Photoactivated UVR8-COP1 Module Determines Photomorphogenic UV-B Signaling Output in Arabidopsis

In Arabidopsis, ultraviolet (UV)-B-induced photomorphogenesis is initiated by a unique photoreceptor UV RESISTANCE LOCUS 8 (UVR8) which utilizes its tryptophan residues as internal chromophore to sense UV-B. As a result of UV-B light perception, the UVR8 homodimer shaped by its arginine residues undergoes a conformational switch of monomerization. Then UVR8 associates with the CONSTITUTIVELY PHOTOMORPHOGENIC 1-SUPPRESSOR OF PHYA (COP1-SPA) core complex(es) that is released from the CULLIN 4-DAMAGED DNA BINDING PROTEIN 1 (CUL4-DDB1) E3 apparatus. This association, in turn, causes COP1 to convert from a repressor to a promoter of photomorphogenesis. It is not fully understood, however, regarding the biological significance of light-absorbing and dimer-stabilizing residues for UVR8 activity in photomorphogenic UV-B signaling. Here, we take advantage of transgenic UVR8 variants to demonstrate that two light-absorbing tryptophans, W233 and W285, and two dimer-stabilizing arginines, R286 and R338, play pivotal roles in UV-B-induced photomorphogenesis. Mutation of each residue results in alterations in UV-B light perception, UVR8 monomerization and UVR8-COP1 association in response to photomorphogenic UV-B. We also identify and functionally characterize two constitutively active UVR8 variants, UVR8^W285A and UVR8^R338A, whose photobiological activities are enhanced by the repression of CUL4, a negative regulator in this pathway. Based on our molecular and biochemical evidence, we propose that the UVR8-COP1 affinity in plants critically determines the photomorphogenic UV-B signal transduction coupling with UVR8-mediated UV-B light perception.     

Organization of protein complexes under photomorphogenic UV-B in Arabidopsis

Low-fluence and long-wavelength UV-B light promotes photomorphogenic development in Arabidopsis. CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) is a positive regulator in this pathway while it is a negative regulator of the traditional photomorphogenesis triggered by far-red and visible light. We have recently reported the mechanism by which the switch of COP1 function is accomplished in distinct light contexts. In response to photomorphogenic UV-B, the photoactivated UV RESISTANCE LOCUS 8 (UVR8) associates with the COP1- SUPRESSOR OF PHYA (SPA) core complexes, resulting in the physical and functional disassociation of COP1-SPA from the CULLIN4-DAMAGED DNA BINDING PROTEIN 1 (CUL4-DDB1) E3 scaffold. These UV-B dependent UVR8-COP1-SPA complexes promote the stability and activity of ELONGATED HYPOCOTYL 5 (HY5), and eventually cause COP1 to switch from repressing to promoting photomorphogenesis. In addition, it is possible that CUL4-DDB1 might simultaneously recruit alternative DDB1 BINDING WD40 (DWD) proteins to repress this UV-B-specific signaling. Further investigation is required, however, to verify this hypothesis. Overall, the coordinated organization of various protein complexes facilitates an efficient and balanced UV-B signaling.     

植物UV-B生理效应的分子机制研究进展

中波紫外线UV-B（280～320nm）是植物必需的太阳光线的组成部分,具有明显的双重效应：一方面UV-B在强度较高时,就触发产生大量活性氧对DNA、蛋白质以及生物膜等造成伤害,同时植物通过抗氧化系统对其作出防御反应以减轻伤害;另一方面,低强度的UV-B是植物生长发育的光信号因子之一,经由UVR8等光受体介导中、低、极低强度的UV-B信号,可能通过几个分子途径控制相关基因的表达,分别对植物的UV-B保护基因表达、形态建成、昼夜节律、生长发育等进行调控。目前对UVR8介导的低强度UV-B信号转导的分子机制研究相对深入。在本文中,将对UV-B生理效应分子机制的最新研究进展作一个比较全面的介绍。     

Arabidopsis MAP kinase phosphatase 1 and its target MAP kinases 3 and 6 antagonistically determine UV-B stress tolerance, independent of the UVR8 photoreceptor pathway

Plants perceive UV-B radiation as an informational signal by a pathway involving UVR8 as UV-B photoreceptor, activating photomorphogenic and acclimation responses. In contrast, the response to UV-B as an environmental stress involves mitogen-activated protein kinase (MAPK) signalling cascades. Whereas the perception pathway is plant specific, the UV-B stress pathway is more broadly conserved. Knowledge of the UV-B stress-activated MAPK signalling pathway in plants is limited, and its potential interplay with the UVR8-mediated pathway has not been defined. Here, we show that loss of MAP kinase phosphatase 1 in the mutant mkp1 results in hypersensitivity to acute UV-B stress, but without impairing UV-B acclimation. The MKP1-interacting proteins MPK3 and MPK6 are activated by UV-B stress and are hyperactivated in mkp1. Moreover, mutants mpk3 and mpk6 exhibit elevated UV-B tolerance and partially suppress the UV-B hypersensitivity of mkp1. We show further that the MKP1-regulated stress-response MAPK pathway is independent of the UVR8 photoreceptor, but that MKP1 also contributes to survival under simulated sunlight. We conclude that, whereas UVR8-mediated acclimation in plants promotes UV-B-induced defence measures, MKP1-regulated stress signalling results when UV-B protection and repair are insufficient and damage occurs. The combined activity of these two mechanisms is crucial to UV-B tolerance in plants.     

光受体UVR8对UV-B响应机制研究进展

来自太阳光谱中的UV-B辐射被认为是一种重要的环境信号,可以被植物感受并诱导植物调整自身生长和发育状态以适应环境。人们对植物中光敏色素、隐花色素和蓝光受体向光素的研究已非常深入,但对植物响应UV-B的机制仅在最近才取得一些突破性进展。这些研究发现,植物中存在着UV-B受体UVR8(UV Resistance Locus 8)。目前认为,UVR8二聚体感应UV-B后瞬间解聚为单体,并与E3泛素连接酶COP1(constitutively photomorphogenic 1)相互作用,从而激活UV-B响应基因的表达。该文从UVR8的发现、UVR8的结构和感受UV-B机制、UVR8二聚体重新形成以及UV-B信号传导与可见光信号传导途径间的差异等方面综述了关于UV-B受体UVR8的最新研究成果。     

UV-B photoreceptor-mediated signalling in plants

Ultraviolet-B radiation (UV-B) is a key environmental signal that is specifically perceived by plants to promote UV acclimation and survival in sunlight. Whereas the plant photoreceptors for visible light are rather well characterised, the UV-B photoreceptor UVR8 was only recently described at the molecular level. Here, we review the current understanding of the UVR8 photoreceptor-mediated pathway in the context of UV-B perception mechanism, early signalling components and physiological responses. We further outline the commonalities in UV-B and visible light signalling as well as highlight differences between these pathways.     

植物UV-B受体及其介导的光信号转导

拟南芥（Arabidopsis thaliana）蛋白UVR8（UV RESISTANCE LOCUS 8）是UV-B特异的光受体,介导UV-B诱导的光形态建成。无UV-B照射时,UVR8以二聚体的形式存在于细胞质和细胞核中。接收到UV-B光信号后,细胞质中的UVR8转移到细胞核中并解聚,之后与E3泛素连接酶COP1（CONSTITUTIVELY PHOTOMORPHOGENIC 1）相互作用,调节一系列重要的UV防御基因的表达。UVR8除了作为UV-B特异的光受体,在细胞中也具有重要作用,协调整个植物体对UV-B的应答。该文重点综述了UVR8蛋白的结构、生理功能及其介导的UV-B光信号转导分子机制等方面的研究进展。     

UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate accumulation

Light is emerging as a central regulator of plant immune responses against herbivores and pathogens. Solar UV-B radiation plays an important role as a positive modulator of plant defense. However, since UV-B photons can interact with a wide spectrum of molecular targets in plant tissues, the mechanisms that mediate their effects on plant defense have remained elusive. Here, we show that ecologically meaningful doses of UV-B radiation increase Arabidopsis resistance to the necrotrophic fungus Botrytis cinerea and that this effect is mediated by the photoreceptor UVR8. The UV-B effect on plant resistance was conserved in mutants impaired in jasmonate (JA) signaling (jar1-1 and P35S:JAZ10.4) or metabolism of tryptophan-derived defense compounds (pen2-1, pad3-1, pen2 pad3), suggesting that neither regulation of the JA pathway nor changes in levels of indolic glucosinolates (iGS) or camalexin are involved in this response. UV-B radiation, acting through UVR8, increased the levels of flavonoids and sinapates in leaf tissue. The UV-B effect on pathogen resistance was still detectable in tt4-1, a mutant deficient in chalcone synthase and therefore impaired in the synthesis of flavonoids, but was absent in fah1-7, a mutant deficient in ferulic acid 5-hydroxylase, which is essential for sinapate biosynthesis. Collectively, these results indicate that UVR8 plays an important role in mediating the effects of UV-B radiation on pathogen resistance by controlling the expression of the sinapate biosynthetic pathway.     

Two Distinct Domains of the UVR8 Photoreceptor Interact with COP1 to Initiate UV-B Signaling in Arabidopsis

UV-B photon reception by the Arabidopsis thaliana homodimeric UV RESISTANCE LOCUS8 (UVR8) photoreceptor leads to its monomerization and a crucial interaction with CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1). Relay of the subsequent signal regulates UV-B-induced photomorphogenesis and stress acclimation. Here, we report that two separate domains of UVR8 interact with COP1: the β-propeller domain of UVR8 mediates UV-B-dependent interaction with the WD40 repeats-based predicted β-propeller domain of COP1, whereas COP1 activity is regulated by interaction through the UVR8 C-terminal C27 domain. We show not only that the C27 domain is required for UVR8 activity but also that chemically induced expression of the C27 domain is sufficient to mimic UV-B signaling. We further show, in contrast with COP1, that the WD40 repeat proteins REPRESSOR OF UV-B PHOTOMORPHOGENESIS1 (RUP1) and RUP2 interact only with the UVR8 C27 domain. This coincides with their facilitation of UVR8 reversion to the ground state by redimerization and their potential to interact with UVR8 in a UV-B-independent manner. Collectively, our results provide insight into a key mechanism of photoreceptor-mediated signaling and its negative feedback regulation.     

Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1

To further our understanding of how plants defend against the harmful effects of ultraviolet (UV) light, we characterized an Arabidopsis mutant hypersensitive to UV-B. This mutant, UV resistance locus 8-1 (uvr8-1), contains a single recessive mutation at the bottom of chromosome 5. Fine-scale mapping localized uvr8-1 to a 21-kb locus containing five predicted open reading frames. Sequencing of this entire region revealed that the uvr8-1 allele contains a 15-nucleotide deletion in a gene similar to the human guanine nucleotide exchange factor regulator of chromatin condensation 1. This mutation reduces the UV-B-mediated induction of flavonoids and blocks chalcone synthase mRNA and protein induction. In contrast, uvr8-1 has enhanced induction of PR1 and PR5 proteins in response to UV-B, an indication of increased UV-B injury. These results suggest that UVR8 acts in a UV-B signal transduction pathway leading to induction of flavonoid biosynthesis.     

How plants protect themselves from ultraviolet-B radiation stress

Ultraviolet-B (UV-B) radiation has a wavelength range of 280–315 nm. Plants perceive UV-B as an environmental signal and a potential abiotic stress factor that affects development and acclimation. UV-B regulates photomorphogenesis including hypocotyl elongation inhibition, cotyledon expansion, and flavonoid accumulation, but high intensity UV-B can also harm plants by damaging DNA, triggering accumulation of reactive oxygen species, and impairing photosynthesis. Plants have evolved “sunscreen” flavonoids that accumulate under UV-B stress to prevent or limit damage. The UV-B receptor UV RESISTANCE LOCUS 8 (UVR8) plays a critical role in promoting flavonoid biosynthesis to enhance UV-B stress tolerance. Recent studies have clarified several UVR8-mediated and UVR8-independent pathways that regulate UV-B stress tolerance. Here, we review these additions to our understanding of the molecular pathways involved in UV-B stress tolerance, highlighting the important roles of ELONGATED HYPOCOTYL 5, BRI1-EMS-SUPPRESSOR1, MYB DOMAIN PROTEIN 13, MAP KINASE PHOSPHATASE 1, and ATM- and RAD3-RELATED. We also summarize the known interactions with visible light receptors and the contribution of melatonin to UV-B stress responses. Finally, we update a working model of the UV-B stress tolerance pathway.

Recent findings that update our understanding of the molecular pathway for ultraviolet-B radiation stress responses in plants are summarized.