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      Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids

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          Abstract

          The notion that plants use specialized metabolism to protect against environmental stresses needs to be experimentally proven by addressing the question of whether stress tolerance by specialized metabolism is directly due to metabolites such as flavonoids. We report that flavonoids with radical scavenging activity mitigate against oxidative and drought stress in Arabidopsis thaliana. Metabolome and transcriptome profiling and experiments with oxidative and drought stress in wild-type, single overexpressors of MYB12/PFG1 (PRODUCTION OF FLAVONOL GLYCOSIDES1) or MYB75/PAP1 (PRODUCTION OF ANTHOCYANIN PIGMENT1), double overexpressors of MYB12 and PAP1, transparent testa4 ( tt4) as a flavonoid-deficient mutant, and flavonoid-deficient MYB12 or PAP1 overexpressing lines (obtained by crossing tt4 and the individual MYB overexpressor) demonstrated that flavonoid overaccumulation was key to enhanced tolerance to such stresses. Antioxidative activity assays using 2,2-diphenyl-1-picrylhydrazyl, methyl viologen, and 3,3′-diaminobenzidine clearly showed that anthocyanin overaccumulation with strong in vitro antioxidative activity mitigated the accumulation of reactive oxygen species in vivo under oxidative and drought stress. These data confirm the usefulness of flavonoids for enhancing both biotic and abiotic stress tolerance in crops.

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          Most cited references66

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          Gene Expression Omnibus: NCBI gene expression and hybridization array data repository.

          R. Edgar (2002)
          The Gene Expression Omnibus (GEO) project was initiated in response to the growing demand for a public repository for high-throughput gene expression data. GEO provides a flexible and open design that facilitates submission, storage and retrieval of heterogeneous data sets from high-throughput gene expression and genomic hybridization experiments. GEO is not intended to replace in house gene expression databases that benefit from coherent data sets, and which are constructed to facilitate a particular analytic method, but rather complement these by acting as a tertiary, central data distribution hub. The three central data entities of GEO are platforms, samples and series, and were designed with gene expression and genomic hybridization experiments in mind. A platform is, essentially, a list of probes that define what set of molecules may be detected. A sample describes the set of molecules that are being probed and references a single platform used to generate its molecular abundance data. A series organizes samples into the meaningful data sets which make up an experiment. The GEO repository is publicly accessible through the World Wide Web at http://www.ncbi.nlm.nih.gov/geo.
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            MYB transcription factors in Arabidopsis.

            The MYB family of proteins is large, functionally diverse and represented in all eukaryotes. Most MYB proteins function as transcription factors with varying numbers of MYB domain repeats conferring their ability to bind DNA. In plants, the MYB family has selectively expanded, particularly through the large family of R2R3-MYB. Members of this family function in a variety of plant-specific processes, as evidenced by their extensive functional characterization in Arabidopsis (Arabidopsis thaliana). MYB proteins are key factors in regulatory networks controlling development, metabolism and responses to biotic and abiotic stresses. The elucidation of MYB protein function and regulation that is possible in Arabidopsis will provide the foundation for predicting the contributions of MYB proteins to the biology of plants in general. Copyright © 2010 Elsevier Ltd. All rights reserved.
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              Flavonoids as antioxidants in plants: location and functional significance.

              Stress-responsive dihydroxy B-ring-substituted flavonoids have great potential to inhibit the generation of reactive oxygen species (ROS) and reduce the levels of ROS once they are formed, i.e., to perform antioxidant functions. These flavonoids are located within or in the proximity of centers of ROS generation in severely stressed plants. Efficient mechanisms have been recently identified for the transport of flavonoids from the endoplasmic reticulum, the site of their biosynthesis, to different cellular compartments. The mechanism underlying flavonoid-mediated ROS reduction in plants is still unclear. 'Antioxidant' flavonoids are found in the chloroplast, which suggests a role as scavengers of singlet oxygen and stabilizers of the chloroplast outer envelope membrane. Dihydroxy B-ring substituted flavonoids are present in the nucleus of mesophyll cells and may inhibit ROS-generation making complexes with Fe and Cu ions. The genes that govern the biosynthesis of antioxidant flavonoids are present in liverworts and mosses and are mostly up-regulated as a consequence of severe stress. This suggests that the antioxidant flavonoid metabolism is a robust trait of terrestrial plants. Vacuolar dihydroxy B-ring flavonoids have been reported to serve as co-substrates for vacuolar peroxidases to reduce H(2)O(2) escape from the chloroplast, following the depletion of ascorbate peroxidase activity. Antioxidant flavonoids may effectively control key steps of cell growth and differentiation, thus acting regulating the development of the whole plant and individual organs. Copyright © 2012 Elsevier Ireland Ltd. All rights reserved.
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                Author and article information

                Journal
                Plant J
                Plant J
                tpj
                The Plant Journal
                BlackWell Publishing Ltd (Oxford, UK )
                0960-7412
                1365-313X
                February 2014
                02 December 2013
                : 77
                : 3
                : 367-379
                Affiliations
                [1 ]RIKEN Center for Sustainable Resource Science 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, 230-0045, Japan
                [2 ]Graduate School of Pharmaceutical Sciences, Chiba University 1-8-1 Chuo-ku, Chiba, 260-8675, Japan
                [3 ]CREST, Japan Science and Technology Agency 4-1-8 Honcho, Kawaguchi, Saitama, 332-0012, Japan
                [4 ]Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science 3-1-1 Koyadai, Tsukuba, Ibaraki, 305-0074, Japan
                [5 ]Department of Pharmacology, University of Texas Southwestern Medical Center Dallas, TX, 75390, USA
                Author notes
                †Graduate School of Information Science and Technology, Osaka University 1-5 Yamadaoka, Suita, Osaka, 565-0871, Japan
                ‡Max-Planck Institute for Molecular Plant Physiology 14476, Potsdam, Germany
                Article
                10.1111/tpj.12388
                4282528
                24274116
                b9fa53d1-0b8b-4809-9fbe-9e4a8480cb72
                © 2013 The Authors. The Plant Journal © 2013 John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

                History
                : 17 May 2013
                : 11 November 2013
                : 20 November 2013
                Categories
                Original Articles

                Plant science & Botany
                metabolomics,transcriptomics,stress tolerance,flavonols,anthocyanins
                Plant science & Botany
                metabolomics, transcriptomics, stress tolerance, flavonols, anthocyanins

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