Conservation and divergence of UVR8-COP1/SPA-HY5 signaling in UV-B responses of Marchantia polymorpha

Ultraviolet-B radiation (UV-B) poses a major challenge to all forms of plant life. The liverwort Marchantia polymorpha (Marchantia) serves as a key model organism to study signaling pathways and to infer their evolution throughout the green lineage. Marchantia expresses key components of UV-B signaling, including the photoreceptor UV RESISTANCE LOCUS 8 (MpUVR8), the WD40-repeat protein REPRESSOR OF UV-B PHOTOMORPHOGENESIS (MpRUP), the E3 ubiquitin ligase complex CONSTITUTIVELY PHOTOMORPHOGENIC 1 / SUPPRESSOR OF phyA-105 (MpCOP1/MpSPA), and the transcriptional regulator ELONGATED HYPOCOTYL 5 (MpHY5). Here, we show that MpUVR8 exists as a homodimer in its ground-state in vivo, then monomerizes and accumulates in the nucleus upon UV-B activation. Activated MpUVR8 interacts with MpCOP1, triggering growth inhibition, gene expression changes, biosynthesis of UV-absorbing metabolites, and photoprotection, which overall contributes to UV-B stress tolerance. MpRUP facilitates redimerization of MpUVR8 and Mp rup null mutants show enhanced UV-B photomorphogenesis, indicating that MpRUP efficiently represses MpUVR8 signaling. Unlike the case in Arabidopsis and in contrast to the strong Mp cop1 mutant phenotype, Mp spa mutants develop only a weak constitutive photomorphogenesis phenotype, indicating that COP1 function is more independent of SPA in Marchantia than in Arabidopsis. Interestingly, however, Mp spa is linked with a hyper-responsive UV-B phenotype, suggesting that MpSPA is a negative regulator of MpUVR8 signaling. Our findings demonstrate that core components of UV-B signaling existed in the last common ancestor of extant land plants; however, regulatory interactions have diversified in different lineages since their divergence more than 400 million years ago.