RESEARCH
UV-B Perception and Signalling by the UVR8 Photoreceptor
The light environment is a key factor that governs a multitude of developmental processes during the entire life cycle of plants. An important part of the incident sunlight encompasses a segment of the UV-B region (280-315 nm) that is not entirely absorbed by the ozone layer in the stratosphere of the earth. This portion of the solar radiation, which inevitably reaches the sessile plants, can act both as an environmental stress factor and as an informational signal. In the latter case, dimers of the UV RESISTANCE LOCUS 8 (UVR8) protein perceive UV-B, by a tryptophan-based mechanism. UVR8-mediated signalling involves the early and UV-B-dependent interaction with the E3 ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1). UVR8 and COP1 are both required for transcriptional activation of the ELONGATED HYPOCOTYL 5 (HY5) gene under UV-B, which encodes a bZIP transcription factor that regulates target genes involved in photoregulatory UV-B responses, including those required for UV-B acclimation. In addition to these positive players, we have identified two WD40-repeat proteins, REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 (RUP1) and RUP2, that function as negative feedback regulators of UVR8 action. RUP1 and RUP2 mediate the reversion of UVR8 to the homodimeric ground state by redimerization, regenerating reactivatable UVR8 homodimers.
UV-B perception by the UVR8 photoreceptor:
UVR8 homodimerizes in the absence of UV-B. UV-B absorption by tryptophan residues results in an immediate monomerisation into active UVR8 monomers. Model from Heijde and Ulm, 2012.
The UVR8 photocycle:
The UVR8 homodimer absorbs UV-B via a tryptophan chromophore, which results in instantaneous UVR8 monomerisation. The UVR8 monomer interacts directly with COP1 to initiate UV-B signaling. UVR8 monomer is redimerized through the action of RUP1 and RUP2, which disrupts the UVR8-COP1 interaction, inactivates the signaling pathway and regenerates the UVR8 homodimer again ready for UV-B perception. Model from Tilbrook et al., 2013.
Selected key publications:
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Heijde, M. and Ulm, R. (2013) Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state. Proc. Natl. Acad. Sci. USA 110: 1113-1118.
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Rizzini et al. (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332: 103-106.
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Favory et al. (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J. 28: 591-601.
Further reading (recent reviews):
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Podolec et al. (2021). Perception and signaling of ultraviolet-B radiation in plants. Annu. Rev. Plant Biol. 72: 793-822.
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Demarsy et al. (2018) Coping with ‘dark sides of the sun’ through photoreceptor signaling. Trends Plant Sci. 23: 260-271.
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Podolec, R. and Ulm, R. (2018) Photoreceptor-mediated regulation of the COP1-SPA E3 ubiquitin ligase complex. Curr. Opin. Plant Biol. 45: 18-25.
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Yin, R. and Ulm, R. (2017) How plants cope with UV-B: from perception to response. Curr. Opin. Plant Biol. 37: 42-48.
SELECTED PROJECTS
UVR8-Mediated Regulation of the COP1 E3 Ubiquitin Ligase
In response to UV-B, the surface of the UVR8 monomer freed by UV-B-dependent monomerization binds to the structurally closely related β-propeller surface of the COP1 WD40-repeat domain, and the UVR8 C-terminus (C27 domain) is released from structural restraints that prevent its interaction with COP1 in the absence of UV-B. This indicates that the UV-B-dependent UVR8 β-propeller interaction contributes to address COP1, thereby efficiently directing the C-terminal C27 domain to the target protein for signal propagation.
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Lau et al. (2019) Plant photoreceptors and their signaling components compete for COP1 binding via VP peptide motifs. EMBO J. 38: e102140.
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Yin et al. (2015) Two distinct domains of the UVR8 photoreceptor interact with COP1 to initiate UV-B signaling in Arabidopsis. Plant Cell 27: 202-213.
Regulation of the UVR8 Activity State
We have identified the importance of redimerization for ground state reversion of the UV-B photoreceptor UVR8 and that RUP1 and RUP2 strongly facilitate this process, providing a negative feedback loop. Moreover, we recently identified a previously unknown activity of COP1 in mediating nuclear accumulation of the UVR8 photoreceptor in response to UV-B.
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Podolec et al. (2021). A constitutively monomeric UVR8 photoreceptor confers enhanced UV-B photomorphogenesis. Proc. Natl. Acad. Sci. USA 118: e2017284118.
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Yin et al. (2016) COP1 is required for UV-B–induced nuclear accumulation of the UVR8 photoreceptor. Proc. Natl. Acad. Sci. USA 113: E4415-E4422.
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Heijde, M. and Ulm, R. (2013) Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state. Proc. Natl. Acad. Sci. USA 110: 1113-1118.
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Gruber et al. (2010) Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc. Natl. Acad. Sci. USA 107: 20132-20137.
UVR8-Mediated Photoprotection of Photosynthesis
UVR8 photoreceptor signalling regulates photoprotection of the photosynthetic machinery by non-photochemical quenching (NPQ) in the single-cell alga Chlamydomonas reinhardtii. Interestingly, the molecular features of UV-B photoreceptor-mediated photoprotection were found to be surprisingly different from those arising under high light
Dannay et al. (2024) Photoreceptor-induced LHL4 protects photosystem II in Chlamydomonas reinhardtii. bioRxiv doi.org/10.1101/2024.02.23.581703.
Allorent et al. (2016) UV-B photoreceptor-mediated protection of the photosynthetic machinery in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 113: 14864-14869.
Photoperiodic Flowering under UV-B
We identified a crucial role for the Arabidopsis RUP2 protein as potent repressor of flowering under non-inductive short days. In the presence of UV-B and dependent on UVR8, mutation of RUP2 renders the facultative long-day plant Arabidopsis thaliana into a day-neutral plant.
Chen et al. (2024) Functional divergence of Arabidopsis REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 and 2 in repression of flowering. Plant Physiol. 194: 1563-1576.
Arongaus et al. (2018) Arabidopsis RUP2 represses UVR8-mediated flowering in noninductive photoperiods. Genes & Dev. 32: 1332-1343.
Sunfleck Perception
In collaboration with Jorge Casal and his team we provided evidence suggesting that UVR8 is able to perceive the occurrence of gaps in the canopy through which sunflecks penetrate, reducing potential UV-B damage.
Belmonte et al. (2024) Sensory perception of fluctuating light in Arabidopsis. bioRxiv doi.org/10.1101/2024.02.21.581400.
Moriconi et al. (2018) Perception of sunflecks by the UV-B photoreceptor UV RESISTANCE LOCUS 8. Plant Physiol. 177: 75-81.
MAP KINASE PHOSPHATASE 1 and UV-B Stress Signalling
Arabidopsis MKP1 plays an important role in UV-B stress signalling, independently of UVR8 signalling. MKP1 is rapidly phosphorylated and stabilised in response to UV-B stress.
González Besteiro, M.A. and Ulm, R. (2013) ATR and MKP1 play distinct roles in response to UV-B stress in Arabidopsis. Plant J. 73: 1034-1043.
González Besteiro, M.A. and Ulm, R. (2013) Phosphorylation and stabilization of Arabidopsis MAP Kinase Phosphatase 1 in response to UV-B stress. J. Biol. Chem. 288: 480-486.
González Besteiro et al. (2011) Arabidopsis MAP kinase phosphatase 1 and its target MAP kinases 3 and 6 antagonistically determine UV-B stress tolerance, independent of the UVR8 photoreceptor pathway. Plant J. 68: 727-737.