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C-Terminal Region of the UV-B Photoreceptor UVR8 Initiates Signaling Through Interaction with the COP1 Protein

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C-Terminal Region of the UV-B Photoreceptor UVR8 Initiates Signaling Through Interaction with the COP1 Protein C-terminal region of the UV-B photoreceptor UVR8 initiates signaling through interaction with the COP1 protein Catherine Cloix, Eirini Kaiserli1, Monika Heilmann, Katherine J. Baxter, Bobby A. Brown, Andrew O’Hara, Brian O. Smith, John M. Christie, and Gareth I. Jenkins2 Institute of Molecular, Cell and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom Edited by Anthony R. Cashmore, University of Pennsylvania, Philadelphia, PA, and approved August 21, 2012 (received for review June 27, 2012) UV-B light initiates photomorphogenic responses in plants. Arabi- UVR8 is a seven-bladed β-propeller protein (8, 10, 11). UVR8 dopsis UV RESISTANCE LOCUS8 (UVR8) specifically mediates these exists as a homodimer in plants and in vitro, which rapidly disso- responses by functioning as a UV-B photoreceptor. UV-B exposure ciates to form monomers following exposure to low doses of UV-B converts UVR8 from a dimer to a monomer, stimulates the rapid (10–12). Recent elucidation of the crystal structure of UVR8 accumulation of UVR8 in the nucleus, where it binds to chromatin, shows that the dimer is maintained by salt-bridge interactions and induces interaction of UVR8 with CONSTITUTIVELY PHOTO- between specific charged amino acids at the dimer interface (10, MORPHOGENIC1 (COP1), which functions with UVR8 to control pho- 11). UV-B is perceived by specific excitonically coupled trypto- tomorphogenic UV-B responses. Although the crystal structure of phans that are adjacent to salt-bridging arginine residues, and UVR8 reveals the basis of photoreception, it does not show how hence photoreception results in breakage of salt bridges leading to UVR8 initiates signaling through interaction with COP1. Here we monomerization. Photoreception leads to the rapid nuclear ac- report that a region of 27 amino acids from the C terminus of cumulation of UVR8 (13) and interaction with the COP1 protein UVR8 (C27) mediates the interaction with COP1. The C27 region is (5, 12). Although necessary for UVR8 function, nuclear localiza- necessary for UVR8 function in the regulation of gene expression tion alone is insufficient to cause expression of target genes; UV-B and hypocotyl growth suppression in Arabidopsis. However, UVR8 exposure is still needed to activate UVR8 in the nucleus (13). lacking C27 still undergoes UV-B–induced monomerization in both COP1 and UVR8 regulate essentially the same set of genes (5, 14) yeast and plant protein extracts, accumulates in the nucleus in re- and this positive regulatory function contrasts with the role of sponse to UV-B, and interacts with chromatin at the UVR8-regulated COP1 as a negative regulator of photomorphogenesis in dark- ELONGATED HYPOCOTYL5 (HY5) gene. The UV-B–dependent inter- grown seedlings (15). In UV-B responses, COP1 is required for the action of UVR8 and COP1 is reproduced in yeast cells and we show stimulation of HY5 gene expression (14), whereas in dark-grown that C27 is both necessary and sufficient for the interaction of UVR8 seedlings COP1 acts as an E3 ubiquitin ligase to promote the de- with the WD40 domain of COP1. Furthermore, we show that C27 struction of HY5 (16). There is no evidence that COP1 acts as an interacts in yeast with the REPRESSOR OF UV-B PHOTOMORPHO- E3 ubiquitin ligase in UV-B photomorphogenic responses, al- GENESIS proteins, RUP1 and RUP2, which are negative regulators though in principle it could act to degrade an unidentified negative of UVR8 function. Hence the C27 region has a key role in UVR8 regulator of the responses. The RUP1 and RUP2 proteins nega- function. tively regulate UV-B photomorphogenic responses and interact directly with UVR8, but COP1 is required for their UV-B–induced V-B wavelengths (280–315 nm) are a minor component of expression, along with UVR8, rather than their degradation (17). Usunlight but have a major impact on living organisms. The The recent determination of UVR8 structure combined with damaging effects of UV-B are well documented, but plants rarely mutational analysis explains how UVR8 acts in photoreception (10, show signs of UV-damage despite constant exposure to sunlight. 11). However, these studies do not show how UVR8 interacts with This is because plants have evolved effective means of protection COP1 to initiate signaling, which is key to understanding UVR8 against UV-B, including the deposition of UV-absorbing phenolic function. Here we identify the region of UVR8 that interacts with compounds in the outer tissues and the production of efficient COP1 and show that it has a crucial role in UVR8 function in vivo. antioxidant and DNA repair systems (1–4). These UV-protective mechanisms are stimulated by low doses of UV-B through dif- Results ferential gene expression. Moreover, low levels of UV-B regulate C-Terminal 27-Amino-Acid Region of UVR8 Is Required for Function in uvr8 other responses in plants, including the suppression of hypocotyl Plants. In a previous mutant screen (6) we isolated several A uvr8-2 extension (5). Thus, in plants, UV-B acts as a key regulatory signal alleles (Fig. S1 ). One allele ( ) has a premature stop codon that initiates photomorphogenic responses and promotes survival. and lacks 40 amino acids at the C terminus of the protein. The uvr8-2 B The low dose, photomorphogenic responses to UV-B are truncated protein is detectable in plants (Fig. S1 ) but the CHS mediated by the photoreceptor UVR8 (3–7). UVR8 acts spe- mutant fails to induce UVR8-regulated transcripts in re- C cifically in UV-B to regulate over 100 genes, many of which are sponse to UV-B exposure (Fig. S1 ). A 27-amino-acid region from involved in UV protection (5, 6). Arabidopsis uvr8 mutant plants are highly sensitive to UV-B because they fail to express UV- protective genes (6, 8). Among the genes regulated by UVR8 is Author contributions: G.I.J. designed research; C.C., E.K., M.H., K.J.B., B.A.B., and A.O. performed research; C.C., E.K., M.H., B.O.S., J.M.C., and G.I.J. analyzed data; and G.I.J. that encoding the ELONGATED HYPOCOTYL 5 (HY5) wrote the paper. transcription factor, which mediates most, if not all, gene ex- The authors declare no conflict of interest. pression responses initiated by UVR8 (6, 7). UVR8 interacts This article is a PNAS Direct Submission. HY5 with chromatin via histones, in particular H2B (9) at the 1Present address: Chory Laboratory, Plant Biology, The Salk Institute for Biological Stud- gene (6, 9) and a number of other UVR8-regulated genes (9), ies, La Jolla, CA 92037. which raises the possibility that UVR8 promotes recruitment or 2To whom correspondence should be addressed. E-mail: [email protected]. activation of transcription factors and/or chromatin remodeling This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. proteins that regulate target genes such as HY5. 1073/pnas.1210898109/-/DCSupplemental. 16366–16370 | PNAS | October 2, 2012 | vol. 109 | no. 40 www.pnas.org/cgi/doi/10.1073/pnas.1210898109 Downloaded by guest on October 1, 2021 the C terminus of UVR8 (C27; amino acids 397–423) contains required for function, it is not required for UVR8 to bind to a number of amino acids that are highly conserved among UVR8 chromatin at a target gene locus. proteins from different plant species (boxed in Fig. S2), but not UV-B promotes the conversion of UVR8 from a dimer to present in sequences related to UVR8, such as eukaryotic RCC1 a monomer in vitro (10), in plants and when it is expressed het- (8). The fact that these amino acids are lacking in the uvr8-2 mu- erologously in yeast (12). Fig. 2B shows the effect of UV-B illu- tant led us to investigate their role in UVR8 function. mination on HA-tagged UVR8 in protein extracts of yeast. UVR8 lacking specifically the C27 region, with a translational Following UV-B illumination of the extracts, proteins were re- GFP fusion at the N terminus was expressed in uvr8-1 null mutant solved by native gel electrophoresis and HA–UVR8 was detected plants under the control of the native UVR8 promoter (Fig. 1A). by an anti-HA antibody. The HA–UVR8 dimer is present before The level of expression of the GFP–ΔC27UVR8 fusion in trans- illumination and the monomer is detectable after 5 min illumination genic plants (Fig. 1B) was similar to that of a wild-type GFP– with a relatively low fluence rate of UV-B. Longer exposures gen- UVR8 fusion that was shown previously to complement the im- erate increasing amounts of the monomer while the amount of di- paired UV-B induction of gene expression in uvr8-1 (13) (Fig. 1C). mer decreases. The same result is observed with yeast expressing However, as shown in Fig. 1C,GFP–ΔC27UVR8 fails to com- HA–ΔC27UVR8. plement uvr8-1 in that no UV-B induction of UVR8-regulated UVR8 monomerization is observed when plant extracts are HY5 transcripts is observed in three independent transgenic lines. exposed specifically to UV-B wavelengths (Fig. S4) and analyzed Moreover, uvr8-1 plants transformed with GFP–ΔC27UVR8 are by SDS/PAGE without boiling to denature the samples (12). The highly sensitive to UV-B, similar to the uvr8-1 mutant (Fig. S3). UVR8 dimer is very resistant to SDS when not boiled (10–12) and Therefore, the C27 region is required for UVR8 function in vivo. only dissociates in the absence of UV-B under low pH (10) or high To further examine the role of the C27 region in UVR8 function salt (11).
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