolution in plants.