Conservation and divergence of UVR8 photoreceptor-mediated UV-B signaling in Marchantia polymorpha

Ultraviolet-B radiation (UV-B) poses a major challenge to all forms of plant life. The liverwort Marchantia (Marchantia polymorpha) serves as a key model organism for studying signaling pathways and inferring 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 whereas the core UVR8 photocycle is well conserved, regulatory roles of SPA and HY5 diverged during plant evolution. Unlike the case in Arabidopsis (Arabidopsis thaliana) and in contrast to the strong Mpcop1 mutant phenotype, Mpspa mutants developed only a very weak constitutive photomorphogenesis phenotype, indicating that COP1 function is much more independent of SPA in Marchantia than in Arabidopsis. Moreover, in contrast to Arabidopsis SPAs, Mpspa showed enhanced UV-B acclimation and UV stress tolerance, indicating that MpSPA is a negative regulator of MpUVR8 signaling. Similar to Arabidopsis HY5/HYH, MpHY5 functioned antagonistically to MpCOP1, but its role in UV-B-mediated gene expression changes was more limited. Our findings demonstrate that although core components of UV-B signaling existed in the last common ancestor of extant land plants, regulatory interactions have diversified in different lineages since their divergence more than 400 million years ago.