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      Convergence of Light and ABA Signaling on the ABI5 Promoter

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          Abstract

          Light is one of the most important environmental cues regulating multiple aspects of plant growth and development, and abscisic acid (ABA) is a plant hormone that plays important roles during many phases of the plant life cycle and in plants' responses to various environmental stresses. How plants integrate the external light signal with endogenous ABA pathway for better adaptation and survival remains poorly understood. Here, we show that BBX21 (also known as SALT TOLERANCE HOMOLOG 2), a B-box (BBX) protein previously shown to positively regulate seedling photomorphogenesis, is also involved in ABA signaling. Our genetic data show that BBX21 may act upstream of several ABA INSENSITIVE (ABI) genes and ELONGATED HYPOCOTYL 5 (HY5) in ABA control of seed germination. Previous studies showed that HY5 acts as a direct activator of ABI5 expression, and that BBX21 interacts with HY5. We further demonstrate that BBX21 negatively regulates ABI5 expression by interfering with HY5 binding to the ABI5 promoter. In addition, ABI5 was shown to directly activate its own expression, whereas BBX21 negatively regulates this activity by directly interacting with ABI5. Together, our study indicates that BBX21 coordinates with HY5 and ABI5 on the ABI5 promoter and that these transcriptional regulators work in concert to integrate light and ABA signaling in Arabidopsis thaliana.

          Author Summary

          Many factors such as light, phytohormone abscisic acid (ABA), etc., regulate multiple developmental processes throughout the plants' life cycle. Light promotes seed germination and ABA maintains seed dormancy. However, little is known about how light and ABA signaling pathways interact with each other. It was previously reported that Arabidopsis HY5, a well-known bZIP transcription factor involved in promoting seedling photomorphogenesis, is involved in ABA signaling by directly activating ABI5 expression. Here, we report that the B-box protein BBX21 negatively regulates ABI5 expression by interfering with HY5 binding to the ABI5 promoter. Interestingly, ABI5 was shown to directly bind to its own promoter and activate its expression, whereas BBX21 also negatively regulates this activity by interacting with ABI5. Together, our study shows that light and ABA signaling pathways converge on the ABI5 promoter, on which BBX21 acts as a negative regulator of ABI5 expression.

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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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            The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors.

            The vegetative and reproductive (flowering) phases of Arabidopsis development are clearly separated. The onset of flowering is promoted by long photoperiods, but the constans (co) mutant flowers later than wild type under these conditions. The CO gene was isolated, and two zinc fingers that show a similar spacing of cysteines, but little direct homology, to members of the GATA1 family were identified in the amino acid sequence. co mutations were shown to affect amino acids that are conserved in both fingers. Some transgenic plants containing extra copies of CO flowered earlier than wild type, suggesting that CO activity is limiting on flowering time. Double mutants were constructed containing co and mutations affecting gibberellic acid responses, meristem identity, or phytochrome function, and their phenotypes suggested a model for the role of CO in promoting flowering.
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              The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor.

              The Arabidopsis abscisic acid (ABA)-insensitive abi5 mutants have pleiotropic defects in ABA response, including decreased sensitivity to ABA inhibition of germination and altered expression of some ABA-regulated genes. We isolated the ABI5 gene by using a positional cloning approach and found that it encodes a member of the basic leucine zipper transcription factor family. The previously characterized abi5-1 allele encodes a protein that lacks the DNA binding and dimerization domains required for ABI5 function. Analyses of ABI5 expression provide evidence for ABA regulation, cross-regulation by other ABI genes, and possibly autoregulation. Comparison of seed and ABA-inducible vegetative gene expression in wild-type and abi5-1 plants indicates that ABI5 regulates a subset of late embryogenesis-abundant genes during both developmental stages.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                February 2014
                27 February 2014
                : 10
                : 2
                : e1004197
                Affiliations
                [1 ]Department of Biological and Environmental Sciences, Gothenburg University, Gothenburg, Sweden
                [2 ]Peking-Yale Joint Center for Plant Molecular Genetics and Agro-Biotechnology, State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, Peking University, Beijing, China
                [3 ]State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, China
                [4 ]Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut, United States of America
                Peking University, China
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DX MH. Performed the experiments: DX SNG CH FL MXA YJ. Analyzed the data: JL DX XWD. Wrote the paper: JL DX XWD.

                [¤a]

                Current address: Department of Biotechnology, National Institute of Technology, Durgapur, West Bengal, India.

                [¤b]

                Current address: Department of Chemistry, University of Colombo, Colombo, Sri Lanka.

                Article
                PGENETICS-D-13-02170
                10.1371/journal.pgen.1004197
                3937224
                24586210
                a0c7b109-a398-4e73-9040-95a76d89d606
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 August 2013
                : 8 January 2014
                Page count
                Pages: 11
                Funding
                This work was supported by The Swedish Research Council, the Magnus Bergvalls Foundation, the Royal Physiographic Society in Lund, the Royal Swedish Academy of Agriculture and Forestry, the Adlerbert Research Foundation (to MH), PA Larsson's Foundation (to DX), the Wenner-Gren Foundation (to YJ), the Carl Trygger Foundation (to SNG), and the Olle Engkvist Byggmästare Foundation (MXA and MH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Biology

                Genetics
                Genetics

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