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      Tomato UV-B receptor SlUVR8 mediates plant acclimation to UV-B radiation and enhances fruit chloroplast development via regulating SlGLK2

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          Abstract

          Plants utilize energy from sunlight to perform photosynthesis in chloroplast, an organelle that could be damaged by solar UV radiation. The ultraviolet-B (UV-B) photoreceptor UVR8 is required for UV-B perception and signal transduction. However, little is known about how UVR8 influence chloroplast development under UV-B radiation. Here, we characterized tomato UVR8 gene ( SlUVR8) and our results indicated that SlUVR8 facilitate plant acclimation to UV-B stress by orchestrating expression of the UVB-responsive genes ( HY5 and CHS) and accumulating UV-absorptive compounds. In addition, we also discovered that SlUVR8 promotes fruit chloroplast development through enhancing accumulation of transcription factor GOLDEN2-LIKE2 (SlGLK2) which determines chloroplast and chlorophyll levels. Furthermore, UV-B radiation could increase expression of SlGLK2 and its target genes in fruits and leaves. SlUVR8 is required for UVB-induced SlGLK2 expression. Together, our work not only identified the conserved functions of SlUVR8 gene in response to UV-B stress, but also uncovered a novel role that SlUVR8 could boost chloroplast development by accumulating SlGLK2 proteins.

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          Perception of UV-B by the Arabidopsis UVR8 protein.

          To optimize their growth and survival, plants perceive and respond to ultraviolet-B (UV-B) radiation. However, neither the molecular identity of the UV-B photoreceptor nor the photoperception mechanism is known. Here we show that dimers of the UVR8 protein perceive UV-B, probably by a tryptophan-based mechanism. Absorption of UV-B induces instant monomerization of the photoreceptor and interaction with COP1, the central regulator of light signaling. Thereby this signaling cascade controlled by UVR8 mediates UV-B photomorphogenic responses securing plant acclimation and thus promotes survival in sunlight.
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            Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis.

            The ultraviolet-B (UV-B) portion of the solar radiation functions as an environmental signal for which plants have evolved specific and sensitive UV-B perception systems. The UV-B-specific UV RESPONSE LOCUS 8 (UVR8) and the multifunctional E3 ubiquitin ligase CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) are key regulators of the UV-B response. We show here that uvr8-null mutants are deficient in UV-B-induced photomorphogenesis and hypersensitive to UV-B stress, whereas overexpression of UVR8 results in enhanced UV-B photomorphogenesis, acclimation and tolerance to UV-B stress. By using sun simulators, we provide evidence at the physiological level that UV-B acclimation mediated by the UV-B-specific photoregulatory pathway is indeed required for survival in sunlight. At the molecular level, we demonstrate that the wild type but not the mutant UVR8 and COP1 proteins directly interact in a UV-B-dependent, rapid manner in planta. These data collectively suggest that UV-B-specific interaction of COP1 and UVR8 in the nucleus is a very early step in signalling and responsible for the plant's coordinated response to UV-B ensuring UV-B acclimation and protection in the natural environment.
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              A UV-B-specific signaling component orchestrates plant UV protection.

              UV-B radiation in sunlight has diverse effects on humans, animals, plants, and microorganisms. UV-B can cause damage to molecules and cells, and consequently organisms need to protect against and repair UV damage to survive in sunlight. In plants, low nondamaging levels of UV-B stimulate transcription of genes involved in UV-protective responses. However, remarkably little is known about the underlying mechanisms of UV-B perception and signal transduction. Here we report that Arabidopsis UV RESISTANCE LOCUS 8 (UVR8) is a UV-B-specific signaling component that orchestrates expression of a range of genes with vital UV-protective functions. Moreover, we show that UVR8 regulates expression of the transcription factor HY5 specifically when the plant is exposed to UV-B. We demonstrate that HY5 is a key effector of the UVR8 pathway, and that it is required for survival under UV-B radiation. UVR8 has sequence similarity to the eukaryotic guanine nucleotide exchange factor RCC1, but we found that it has little exchange activity. However, UVR8, like RCC1, is located principally in the nucleus and associates with chromatin via histones. Chromatin immunoprecipitation showed that UVR8 associates with chromatin in the HY5 promoter region, providing a mechanistic basis for its involvement in regulating transcription. We conclude that UVR8 defines a UV-B-specific signaling pathway in plants that orchestrates the protective gene expression responses to UV-B required for plant survival in sunlight.
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                Author and article information

                Contributors
                liu_ys@scu.edu.cn
                wangsh1@cib.ac.cn
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                17 April 2018
                17 April 2018
                2018
                : 8
                : 6097
                Affiliations
                [1 ]ISNI 0000 0001 0807 1581, GRID grid.13291.38, Ministry of Education Key Laboratory for Bio-resource and Eco-environment, , College of Life Science, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, ; Chengdu, 610064 China
                [2 ]ISNI 0000 0000 9339 5152, GRID grid.458441.8, CAS Center for Excellence in Molecular Plant Sciences, , Chengdu Institute of Biology, Chinese Academy of Sciences, ; Chengdu, 610041 China
                [3 ]GRID grid.256896.6, School of Biotechnology and Food Engineering, , Hefei University of Technology, ; Hefei, 230009 China
                [4 ]ISNI 0000 0004 1808 3334, GRID grid.440649.b, School of Life Science and Engineering, , Southwest University of Science and Technology, ; Mianyang, Sichuan 621010 China
                [5 ]ISNI 0000 0004 0646 966X, GRID grid.449637.b, Shaanxi University of Chinese Medicine/Shaanxi Collaborative Innovation Center of Chinese Medicinal Resources Industrialization, ; Shaanxi Sheng, China
                Article
                24309
                10.1038/s41598-018-24309-y
                5904186
                29666396
                7f21469a-4c6a-49cf-8244-25f930525544
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 16 May 2017
                : 27 March 2018
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