Plastome phylogenomics unveils an East Asian origin and climatic niche-driven radiation of the temperate tribe Polygoneae (Polygonaceae).

As a core lineage within Polygonoideae, the tribe Polygoneae holds significant taxonomic and evolutionary importance. These species are primarily distributed across the North Temperate Zone, with a few extending into the tropics. China serves as a distribution hotspot, particularly in its southwestern mountains and the arid regions of Xinjiang, hosting remarkable diversity that reflects the tribe's extensive adaptive radiation in dry habitats. Despite its ecological prominence, the phylogenetic relationships and spatiotemporal diversification patterns of the tribe remain poorly resolved. We employed plastome phylogenomics to reconstruct a robust evolutionary framework for Polygoneae and allied taxa, with comprehensive sampling of 175 accessions representing 163 species across 21 genera of Polygonaceae. Phylogenetic analyses yielded a well-supported topology resolving previously contentious relationships. Molecular dating indicates that Polygoneae experienced an intense burst of diversification in East Asia during the late Oligocene (28-20 Ma), followed by a rapid radiation during the Miocene-Pliocene transition (8-3 Ma). These diversification phases show a temporal correspondence with the intensification of the East Asian monsoon and the uplift of the Tianshan Mountains. Ancestral area reconstruction confirmed an East Asian origin for Polygoneae, with subsequent dispersals across the Northern Hemisphere occurring through three major corridors. Specifically, the Southwest China-Central Asia corridor acted as an environmental filter, favoring the westward expansion of xeric-adapted woody shrubs; the Southwest-Northeast corridor served as a mesic refugium, maintaining stable conditions for herbaceous lineages throughout Quaternary glacial-interglacial cycles; and the Hengduan-Qinling-Yanshan mountain corridor facilitated liana dispersal via its topographically complex terrain. Ecological niche modeling demonstrated that climatic niche shifts, particularly adaptations to aridity and temperature extremes, drove lineage diversification. The trait evolution analyses revealed multiple independent origins of woodiness among arid-adapted genera, demonstrating convergent evolution in response to xeric habitats. By reconstructing a comprehensive phylogeny of Polygoneae using complete plastome sequences, this study reveals its East Asian origin and climate-driven radiation pattern. These findings highlight the pivotal role of Cenozoic geological and climatic changes in shaping temperate Asian plant diversity, offering insights into adaptive radiation mechanisms under environmental heterogeneity.