Dynamics and mechanism of dimer dissociation of photoreceptor UVR8

Li, Xiankun; Liu, Zheyun; Ren, Haisheng; Kundu, Mainak; Zhong, Frank; Wang, Lijuan; Gao, Jiali; Zhong, Dongping

doi:10.1038/s41467-021-27756-w

Cited by 13 publications

(14 citation statements)

References 41 publications

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“…In addition, UVR8 regulates flowering time, lateral root development, circadian rhythms, phototropism, resistance to biotic and abiotic stresses, shade avoidance, and thermomorphogenesis (Arongaus et al., 2018; Ballare et al., 2012; Demkura & Ballare, 2012; Fasano et al., 2014; Feher et al., 2011; Hayes et al., 2014; Hayes et al., 2017; Mazza & Ballare, 2015; Vandenbussche et al., 2014; Vanhaelewyn et al., 2019; Yang et al., 2020; Zioutopoulou et al., 2022). UV‐B induces a conformational change of UVR8, which results in the dissociation of homodimers, generating monomers, triggering UV‐B signaling (Christie et al., 2012; Li, Liu, et al., 2022; Rizzini et al., 2011; Wu et al., 2012). UVR8 monomers regulate the transcription of a large set of UV‐B target genes, which is viewed as the basis for UV‐B responses (Jenkins, 2017; Li et al., 2013; Liang et al., 2019; Podolec et al., 2021; Yin & Ulm, 2017).…”

Section: Introductionmentioning

confidence: 99%

Dissecting the functions of COP1 in the UVR8 pathway with a COP1 variant in Arabidopsis

Zhang

Fang

et al. 2022

The Plant Journal

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SUMMARY COP1 is a critical repressor of plant photomorphogenesis in darkness. However, COP1 plays distinct roles in the photoreceptor UVR8 pathway in Arabidopsis thaliana. COP1 interacts with ultraviolet B (UV‐B)‐activated UVR8 monomers and promotes their retention and accumulation in the nucleus. Moreover, COP1 has a function in UV‐B signaling, which involves the binding of its WD40 domain to UVR8 and HY5 via conserved Val‐Pro (VP) motifs of these proteins. UV‐B‐activated UVR8 interacts with COP1 via both the core domain and the VP motif, leading to the displacement of HY5 from COP1 and HY5 stabilization. However, it remains unclear whether the function of COP1 in UV‐B signaling is solely dependent on its VP motif binding capacity and whether UV‐B regulates the subcellular localization of COP1. Based on published structures of the COP1 WD40 domain, we generated a COP1 variant with a single amino acid substitution, COP1C509S, which cannot bind to VP motifs but retains the ability to interact with the UVR8 core domain. UV‐B only marginally increased nuclear YFP‐COP1 levels and significantly promoted YFP‐COP1 accumulation in the cytosol, but did not exert the same effects on YFP‐COP1C509S. Thus, the full UVR8–COP1 interaction is important for COP1 accumulation in the cytosol. Notably, UV‐B signaling including activation of HY5 transcription was obviously inhibited in the Arabidopsis lines expressing YFP‐COP1C509S, which cannot bind VP motifs. We conclude that the full binding of UVR8 to COP1 leads to the predominant accumulation of COP1 in the cytosol and that COP1 has an additional function in UV‐B signaling besides VP binding‐mediated protein destabilization.

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Section: Introductionmentioning

confidence: 99%

Dissecting the functions of COP1 in the UVR8 pathway with a COP1 variant in Arabidopsis

Zhang

Fang

et al. 2022

The Plant Journal

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“…Specifically, the hydrogen bond distance between UVR8 W285A D129 and W233 in RUP2-UVR8 W285A (2.9 Å) is comparable to that in dimeric UVR8 (2.8 Å), whereas those in UVR8 W285A (PDB: 4DNU ) and COP1 WD40 -UVR8 are 5.8 Å and 6.7 Å, respectively ( Supplemental Figures 9 and 10 A). As UVR8 D129 is involved in the COP1 WD40 -UVR8 interaction and reported to function in electron-coupled proton-transfer-mediated UVR8 monomerization ( Li et al., 2014 , 2022 ; Wu et al., 2014 ; Wang et al., 2022 ), we wondered whether this residue is involved in UVR8 redimerization. In gel filtration chromatography, UVR8 D129A was characterized as a dimer in the absence of UV-B exposure, whereas UV-B activated UVR8 D129A appeared to be monomeric.…”

Section: Resultsmentioning

confidence: 99%

“…Several intrinsic tryptophan residues (especially W285 and W233) located at the dimer interface serve as the chromophores for UV-B perception ( Christie et al., 2012 ; Wu et al., 2012 ). It is proposed that UV-B irradiation results in excitation of the W285 and W233 indole rings, thus destabilizing the cation-π interactions and/or neutralizing the key salt bridge interactions via a proton-coupled electron transfer reaction ( Christie et al., 2012 ; Wu et al., 2012 , 2014 ; Li et al., 2014 , 2020 , 2022 ; Voityuk et al., 2014 ; Mathes et al., 2015 ). The destabilization and/or neutralization consequently lead(s) to the dissociation of the UVR8 homodimer into monomers ( Christie et al., 2012 ; Wu et al., 2012 , 2014 ; Li et al., 2014 , 2020 , 2022 ; Voityuk et al., 2014 ; Mathes et al., 2015 ; Podolec et al., 2021a ).…”

Section: Introductionmentioning

confidence: 99%

RUP2 facilitates UVR8 redimerization via two interfaces

Wang¹,

Wang²,

Chang³

et al. 2023

Plant Communications

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“…Ultraviolet‐B radiation not only alters the subcellular localization of UVR8, but also induces the photo‐switching of UVR8 from a homodimer to a monomer (Rizzini et al ., 2011; Christie et al ., 2012; D. Wu et al ., 2012; Li et al ., 2022). UVR8 monomers also can reassociate to form homodimers (Heijde & Ulm, 2013; Heilmann & Jenkins, 2013).…”

Section: Introductionmentioning

confidence: 99%

Mechanisms of UV‐B light‐induced photoreceptor UVR8 nuclear localization dynamics

Fang

Zhang

et al. 2022

New Phytologist

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Summary Light regulates the subcellular localization of plant photoreceptors, a key step in light signaling. Ultraviolet‐B radiation (UV‐B) induces the plant photoreceptor UV RESISTANCE LOCUS 8 (UVR8) nuclear accumulation, where it regulates photomorphogenesis. However, the molecular mechanism for the UV‐B‐regulated UVR8 nuclear localization dynamics is unknown. With fluorescence recovery after photobleaching (FRAP), cell fractionation followed by immunoblotting and co‐immunoprecipitation (Co‐IP) assays we tested the function of UVR8‐interacting proteins including CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1), REPRESSOR OF UV‐B PHOTOMORPHOGENESIS 1 (RUP1) and RUP2 in the regulation of UVR8 nuclear dynamics in Arabidopsis thaliana. We showed that UV‐B‐induced rapid UVR8 nuclear translocation is independent of COP1, which previously was shown to be required for UV‐B‐induced UVR8 nuclear accumulation. Instead, we provide evidence that the UV‐B‐induced UVR8 homodimer‐to‐monomer photo‐switch and the concurrent size reduction of UVR8 enables its monomer nuclear translocation, most likely via free diffusion. Nuclear COP1 interacts with UV‐B‐activated UVR8 monomer, thereby promoting UVR8 nuclear retention. Conversely, RUP1and RUP2, whose expressions are induced by UV‐B, inhibit UVR8 nuclear retention via attenuating the UVR8–COP1 interaction, allowing UVR8 to exit the nucleus. Collectively, our data suggest that UV‐B‐induced monomerization of UVR8 promotes its nuclear translocation via free diffusion. In the nucleus, COP1 binding promotes UVR8 monomer nuclear retention, which is counterbalanced by the major negative regulators RUP1 and RUP2.

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Dynamics and mechanism of dimer dissociation of photoreceptor UVR8

Cited by 13 publications

References 41 publications

Dissecting the functions of COP1 in the UVR8 pathway with a COP1 variant in Arabidopsis

Dissecting the functions of COP1 in the UVR8 pathway with a COP1 variant in Arabidopsis

RUP2 facilitates UVR8 redimerization via two interfaces

Mechanisms of UV‐B light‐induced photoreceptor UVR8 nuclear localization dynamics

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