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

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 trajectory 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 modeling, 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 reveal 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 through a BIM1-dependent mechanism in the LCA of land plants and later evolved to function as a dominant integrator within UV-B-BR crosstalk in angiosperms. The expansion of the BES1 regulatory network and its binding specificity largely parallels the elaboration of UV-B transcriptional programs during land plant evolution. Our study thus demonstrates that the functional evolution of the UVR8-BES1/BIM1 module enables the stepwise integration of UV-B and BR signaling in green plants, advancing our understanding of how plants have wired hormonal and environmental signals to adapt to terrestrial habitats.