Beyond Arabidopsis: Differential UV-B Response Mediated by UVR8 in Diverse Species

Abstract

Ultraviolet-B radiation (UV-B, 280-315 nm) is an important environmental signal that regulates growth and development in plants. Two dose-dependent UV-B response pathways were described in plants: a specific one, mediated by UVR8 (the specific UV-B receptor) and an unspecific one, activated by the oxidative damage produced by radiation. The constitutively expressed receptor appears inactive as a dimer, with the two monomers dissociating upon UV-B irradiation. The monomer then interacts with COP1, an ubiquitin ligase, hindering its ability to poly-ubiquitinate transcriptional factor HY5, thus averting its degradation and activating the photomorphogenic response. HY5 induces the synthesis of proteins RUP1 and RUP2, which interact with UVR8, releasing COP1, and inducing the re-dimerization of UVR8. This mechanism has been thoroughly characterized in Arabidopsis, where studies have demonstrated that the UVR8 receptor is key in UV-B response. Although Arabidopsis importance as a model plant many mechanisms described in this specie differ in other plants. In this paper, we review the latest information regarding UV-B response mediated by UVR8 in different species, focusing on the differences reported compared to Arabidopsis. For instance, UVR8 is not only induced by UV-B but also by other agents that are expressed differentially in diverse tissues. Also, in some of the species analyzed, proteins with low homology to RUP1 and RUP2 were detected. We also discuss how UVR8 is involved in other developmental and stress processes unrelated to UV-B. We conclude that the receptor is highly versatile, showing differences among species.

Keywords: Arabidopsis; RUP1; RUP2; UV-B; UVR8; gene expression; photomorphogenic response; terrestrial plants.

Figure 1

UVR8-mediated signal transduction model in Arabidopsis. In white light (left panel), the UV-B photoreceptor UVR8 homodimer and E3 ubiquitin ligase complex are located in the cytosol. The E3 ubiquitin ligase promotes degradation of the HY5 and HYH transcription factors. HY5, acting redundantly with HYH, mediates transcriptional responses. Transcription factors HY5, WRKY36, BIM1 and the functional BES1 are localized in the nucleus. HY5 binds to its own promoter to activate HY5 transcription, and WRKY36 also binds to the HY5 promoter to inhibit its transcription. BIM1 and BES1 act together to induce the expression of brassinosteroid (BR)-responsive genes. When plants are exposed to UV-B (right panel), the UVR8 homodimer is dissociated into active monomers. Monomeric UVR8 binds to COP1–SPA and elicits the COP1–SPA dissociation from the CUL4–DDB1 E3 ubiquitin ligase complex precluding HY5/HYH degradation. UVR8–COP1–SPA travels to the nucleus and facilitates HY5 protein stabilization and enhances the binding of HY5 to its own promoter. UVR8 monomer interacts with WRKY36 to inhibit WRKY36 binding to the HY5 promoter hence removing the inhibition of HY5 expression. In addition, the UVR8 monomer interacts with BIM1 and the functional dephosphorylated BES1 to inhibit their binding to the BR-induced genes involved in cell elongation, thus repressing the expression of BR-induced elongation genes and further repressing the BR-promoted plant growth. HY5 induces the transcription of key genes in the photomorphogenic response and defense mechanism. RUP1 y RUP2 are two of the genes induced by HY5. RUP proteins (RUP1 and RUP2) negatively regulate UVR8 by binding to the C27 region, displacing COP1, and promoting re-dimerization of the photoreceptor (pink arrows). RUP could act both in the nucleus and in the cytosol. Currently, the mechanism that transports RUP between the cytosol and the nucleus is unknown. The figure is based on the models proposed by Jenkins (2017) and Liang et al. (2019). UV-B, ultraviolet-B radiation; UVR8, UV RESISTANCE LOCUS 8; COP1, CONSTITUTIVELY PHOTOMORPHOGENIC 1; HY5, ELONGATED HYPOCOTYL 5; HYH, HY5 HOMOLOG; SPA1, SUPPRESSOR OF PHYA; DDB1, DNA DAMAGE-BINDING PROTEIN 1; CUL4, CULLIN 4; WRKY36, WRKY DNA-BINDING PROTEIN 36; BES1, BRI1-EMS-SUPPRESSOR1; BIM1, BES1-INTERACTING MYC-LIKE 1; BRs, Brassinosteroids; RUP1 and RUP2, REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 and 2; FLS, FLAVONOL SYNTHASE; UVR3, UV REPAIR DEFECTIVE 3; ELIP1, EARLY LIGHT-INDUCIBLE PROTEIN 1; CHS, CHALCONE SYNTHASE.

Figure 2

Phylogram of RUP1 and RUP2 proteins. RUPs proteins sequences of plant species and the percentage identity were obtained from the NCBI database (http://www.ncbi.nlm.nih.gov/) using the BLASTP method. The query sequences used were AtRUP1(OAO92149.1) and AtRUP2 (OAO92900.1). The tree was built using Maximum Likelihood method and JTT matrix-based model (Jones et al., 1992). Initial tree obtained by Neighbor-Join and BioNJ algorithms. Distances estimated using JTT. Evolutionary analyses were conducted in MEGA X (Kumar et al., 2018). The highest log likelihood: −15691.88. To make this tree we used some representative sequence of each species. For more information about sequences see Supplementary Table 1.