Functional evolution and rewiring of the UVR8-BES1/BIM1 module underpin the refined UV-B responses during plant terrestrialization

The UVR8-BES1/BIM1-mediated crosstalk between UV-B and brassinosteroid (BR) signaling orchestrates transcriptional reprogramming and thereby coordinates BR-mediated growth and UV-B responses in flowering plants. However, when the UVR8-BES1/BIM1 module originated and how this transcriptional regulatory network evolved in plants remain largely unknown. Here, we traced the evolutionary scenarios of the UVR8-BES1/BIM1 module using a structure-guided approach that integrates homology modeling and structural alignment across major plant lineages. By integrating protein interaction modelling, transcriptome profiling, and genome-wide binding analyses, we elucidated the functional evolution of the UVR8-BES1/BIM1 module driven by structural innovations and genetic co-option. Our results revealed that UVR8 and BIM1 orthologs originated in the last common ancestor (LCA) of chlorophytes and maintained a conserved interaction in green plants, whereas BES1 orthologs emerged in the LCA of streptophyte algae and acquired the capacity to interact with UVR8 in vascular plants. BIM1 served as a core UV-B-responsive transcription factor in the LCA of green plants. By contrast, BES1 initially participated in UV-B signaling via a BIM1-dependent mechanism in the LCA of land plants, and evolved to function as a dominant integrator within UV-B-BR crosstalk in angiosperms. The expansion of BES1 regulatory network and binding specificity largely paralleled the elaboration of UV-B transcriptional programs during land plant evolution. Our study demonstrated that the functional evolution of UVR8-BES1/BIM1 module enabled the stepwise integration of UV-B and BR signaling in green plants, advancing the understanding of how plants wired hormonal and environmental signals to adapt to terrestrial habitats.