Native mass spectrometry reveals the conformational diversity of the UVR8 photoreceptor

Camacho, Inês S; Theisen, Alina; Johannissen, Linus O.; Díaz-Ramos, L. Aranzazú; Christie, John M.; Jenkins, Gareth I.; Bellina, Bruno; Barran, Perdita E.; Jones, Alex R.

doi:10.1073/pnas.1813254116

Cited by 39 publications

(52 citation statements)

References 41 publications

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“…For both types of photoreceptors, interaction through a linear VP peptide motif and a folded, light‐regulated interaction domain leads to cooperative, high‐affinity binding of the activated photoreceptor to COP1. We propose that in response to UV‐B light, UVR8 dimers monomerize, exposing a new interaction surface that binds to the COP1 WD40 domain and releases the UVR8 C‐terminal VP motif from structural restraints that prevent its interaction with COP1 in the absence of UV‐B (Yin et al , ; Heilmann et al , ; Camacho et al , ; Wu et al , ). Similarly, the VP motif in the CCT domain of cryptochromes may become exposed and available for interaction upon blue‐light activation of the photoreceptor (Müller & Bouly, ; Wang et al , ).…”

Section: Discussionmentioning

confidence: 99%

Plant photoreceptors and their signaling components compete for COP 1 binding via VP peptide motifs

et al. 2019

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Plants sense different parts of the sun's light spectrum using distinct photoreceptors, which signal through the E3 ubiquitin ligase COP1. Here, we analyze why many COP1‐interacting transcription factors and photoreceptors harbor sequence‐divergent Val‐Pro (VP) motifs that bind COP1 with different binding affinities. Crystal structures of the VP motifs of the UV‐B photoreceptor UVR8 and the transcription factor HY5 in complex with COP1, quantitative binding assays, and reverse genetic experiments together suggest that UVR8 and HY5 compete for COP1. Photoactivation of UVR8 leads to high‐affinity cooperative binding of its VP motif and its photosensing core to COP1, preventing COP1 binding to its substrate HY5. UVR8–VP motif chimeras suggest that UV‐B signaling specificity resides in the UVR8 photoreceptor core. Different COP1–VP peptide motif complexes highlight sequence fingerprints required for COP1 targeting. The blue‐light photoreceptors CRY1 and CRY2 also compete with transcription factors for COP1 binding using similar VP motifs. Thus, our work reveals that different photoreceptors and their signaling components compete for COP1 via a conserved mechanism to control different light signaling cascades.

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Section: Discussionmentioning

confidence: 99%

Plant photoreceptors and their signaling components compete for COP 1 binding via VP peptide motifs

et al. 2019

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“…It is proposed that photoreception 'activates' the monomer in some way so that it can interact with relevant proteins to initiate a response (Jenkins, 2014). Such activation could, for instance, involve observed conformational changes to the monomer (Heilmann et al, 2014;Miyamori et al, 2015;Zeng et al, 2015;Camacho et al, 2019). There is evidence that conformational changes to the monomer alter the exposure of the C-terminal region that interacts with other proteins (Camacho et al, 2019).…”

Section: Uvr8 Monomer Photoreception Likely Contributes To Uv-b Percementioning

confidence: 99%

“…Such activation could, for instance, involve observed conformational changes to the monomer (Heilmann et al, 2014;Miyamori et al, 2015;Zeng et al, 2015;Camacho et al, 2019). There is evidence that conformational changes to the monomer alter the exposure of the C-terminal region that interacts with other proteins (Camacho et al, 2019). Current models of UVR8 signalling involve the monomer binding to COP1, which results in stabilisation of HY5 protein (Favory et al, 2009;Rizzini et al, 2011;Huang et al, 2013), which in turn can stimulate downstream responses including its own transcription (Binkert et al, 2014).…”

Section: Uvr8 Monomer Photoreception Likely Contributes To Uv-b Percementioning

confidence: 99%

A dynamic model of UVR8 photoreceptor signalling in UV‐B‐acclimated Arabidopsis

et al. 2020

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The photoreceptor UVR8 mediates numerous photomorphogenic responses of plants to UV-B wavelengths by regulating transcription. Studies with purified UVR8 and seedlings not previously exposed to UV-B have generated a model for UVR8 action in which dimeric UVR8 rapidly monomerises in response to UV-B exposure to initiate signalling. However, the mechanism of UVR8 action in UV-B-acclimated plants growing under photoperiodic conditions, where UVR8 exists in a dimer/monomer photo-equilibrium, is poorly understood. We examined UVR8 dimer/monomer status, gene expression responses, amounts of key UVR8 signalling proteins and their interactions with UVR8 in UV-B-acclimated Arabidopsis. We show that in UV-B-acclimated plants UVR8 can mediate a response to a 15-fold increase in UV-B without any increase in abundance of UVR8 monomer. Following transfer to elevated UV-B, monomers show increased interaction with both COP1, to initiate signalling and RUP2, to maintain the photo-equilibrium when the dimer/monomer cycling rate increases. Native RUP1 is present in low abundance compared with RUP2. We present a model for UVR8 action in UV-B-acclimated plants growing in photoperiodic conditions that incorporates dimer and monomer photoreception, dimer/monomer cycling, abundance of native COP1 and RUP proteins, and interactions of the monomer population with COP1, RUP2 and potentially other proteins.

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“…Even though the crystal structure of UVR8 has been solved, the exact roles of the UVR8 N‐ and C‐terminal ends are not well understood (Jenkins 2014). Structural analysis revealed that the C‐terminus of UVR8 C adopts both a compact and extended state, which are postulated to be important for the regulation of UVR8 activity (Camacho et al 2019). In this study, we provide evidence that the last 17 amino acids of UVR8 repress UV‐B signaling by preventing the binding of UVR8 to COP1, thereby hindering UV‐B perception.…”

Section: Discussionmentioning

confidence: 99%

“…Recent structural analyses suggest that the C‐terminal tail of UVR8, including both the C27 and C17 domains, adopts diverse conformations, for example, compact and extended states that are believed to be important for the regulation of UVR8 activity (Camacho et al 2019). However, experimental evidence is not available.…”

Section: Introductionmentioning

confidence: 99%

The C‐terminal 17 amino acids of the photoreceptor UVR8 is involved in the fine‐tuning of UV‐B signaling

Dong

Yang

et al. 2020

JIPB

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Plant UV‐B responses are mediated by the photoreceptor UV RESISTANCE LOCUS 8 (UVR8). In response to UV‐B irradiation, UVR8 homodimers dissociate into monomers that bind to the E3 ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1). The interaction of the C27 domain in the C‐terminal tail of UVR8 with the WD40 domain of COP1 is critical for UV‐B signaling. However, the function of the last 17 amino acids (C17) of the C‐terminus of UVR8, which are adjacent to C27, is unknown, although they are largely conserved in land plants. In this study, we established that Arabidopsis thaliana UVR8 C17 binds to full‐length UVR8, but not to COP1, and reduces COP1 binding to the remaining portion of UVR8, including C27. We hypothesized that overexpression of C17 in a wild‐type background would have a dominant negative effect on UVR8 activity; however, C17 overexpression caused strong silencing of endogenous UVR8, precluding a detailed analysis. We therefore generated YFP‐UVR8N423 transgenic lines, in which C17 was deleted, to examine C17 function indirectly. YFP‐UVR8N423 was more active than YFP‐UVR8, suggesting that C17 inhibits UV‐B signaling by attenuating binding between C27 and COP1. Our study reveals an inhibitory role for UVR8 C17 in fine‐tuning UVR8–COP1 interactions during UV‐B signaling.

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Native mass spectrometry reveals the conformational diversity of the UVR8 photoreceptor

Cited by 39 publications

References 41 publications

Plant photoreceptors and their signaling components compete for COP 1 binding via VP peptide motifs

Plant photoreceptors and their signaling components compete for COP 1 binding via VP peptide motifs

A dynamic model of UVR8 photoreceptor signalling in UV‐B‐acclimated Arabidopsis

The C‐terminal 17 amino acids of the photoreceptor UVR8 is involved in the fine‐tuning of UV‐B signaling

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