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. 2012 Dec 31;110(3):1113–1118. doi: 10.1073/pnas.1214237110

Reversion of the Arabidopsis UV-B photoreceptor UVR8 to the homodimeric ground state

Marc Heijde 1, Roman Ulm 1,1
PMCID: PMC3549095  PMID: 23277547

Abstract

Plants require the UV-B photoreceptor UV RESISTANCE LOCUS 8 (UVR8) for acclimation and survival in sunlight. Upon UV-B perception, UVR8 switches instantaneously from a homodimeric to monomeric configuration, which leads to interaction with the key signaling protein CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) and induction of UV-B–protective responses. Here, we show that UVR8 monomerization is reversible in vivo, restoring the homodimeric ground state. We also demonstrate that the UVR8-interacting proteins REPRESSOR OF UV-B PHOTOMORPHOGENESIS (RUP)1 and RUP2 mediate UVR8 redimerization independently of COP1. UVR8 redimerization consequently disrupts the UVR8–COP1 interaction, which halts signaling. Our results identify a key role of RUP1- and RUP2-mediated UVR8 redimerization in photoreceptor inactivation, a crucial process that regenerates reactivatable UVR8 homodimers.

Keywords: light signaling, photobiology, signal transduction

UV-B radiation (UV-B; 280–315 nm) is an integral part of sunlight with a strong impact on terrestrial ecosystems (1–3). In plants, UV-B perception is necessary for UV-B acclimation and UV-B stress tolerance (4–6). Specific UV-B perception is facilitated by the photoreceptor UV RESISTANCE LOCUS 8 (UVR8) identified only recently in Arabidopsis (7). In agreement with its photoreceptor function, uvr8 null mutants show a strongly reduced response to UV-B (8–11), which even is absent under conditions specifically activating UV-B photoreceptor responses (4). In contrast, UV-B stress responses are not affected per se in uvr8 mutants (12).

Upon UV-B irradiation, UVR8 homodimers monomerize instantaneously to active monomers (7). The UVR8 monomer then interacts with the WD40-repeat domain of the E3 ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) (4), a central regulator of light-dependent plant photomorphogenesis and also of utmost importance in UV-B signaling (13, 14). COP1–UVR8 interaction is an early event in the UV-B perception and signaling pathway and essential for UV-B–dependent photomorphogenesis and acclimation (4). One of the main molecular outcomes of this interaction is an increase in protein level of the bZIP transcription factor ELONGATED HYPOCOTYL 5 (HY5), which may be the result of reduced HY5 ubiquitination by COP1 (4). HY5 together with its homolog HYH induce expression of the majority but not all genes included in the UVR8-dependent UV-B response (15–18). In a negative feedback loop, the light-regulated SALT TOLERANCE/B-BOX DOMAIN PROTEIN 24 (STO/BBX24) was shown to fine-tune the UV-B response by impinging on HY5 (19).

UVR8 is a seven-bladed β-propeller protein that makes use of tryptophan residues intrinsic to the protein as chromophores for UV-B absorption, with a primary role established for tryptophan-285 (7, 20, 21). In agreement with the major role that Trp-285 plays in UV-B–mediated monomerization of UVR8 (7), it was proposed that UV-B absorption by specific tryptophans, namely Trp-285 and Trp-233, leads to disruption of cross-dimer salt bridges involving crucial arginins (20, 21). Despite recent progress in describing UVR8 monomerization and activation of UV-B signaling, mechanisms behind in vivo UVR8 inactivation remain poorly understood.

We recently described the WD40-repeat proteins REPRESSOR OF UV-B PHOTOMORPHOGENESIS (RUP)1 and RUP2 as negative feedback regulators of the UV-B–signaling cascade (22). Upon UV-B exposure, the RUP1 and RUP2 genes are transcriptionally activated in a UVR8-dependent manner. RUP1- and RUP2-YFP fusion proteins localize to both the nucleus and the cytoplasm (22), mimicking the subcellular localization of UVR8 (23). RUP1 and RUP2 are known to repress the UV-B–signaling pathway, but the mechanism by which they do so is presently unknown (22). However, direct interaction of RUP1 and RUP2 with UVR8 suggests that their repressive mechanism is at the photoreceptor level (22).

In the present study, we demonstrate that the UVR8 photoreceptor is capable of in vivo redimerization, restoring the homodimeric ground state, and that this process requires RUP1 and RUP2, but is not affected by the presence or absence of COP1. We further provide evidence that RUP1- and RUP2-mediated UVR8 redimerization results in the disruption of UVR8–COP1 interaction. The UVR8 “off switch” mechanism thus uses specific regulatory proteins to mediate reversion of UVR8 from the signaling to the ground state by redimerization, a process that is of major importance for optimal plant growth and development in sunlight.

Results and Discussion

UV-B–Dependent UVR8 Monomerization Is Reversible in Vivo.

To understand UVR8 protein dynamics following UV-B perception, we investigated reversion of the UVR8 monomer back to its dimer conformation. Inactive UVR8 homodimers can be detected on protein gel blots of non–heat-denatured protein samples (7). Following UV-B–dependent monomerization, UVR8 redimerization was apparent already 30 min post UV-B exposure, and complete redimerization was observed within approximately 2 h (Fig. 1A). Protein gel blots created in parallel using heat-denatured aliquots of the same protein samples showed comparable levels of UVR8, demonstrating that UVR8 levels remain stable during the recovery phase (Fig. 1A). This in vivo UVR8 redimerization is much faster than recent reports of more than 24 h required for the completion of redimerization in vitro (20, 21). To rule out the possibility that reappearance of the UVR8 homodimer is dependent on de novo synthesis of UVR8, we analyzed UVR8 protein dynamics in the presence of cycloheximide (CHX). Under conditions where CHX efficiently blocked protein translation (Fig. S1), clear UVR8 redimerization was observed at a rate comparable to the mock treatment (Fig. 1A, Right). To investigate the monomerization or “reactivation” potential of redimerized UVR8, we subjected plants to up to three successive UVR8-monomerizing UV-B treatments with a redimerization recovery period of 4 h between each treatment. UVR8 dimers repeatedly monomerized in response to UV-B and redimerized in its absence, regardless of preceding cycles of monomerization/redimerization and also in the presence of CHX (Fig. 1B). We thus conclude that UVR8 redimerization is a property of the protein that is independent of UVR8 de novo synthesis, allowing the regeneration of photoactive homodimers. In addition, UVR8 protein dynamics are fully reversible in vivo with monomerization and dimerization depending on the presence and absence of UV-B, respectively.

Fig. 1.

Fig. 1.

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UV-B–activated UVR8 monomers redimerize in white light without UV-B, and regenerated UVR8 dimers are competent for UV-B perception and monomerization. (A) Seven-day-old seedlings were irradiated by broadband UV-B for 15 min (+UV) to allow UVR8 monomerization before they were subjected to a recovery period in white light (WL) for the indicated times. An asterisk (*) indicates a nonspecific cross-reacting band. (B) Seven-day-old seedlings were repeatedly treated for 15 min with broadband UV-B (+UV) and allowed to recover for 4 h in white light (4 h) (i.e., from left to right: −UV/+UV/+UV+4h/+UV+4h+UV/+UV+4h+UV+4h/+UV+4h+UV+4h+UV). (A and B) Mock-treated plants were in liquid MS medium with DMSO, and cycloheximide (CHX)-treated plants (+CHX) were in liquid MS medium supplied with 0.5 mM CHX in DMSO. UVR8 dimers were detectable in non–heat-denatured protein samples, as described before (7). Parallel denatured samples demonstrated equal amounts of UVR8 protein.

RUP1 and RUP2 Regulate the UVR8 Dimer-to-Monomer Ratio.

RUP1 and RUP2 are negative feedback regulators of UVR8, which function upstream or adjacent to the UVR8–COP1 interaction (22). The RUP1 and RUP2 mechanism of action may be by preventing UVR8 monomerization and/or facilitating UVR8 redimerization post UV-B exposure. Consistent with both possibilities and in contrast to the UV-B–specific UVR8–COP1 interaction, RUP1 and RUP2 can interact with UVR8 under conditions with and without UV-B and thus with both UVR8 monomers and homodimers (22, 24). To begin with, we tested whether RUP1 and RUP2 influence the UVR8 dimer–monomer ratio upon UV-B exposure, which would imply that RUP1 and RUP2 act upstream of the UVR8–COP1 interaction. Under low-level UV-B where UVR8 monomerization is almost undetectable in wild type, clear UVR8 monomerization was apparent in the rup1 rup2 double mutant (Fig. 2A). This is in agreement with the UV-B hyper-responsiveness and enhanced acclimation to UV-B in rup1 rup2 (22). Conversely, under UV-B irradiation that efficiently monomerizes UVR8 in wild type, UVR8 monomerization in a RUP2-overexpression line was undetectable (Fig. 2B). Again, this result is in agreement with the UV-B hypo-responsiveness and reduced acclimation to UV-B that accompanies RUP2 overexpression (22). Moreover, it is of note that the cop1-4 mutant—which expresses the truncated COP1N282 protein that lacks the WD40-repeat domain and thus cannot interact with UVR8 (4, 7)—did not show any difference in comparison with the wild type (Fig. 2 A and B). This suggests that COP1, and therefore also the UVR8–COP1 interaction, has no major role in the regulation of UVR8 activity. Total levels of UVR8 in the rup1 rup2 double mutant and the RUP2-overexpression line were comparable to wild type, suggesting that the effect on UVR8 monomerization was not due to variations in UVR8 levels (Fig. 2 A and B; heat-denatured samples).

Fig. 2.

Fig. 2.

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Redimerization of UVR8 is mediated by RUP1 and RUP2. (A) Seven-day-old seedlings were irradiated for 6 h with supplementary narrowband UV-B (+) or without (−). Wild type (Col) was compared with rup1 rup2, rup2-1/Pro35S:RUP2 (RUP2 Ox#3), cop1-4, and uvr8-6. (B) Seven-day-old seedlings were irradiated for 6 h with supplementary narrowband UV-B and 15-min broadband UV-B (+) or without (−). (C and D) Seven-day-old rup1 rup2 (C) or rup2-1/Pro35S:RUP2 (RUP2 Ox#3) (D) seedlings were irradiated for 15 min with broadband UV-B before recovery in white light (WL) for the indicated times. An asterisk (*) indicates a nonspecific cross-reacting band. (A–D) UVR8 dimers were detectable in non–heat-denatured protein samples, as described before (7). Parallel denatured samples demonstrated equal amounts of UVR8 protein.

As mentioned above, RUP1 and RUP2 may negatively regulate UV-B signaling by mediating UVR8 redimerization post UV-B exposure. This is supported by the fact that RUP1 and RUP2 levels are induced by UV-B exposure to then provide negative feedback regulation of the UVR8 pathway involving direct RUP1/RUP2–UVR8 interaction (22). Thus, we further investigated whether the level of RUP1 and RUP2 influences UVR8 redimerization post UV-B exposure. First, we analyzed UVR8 protein dynamics in the absence of RUP1 and RUP2. Although wild-type seedlings showed complete UVR8 dimer recovery within 2 h post UV-B exposure (Fig. 1A), we observed that rup1 rup2 double mutants were strongly impaired in UVR8 dimer recovery during the entire 6-h duration of the experiment (Fig. 2C). Even 36 h post UV-B exposure UVR8 redimerization was not yet completed in rup1 rup2, even though redimerization during that time became apparent in the absence of RUP1 and RUP2 (Fig. S2). Together, this clearly shows that, without RUP1 and RUP2, the ability of monomerized UVR8 to revert to the inactive homodimeric state is compromised. Relatively normal UVR8 redimerization was seen in rup1 and rup2 single mutants (Fig. S3), reemphasizing the functional redundancy of RUP1 and RUP2 in regulating UVR8 (22). We further tested whether RUP1 and RUP2 may also partially inhibit UVR8 monomer formation. However, UVR8 monomerization within minutes of UV-B was similar in wild-type and rup1 rup2 double mutants (Fig. S4). Although we cannot formally exclude that the presence of RUP1 and RUP2 also prevents UV-B–dependent UVR8 monomerization to a minor extent, it is clear that RUP1 and RUP2 play a major role in facilitating UVR8 redimerization. Second, we analyzed UVR8 protein dynamics with an increased level of RUP2. In contrast to the clear transition of UVR8 to monomer in wild-type and rup1 rup2 double mutants upon UV-B exposure, no change in the UVR8 homodimer/monomer ratio was observed in a RUP2-overexpression line (Fig. 2 B and D). This suggests that high RUP2 levels lead to instantaneous recovery of UVR8 homodimer.

UVR8 protein dynamics in rup1 rup2 and RUP2-overexpression lines is in agreement with the physiological role of RUP1 and RUP2 as negative feedback regulators through direct interaction with UVR8 (22). Therefore, although UV-B–dependent UVR8 monomerization is an intrinsic property of the protein itself (7, 20, 21), we conclude that the efficient reversion of UVR8 monomer to the inactive homodimeric ground state in vivo is strongly dependent on RUP1 and RUP2. Thus, we propose that UVR8 redimerization is the major mechanism of action of RUP1 and RUP2 as negative feedback regulators of UV-B signaling.

RUP1 and RUP2 Negatively Regulate UVR8–COP1 Interaction.

Following UV-B perception by UVR8, a primary molecular event key to the UV-B–signaling pathway is direct interaction of the UVR8 monomer with COP1 (4, 7). It was thus of interest to see whether the UVR8–COP1 interaction was affected by RUP1 and RUP2. We have generated anti-COP1 and anti-UVR8 antibodies that allow UV-B–dependent coimmunoprecipitation (co-IP) of endogenous COP1 with UVR8 from wild-type seedlings (Fig. 3). Interestingly, under a level of UV-B that is insufficient to produce a detectable UVR8–COP1 interaction in wild type, COP1 could be co-IP’ed with UVR8 in rup1 rup2 double mutants (Fig. 3A). Also, under a level of UV-B that yields clear co-IP of COP1 with UVR8 in wild type, elevated levels of COP1 could be co-IP’ed with UVR8 in rup1 rup2 double mutants (Fig. 3B). In contrast, no COP1 co-IP could be detected in a RUP2-overexpression line (Fig. 3B). Our data demonstrate that the UVR8–COP1 interaction is strongly influenced by RUP1 and RUP2. Thus, negative regulation of the UVR8–signaling pathway by RUP1 and RUP2 is associated with the disruption of UVR8–COP1 interaction.

Fig. 3.

Fig. 3.

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UVR8 interaction with COP1 is negatively regulated by RUP1 and RUP2. (A and B) Coimmunoprecipitation of COP1 using UVR8 antibodies in extracts from 7-d-old wild-type (Col), rup1 rup2, RUP2 Ox#3, uvr8-6, and cop1-4 seedlings. (A) Seedlings were irradiated for 6 h with narrowband UV-B (+) or without (−). (B) Seedlings were irradiated for 6 h with supplemental narrowband UV-B and 15-min broadband UV-B (+) or without (−). (C and D) Coimmunoprecipitation of COP1 using UVR8 antibodies in extracts from wild-type (Col) (C) and rup1 rup2 double mutant (D). Seven-day-old seedlings were treated with 6 h narrowband UV-B and 15-min broadband UV-B, followed by recovery in white light (WL) for the indicated time.

We further investigated the stability of the UVR8–COP1 interaction post UV-B exposure to better understand how this facet of UVR8 signaling was inactivated. Following UV-B irradiation that leads to UVR8–COP1 interaction, we monitored the UVR8–COP1 interaction over a 4-h recovery period where seedlings were incubated under white light devoid of UV-B. In agreement with the timing of UVR8 redimerization (Fig. 1A), reduced UVR8–COP1 interaction was apparent already 30 min post UV-B exposure in wild-type seedlings (Fig. 3C). No further COP1 co-IP was detectable after 2 h white light incubation (Fig. 3C). In stark contrast, the UVR8–COP1 interaction was barely affected in rup1 rup2 double mutants after transfer from supplemental UV-B to white light, with clear COP1 co-IP maintained for up to 4 h post UV-B exposure (Fig. 3D). We conclude that UVR8 redimerization, heavily influenced by the action of RUP1 and RUP2, disrupts the UVR8–COP1 interaction. This highlights the underlying mechanism of RUP1 and RUP2 as repressors of the UVR8–signaling pathway.

RUP1 and RUP2 Regulate UVR8 Redimerization Independently of COP1.

Thus far, evidence has been provided for the role of RUP1 and RUP2 in UVR8 redimerization leading to disruption of the UVR8–COP1 interaction. However, the underlying interaction mechanism between these four proteins and the primary effect of RUP1 and RUP2 remains unknown. We initially hypothesized that interaction with COP1 stabilized the UVR8 monomer and that UVR8 redimerization is due to direct disruption of the UVR8–COP1 interaction by RUP1 and RUP2. To test this, we analyzed UVR8 redimerization in the absence of functional COP1. We generated cop1 rup1 rup2 triple mutants and compared UVR8 protein dynamics to that of cop1 single mutants, expecting to see comparable rates of UVR8 redimerization if our hypothesis held true. However, UVR8 redimerization was much slower in the cop1 rup1 rup2 triple mutant than in the cop1 mutant, clearly demonstrating that RUP1 and RUP2 mediate UVR8 redimerization even in the absence of COP1 (Fig. 4). Indeed, UVR8 redimerization was comparable in both cop1 and wild type, whereas it was notably impaired in rup1 rup2 and cop1 rup1 rup2 (Fig. 4). Combined, these data argue against a model in which RUP1- and RUP2-mediated disruption of the UVR8–COP1 interaction allows UVR8 redimerization. We thus propose an alternate model in which RUP1 and RUP2 mediate UVR8 redimerization independently of COP1, and it is this process that releases COP1. It remains to be determined whether the release of COP1 is solely due to UVR8 redimerization or whether competition between RUP1/RUP2 and COP1 for binding sites with UVR8 may play a role as well. The fact that inactive UVR8 dimers do not interact with COP1 (7) supports the hypothesis that the redimerization may be sufficient to impact on the UVR8–COP1 interaction.

Fig. 4.

Fig. 4.

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RUP1- and RUP2-mediated redimerization of UVR8 is independent of COP1. Seven-day-old seedlings were irradiated for 15 min with broadband UV-B before recovery in white light (WL) for the indicated times. UVR8 dimers were detectable in non–heat-denatured protein samples, as described before (7). Parallel denatured samples demonstrated equal amounts of UVR8 protein. An asterisk (*) indicates a nonspecific cross-reacting band.

Conclusions.

Light-induced changes in the structural conformation of plant photoreceptors is a common mechanism to “switch on” corresponding light-signaling pathways. Likewise, reconversion of the photoreceptor to its original conformation provides the signaling “off switch.” In the absence of UV-B, UVR8 exists as a homodimer held together by a large number of intermolecular hydrogen bonds that are disrupted following UV-B absorption by Trp-285 and Trp-233 leading to UVR8 monomerization (7, 20, 21). Here we demonstrate that RUP1 and RUP2 play a major role in the reversal of this process. The mechanistic and structural basis of how RUP1 and RUP2 mediate UVR8 redimerization to form inactive yet functional UVR8 homodimers awaits further investigation. Notwithstanding this, our present data clearly demonstrate that RUP1 and RUP2 provide negative regulation of the UVR8-mediated UV-B–signaling pathway by mediating UVR8 redimerization, which is of primary importance to optimally balance the UV-B–induced photomorphogenic response with plant growth and development.

Materials and Methods

Plant Material and Growth Conditions.

The cop1-4, uvr8-6, and rup1-1 rup2-1 mutants are in the Columbia (Col) accession (4, 22, 25). The RUP2-overexpression line RUP2Ox#3 is in the rup2-1 background (rup2-1/Pro35S:RUP2) (22). Arabidopsis seeds were surface-sterilized and sown on half-strength Murashige and Skoog basal salt medium (MS; Duchefa) containing 1% (wt/vol) sucrose and 1% (wt/vol) phytagel (Sigma). Seeds were stratified for 2 d at 4 °C and germinated at 22 °C in a standard growth chamber under constant white light.

For CHX experiments, seedlings were transferred to liquid half-strength MS medium containing 1% (wt/vol) sucrose for 15 h before 0.5 mM CHX in DMSO (Sigma) was added. For mock controls, an equivalent volume of DMSO was added.

UV-B treatments were performed using previously established conditions with broadband (Philips TL40W/12RS; 21 μmol⋅m−2⋅s−1) (17) or narrowband UV-B lamps (Philips TL20W/01RS; 1.5 μmol⋅m−2⋅s−1) (13), as indicated. Although both treatments activate UVR8 photoreceptor-dependent UV-B responses, broadband irradiation allows very efficient UVR8 monomerization with short-term irradiation (7), whereas narrowband irradiation allows long-term irradiation for physiological responses, but includes the activation of negative feedback regulation in parallel (4, 22).

Antibodies.

Rabbit polyclonal antibodies were generated against synthetic peptides derived from the UVR8 protein sequence [amino acids 410–424 + C: VPDETGLTDGSSKGNC; anti-UVR8(410–424)] and the COP1 protein sequence [amino acids C + 13–26: CVKPDPRTSSVGEGA; anti-COP1(13–26)] and were affinity-purified against the peptide (Eurogentec). Guinea pig polyclonal antibodies were generated against a synthetic peptide [amino acids C + 426–440: CGDISVPQTDVKRVRI; anti-UVR8(426–440)] already previously used to generate polyclonal UVR8 antibodies in rabbits (4) and were affinity-purified against the peptide (Eurogentec).

Protein Immunoprecipitation.

Proteins were extracted in extraction buffer [50 mM Tris, pH 7.5, 150 mM NaCl, 10% (vol/vol) glycerol, 5 mM MgCl2, 0.1% (vol/vol) Igepal, 2 mM benzamidine, 10 μM dichloroisocumarin, 1% (vol/vol) protease inhibitor mixture for plant extracts (Sigma), 10 μM MG132]. Immunoprecipitation of UVR8 was performed using anti-UVR8(426–440) polyclonal rabbit antibodies (4) for 2 h, and immunoprecipitate was captured with protein A-agarose (Roche Applied Science) for 1 h.

Protein Gel Blot Analysis.

For protein gel blot analysis, total cellular proteins (15 μg) or immunoprecipitates were separated by electrophoresis in 8% (wt/vol) SDS–polyacrylamide gels and electrophoretically transferred to PVDF membranes according to the manufacturer’s instructions (Bio-Rad). We used anti-COP1(13–26), anti-UVR8(426–440), anti-actin (A0480; Sigma-Aldrich), and anti-chalcone synthase (sc-12620; Santa Cruz Biotechnology) as primary antibodies, with HRP-conjugated protein A (Pierce) or anti-rabbit, anti-goat, and anti-mouse immunoglobulins (DAKO) used as secondary antibodies, as required. We used anti-UVR8(426–440) from guinea pig and HRP-conjugated anti-guinea pig secondary antibodies (ab7139; Abcam) to detect UVR8 in immunoprecipitates generated using anti-UVR8(426–440) from rabbits. Signal detection was performed using the ECL Plus Western Detection Kit (GE Healthcare).

Analysis of UVR8 dimers was conducted as follows: proteins were extracted in 50 mM Tris, pH 7.6, 150 mM NaCl, 2 mM EDTA, 1% (vol/vol) Igepal (Sigma), 1% (vol/vol) protease inhibitor mixture for plant extracts (Sigma), 10 μM MG132, and 10 μM N-Acetyl-L-leucyl-L-leucyl-L-norleucinal (ALLN). Twenty micrograms of proteins were separated by electrophoresis in 8% (wt/vol) SDS–polyacrylamide gels. Gels were UV-B–irradiated before electrophoretic transfer to PVDF membrane, as described previously (7). Blotting was performed using rabbit anti-UVR8(410–424) antibodies.

Supplementary Material

Supporting Information
supp_110_3_1113__index.html (7.1KB, html)

Acknowledgments

We are grateful to Kimberley Tilbrook and Michel Goldschmidt-Clermont for critically reading the manuscript. This study was supported by the University of Geneva and the Swiss National Science Foundation (Grant 31003A_132902).

Footnotes

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1214237110/-/DCSupplemental.

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