Origin and adaptive evolution of UV RESISTANCE LOCUS 8-mediated signaling during plant terrestrialization

Abstract

UV RESISTANCE LOCUS 8 (UVR8) mediates photomorphogenic responses and acclimation to UV-B radiation by regulating the transcription of a series of transcription factors (TFs). However, the origin and evolution of UVR8-mediated signaling pathways remain largely unknown. In this study, we investigated the origin and evolution of the major components of the UVR8-mediated signaling pathway (UVR8, REPRESSOR OF UV-B PHOTOMORPHOGENESIS [RUP], BRI1-EMS-SUPPRESSOR1 [BES1], BES1-INTERACTING MYC-LIKE 1 (BIM1), WRKY DNA-BINDING PROTEIN 36 (WRKY36), MYB DOMAIN PROTEIN 73/77/13 [MYB73/MYB77/MYB13], and PHYTOCHROME INTERACTING FACTOR 4/5 [PIF4 and PIF5]) using comparative genomics and phylogenetic approaches. We showed that the central regulator UVR8 presented a conservative evolutionary route during plant evolution, and the evolutionary history of downstream negative regulators and TFs was different from that of green plant phylogeny. The canonical UVR8-CONSTITUTIVELY PHOTOMORPHOGENIC 1(COP1)/SUPPRESSOR OF PHYA-105 (SPA)-ELONGATED HYPOCOTYL 5 (HY5)-RUP signaling pathway originated in chlorophytes and conferred green algae the additional ability to cope with UV-B radiation. Moreover, the emergence of multiple UVR8-mediated signaling pathways in charophytes laid the foundations for the cross-talk between UV-B signals and endogenous hormone responses. Importantly, we observed signatures that reflect plant adaptations to high UV-B irradiance in subaerial/terrestrial environments, including positive selection in UVR8 and RUPs and increased copy number of some vital TFs. These results revealed that green plants not only experienced adaptive modifications in the canonical UVR8-COP1/SPA-HY5-RUP signaling pathway, but also diversified their UV-B signal transduction mechanisms through increasing cross-talk with other pathways, such as those associated with brassinosteroids and auxin. This study greatly expands our understanding of molecular evolution and adaptive mechanisms underlying plant UV-B acclimation.

Figure 1

Schematic summary of UVR8-mediated signaling pathways related to UV-B responses and photomorphogenesis. A, Without UV-B irradiation, UVR8 forms a homodimer in cytoplasm. B, UV-B radiation triggers the dissociation of UVR8 homodimer, and the UVR8 monomers are capable to interact with COP1, which can, in turn, regulate the expression of HY5. UVR8 regulates numerous potential transcriptional factors (WRKY36, BES1, BIM1, MYB73, MYB77, PIF4, and PIF5) to mediate the UV-B responses and photomorphogenesis. The negative feedback regulators RUP1 and RUP2 facilitate redimerization of UVR8 to complete the UV-B photocycle.

Figure 2

Phylogenetic tree of plant UVR8 orthologs. The maximum-likelihood tree of UVR8 homologs was constructed using IQTREE with the best-fitting model (JTT + G4). The ML tree of UVR8 homologs (left) and the monophyletic group of plant UVR8 orthologs (right) were shown. Nodes under positive selection (aBSREL of Hyphy) were labeled by red asterisks.

Figure 3

The phylogenetic relationship and structural comparisons of RUP in green plants. A, The comparison of COP1 and RUPs domains among A. thaliana, G. biloba, M. polymorpha, C. braunii, and C. reinhardtii. B, The phylogenetic tree and corresponding conserved motifs in green plants.

Figure 4

Spatial distribution of PSSs on the predicted 3D structure of UVR8 proteins. A, Arabidopsis thaliana; B, M. polymorpha; C, M. viride; and D, C. reinhardtii. PSSs (Cys132, Trp144, Met176, and Thr236) were labeled in A. thaliana and the corresponding positions in C. reinhardtii, M. viride, and M. polymorpha UVR8 proteins. Trp285 and Trp233 were the main UV-B sensor, and Cys132, Trp144, Met176, and Thr236 were PSSs corresponding to the positions in homologous proteins of A. thaliana.

Figure 5

The phylogenetic relationship and structural comparisons of downstream TFs in representative green plants. A, BES1 orthologs; B, BIM1 orthologs; C, WRKY36 orthologs; and D, MYB73/77 orthologs. Conserved motifs were shown against the phylogenetic tree. Bootstrap values >50 were indicated. The 10 distinct MEME-motifs were displayed in different colored boxes.

Figure 6

Origin and evolution of the UVR8-mediated signaling pathway. A, Co-expression analyses based on the 1KP transcriptomes. Venn diagrams of the distribution of UVR8, WRKY36, BES1, BIM1, and MYB73/73 orthologs in 48 charophytes, 69 bryophytes, and 96 ferns transcriptomes. B, Y2H assays showing the interactions between the C-terminal domain of UVR8 and WRKY36 and MYB73/MYB77. C, BiFC assays showing the interactions between BIM1 and UVR8. D, Origin and evolution of UVR8 signaling pathway in Archaeplastida. During the transition from deep sea to shallow water, and from aquatic to terrestrial environments, UV light was a crucial environmental signal for green plants. Red algae live in the deep sea where UV-B was entirely filtered. The evolution of UVR8 signaling pathway (UVR8, COP1, SPA, HY5, and RUP) in chlorophytes facilitated green algae to adapt shallow water environment. The origination of the transcriptional regulatory network (PIFs, WRKY36, BES1, BIM1, MYB73, and MYB73) in charophytes conferred freshwater algae the abilities to colonize the water surface. After plants conquered the land, UVR8 signaling pathway contributed to adapt to high and variable doses of UV-B irradiance.