Integrating physiology, transcriptomics and phylogenomics reveals the adaptive evolution of biennial fruiting in angiosperms.

Abstract

Most angiosperms complete fruit maturation within a single growing season, but a few lineages require two. However, the physiological and molecular mechanisms underlying this prolonged fruit development (PFD), and whether it represents a shared ancestral trait or a convergent adaptation, remain unresolved. Here we investigate 2-year fruiting species in Fagaceae, Rhamnaceae and Tapisciaceae, using morphological, histochemical, transcriptomic and phylogenomic approaches. The results show that fruits enter dormancy in autumn, resume growth in spring, and accumulate sugars and lipids during overwintering, indicating cold acclimation via starch/sucrose and fatty acid metabolism. Transcriptomic and co‑expression network analyses reveal that phytohormone (ABA, ethylene, auxin) and MAPK signaling are intertwined with sugar metabolism, forming a regulatory hub that controls dormancy. Crucially, by integrating phylogenomic dating across multiple lineages, we demonstrate that PFD did not arise from a common ancestor but evolved convergently, with the divergence of major PFD-bearing clades (Fagaceae, Rhamnaceae, Tapisciaceae) clustering near the Eocene-Oligocene boundary-a period of profound global cooling. Our findings provide a mechanistic and evolutionary framework for understanding PFD as a convergent adaptive strategy, linking molecular regulation of winter dormancy to deep-time climatic change.