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The UV-B Photoreceptor UVR8: from Structure to Physiology

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The UV-B Photoreceptor UVR8: from Structure to Physiology The Plant Cell, Vol. 26: 21–37, January 2014, www.plantcell.org ã 2014 American Society of Plant Biologists. All rights reserved. REVIEW The UV-B Photoreceptor UVR8: From Structure to Physiology Gareth I. Jenkins1 Institute of Molecular, Cell, and Systems Biology, College of Medical, Veterinary, and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United Kingdom Low doses of UV-B light (280 to 315 nm) elicit photomorphogenic responses in plants that modify biochemical composition, photosynthetic competence, morphogenesis, and defense. UV RESISTANCE LOCUS8 (UVR8) mediates photomorphogenic responses to UV-B by regulating transcription of a set of target genes. UVR8 differs from other known photoreceptors in that it uses specific Trp amino acids instead of a prosthetic chromophore for light absorption during UV-B photoreception. Absorption of UV-B dissociates the UVR8 dimer into monomers, initiating signal transduction through interaction with CONSTITUTIVELY PHOTOMORPHOGENIC1. However, much remains to be learned about the physiological role of UVR8 and its interaction with other signaling pathways, the molecular mechanism of UVR8 photoreception, how the UVR8 protein initiates signaling, how it is regulated, and how UVR8 regulates transcription of its target genes. INTRODUCTION below (Caldwell et al., 1983; Jordan 1996; Rozema et al., 1997; Frohnmeyer and Staiger, 2003; Jenkins, 2009). Damage caused Light is of paramount importance in promoting the growth and by UV-B exposure is ameliorated in several ways, in particular by development of plants. In addition to its role as the energy source antioxidant systems and enzymes that repair DNA damage. An for photosynthesis, light regulates numerous aspects of plant important feature of these protective responses is that they are form and function throughout the life cycle, from seedling es- stimulated when plants are exposed to UV-B. fl tablishment to owering time. These developmental responses Studies in the last century established that UV-B has regulatory to light, termed photomorphogenesis, are complex in that plants effects on plant growth, morphology, and biochemical content respond to several different facets of their radiation environ- (Klein, 1978). It was discovered that low doses of UV-B initiate ment, in particular its spectral quality, the amount of light (de- photomorphogenic responses that could not be explained by fi fl ned as the photon uence rate), and the duration and direction the action of known photoreceptors and were not a consequence of illumination. To detect and respond to light, plants employ of DNA damage (Wellmann, 1976, 1983). The action spectrum a suite of photoreceptors coupled to a network of signaling for DNA damage peaks at ;260 nm, whereas action spectra for components and transcriptional effectors (Jiao et al., 2007; Kami photomorphogenic UV-B responses peak at ;295 to 300 nm et al., 2010). Whereas a wealth of information has been obtained (Wellmann, 1976; Ensminger, 1993; Jenkins, 2009; Jiang et al., about the photoreceptors and signaling mechanisms that plants 2012a). Photomorphogenic responses to UV-B include the sup- use to detect light in the UV-A to far-red regions of the spec- pression of both hypocotyl extension and root growth in the low trum, much less is known about the perception of UV-B light fluence range and the promotion of cotyledon opening (Wellmann, (280 to 315 nm), which mediates numerous regulatory responses 1976; Ballaré et al., 1995; Kim et al., 1998; Boccalandro et al., in plants (Jordan, 1996; Jansen, 2002; Frohnmeyer and Staiger, 2001; Suesslin and Frohnmeyer, 2003; Shinkle et al., 2004; Tong 2003; Ulm and Nagy, 2005; Jenkins, 2009). et al., 2008; Conte et al., 2010). However, perhaps the most UV-B radiation has a major impact on virtually all organisms, extensively characterized photomorphogenic response to UV-B despite being a very small fraction of the daylight spectrum. Most is the biosynthesis of flavonoid compounds, which are con- UV-B is absorbed by the stratospheric ozone layer, and only stituents of the UV-absorbing sun screen (Caldwell et al., 1983; ; wavelengths above 295 nm reach the surface of our planet. Hahlbrock and Scheel, 1989; Rozema et al., 1997; Ryan et al., Because of its relatively high energy, UV-B radiation has the 2001; Winkel-Shirley, 2002). Low doses of UV-B strongly stimulate potential to damage molecules, such as DNA, and consequently the transcription of flavonoid biosynthesis genes, including that to impair cellular processes, which ultimately may cause death. encoding the key enzyme chalcone synthase (CHS) (Hahlbrock Thus, organisms have evolved strategies both to avoid and re- and Scheel, 1989; Frohnmeyer et al., 1999; Jenkins et al., 2001; pair damage by UV-B. In plants, protection includes the pro- Hartmann et al., 2005). In addition, low doses of UV-B regulate fl duction of re ective surface waxes and hairs and the synthesis the expression of numerous other genes associated with various “ ” of UV-absorbing phenolic sun-screen compounds that accu- plant processes (Ulm et al., 2004; Brown et al., 2005; Favory mulate in the epidermal layer and reduce transmittance to cells et al., 2009). The discovery that plants exhibit photomorphogenic respon- 1 Address correspondence to [email protected]. ses to UV-B suggested the existence of a UV-B photoreceptor www.plantcell.org/cgi/doi/10.1105/tpc.113.119446 comparable to other known photoreceptors. However, research 22 The Plant Cell over several decades failed to shed much light on the nature Table 1. Responses to UV-B Mediated by UVR8 of the UV-B photoreceptor or the mechanisms of photomor- phogenic UV-B signaling. Biochemical and genetic studies Response Referencesa showed that photomorphogenic UV-B responses are distinct Gene regulation 1–10 from phytochrome- and cryptochrome-mediated responses UV-B tolerance 1–4 (Ballaré et al., 1995; Christie and Jenkins, 1996; Frohnmeyer Flavonoid biosynthesis 1, 4, 6, 10, 13 et al., 1998; Boccalandro et al., 2001; Suesslin and Frohnmeyer, Hypocotyl growth suppression 4, 12, 14 2003) and that DNA damage signaling, reactive oxygen species Leaf/epidermal cell expansion 4, 10, 11 signaling, and wound and defense signaling pathways, which Endoreduplication in epidermal cells 11 are important in mediating some responses to UV-B (Jenkins, Stomata per epidermal cell 11 2009), are not the mechanism of photomorphogenic UV-B per- Entrainment of circadian clock 7 Increased photosynthetic efficiency 8 ception (Boccalandro et al., 2001; Jenkins et al., 2001; Ulm et al., Tolerance of B. cinerea infection 13 2004; Gadjev et al., 2006; Jenkins, 2009; González Besteiro et al., a 2011). Progress in the identification of a UV-B photoreceptor 1, Kliebenstein et al. (2002); 2, Brown et al. (2005); 3, Brown and Jenkins came from the application of a genetic approach. Kliebenstein (2008); 4, Favory et al. (2009); 5, Brown et al. (2009); 6, Grüber et al. (2010); 7, Fehér et al. (2011); 8, Davey et al. (2012); 9, Lang-Mladek et al. et al. (2002) isolated an Arabidopsis thaliana mutant of UV (2012); 10, Morales et al. (2013); 11, Wargent et al. (2009); 12, Cloix et al. RESISTANCE LOCUS8 (UVR8), which was subsequently shown to (2012); 13, Demkura and Ballaré (2012); 14, Huang et al. (2013). act as a UV-B photoreceptor (Rizzini et al., 2011). More recently, structural studies have revealed the molecular basis of photo- reception by UVR8 (Christie et al., 2012; Wu et al., 2012). This Rather, UVR8 encodes a seven-bladed b-propeller protein (Figure 1B) article will focus on the physiological role of UVR8, its structure, with moderate similarity to human REGULATOR OF CHROMATIN and the mechanisms of photoreception, signal transduction, and CONDENSATION1 (RCC1), a guanine nucleotide exchange factor regulation. Further discussion of UVR8 can be found in other involved in nucleocytoplasmic transport and the regulation of cell recent reviews (Jenkins, 2009; Heijde and Ulm, 2012; Jiang et al., cycle progression and mitosis (Renault et al., 1998). However, this 2012a; Li et al., 2013; Tilbrook et al., 2013). similarity is purely structural, and there is no evidence of func- tional homology between UVR8 and RCC1 (Brown et al., 2005). The initial characterization of uvr8-1 did not establish whether PHYSIOLOGICAL ROLE OF UVR8 the mutant was altered specifically in responses to UV-B and did The exploration of UVR8 function in vivo is still at an early stage. not explain the basis of its hypersensitivity to UV-B. Sub- Initial studies focused on gene regulation by UVR8 and dem- sequently, Brown et al. (2005) isolated additional uvr8 alleles and onstrated its importance in UV protection. Subsequently, addi- showed that CHS expression in the mutant was only affected by tional aspects of UVR8 function have emerged (Table 1). Present UV-B and not by several other stimuli, indicating that UVR8 acts research is starting to reveal how UVR8 is integrated with other in a UV-B–specific manner. Given that UVR8 functions as a UV-B photoreceptor pathways in mediating responses in vivo. How- photoreceptor, it is unlikely to be involved directly in mediating ever, it is important to remember that virtually everything we responses to other stimuli. Nevertheless, as discussed below, know about UVR8 is derived from studies with Arabidopsis,so UVR8 could influence responses to other stimuli through cross- much remains to be learnt about its physiological role in other, talk with light and non-light signaling pathways, and it is also diverse species. conceivable that other environmental factors could modulate the action of UVR8. Gene Regulation Underpins UVR8 Function UVR8 acts by regulating transcription of a set of genes. Using microarray analysis, Brown et al. (2005) showed that UVR8 reg- The Arabidopsis uvr8-1 mutant was isolated in a screen for plants ulates expression of over 70 genes in response to UV-B in mature hypersensitive to UV-B (Kliebenstein et al., 2002).
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