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      Dissecting the Biochemical and Transcriptomic Effects of a Locally Applied Heat Treatment on Developing Cabernet Sauvignon Grape Berries

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          Abstract

          Reproductive development of grapevine and berry composition are both strongly influenced by temperature. To date, the molecular mechanisms involved in grapevine berries response to high temperatures are poorly understood. Unlike recent data that addressed the effects on berry development of elevated temperatures applied at the whole plant level, the present work particularly focuses on the fruit responses triggered by direct exposure to heat treatment (HT). In the context of climate change, this work focusing on temperature effect at the microclimate level is of particular interest as it can help to better understand the consequences of leaf removal (a common viticultural practice) on berry development. HT (+ 8°C) was locally applied to clusters from Cabernet Sauvignon fruiting cuttings at three different developmental stages (middle green, veraison and middle ripening). Samples were collected 1, 7, and 14 days after treatment and used for metabolic and transcriptomic analyses. The results showed dramatic and specific biochemical and transcriptomic changes in heat exposed berries, depending on the developmental stage and the stress duration. When applied at the herbaceous stage, HT delayed the onset of veraison. Heating also strongly altered the berry concentration of amino acids and organic acids (e.g., phenylalanine, γ-aminobutyric acid and malate) and decreased the anthocyanin content at maturity. These physiological alterations could be partly explained by the deep remodeling of transcriptome in heated berries. More than 7000 genes were deregulated in at least one of the nine experimental conditions. The most affected processes belong to the categories “stress responses,” “protein metabolism” and “secondary metabolism,” highlighting the intrinsic capacity of grape berries to perceive HT and to build adaptive responses. Additionally, important changes in processes related to “transport,” “hormone” and “cell wall” might contribute to the postponing of veraison. Finally, opposite effects depending on heating duration were observed for genes encoding enzymes of the general phenylpropanoid pathway, suggesting that the HT-induced decrease in anthocyanin content may result from a combination of transcript abundance and product degradation.

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          Most cited references112

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          How do plants feel the heat?

          In plants, the heat stress response (HSR) is highly conserved and involves multiple pathways, regulatory networks and cellular compartments. At least four putative sensors have recently been proposed to trigger the HSR. They include a plasma membrane channel that initiates an inward calcium flux, a histone sensor in the nucleus, and two unfolded protein sensors in the endoplasmic reticulum and the cytosol. Each of these putative sensors is thought to activate a similar set of HSR genes leading to enhanced thermotolerance, but the relationship between the different pathways and their hierarchical order is unclear. In this review, we explore the possible involvement of different thermosensors in the plant response to warming and heat stress. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.

            Cell-to-cell communication and long-distance signaling play a key role in the response of plants to pests, mechanical wounding, and extreme environmental conditions. Here, we report on a rapid systemic signal in Arabidopsis thaliana that traveled at a rate of 8.4 centimeters per minute and was dependent on the respiratory burst oxidase homolog D (RbohD) gene. Signal propagation was accompanied by the accumulation of reactive oxygen species (ROS) in the extracellular spaces between cells and was inhibited by the suppression of ROS accumulation at locations distant from the initiation site. The rapid systemic signal was triggered by wounding, heat, cold, high-intensity light, and salinity stresses. Our results reveal the profound role that ROS play in mediating rapid, long-distance, cell-to-cell propagating signals in plants.
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              Climate Change and Global Wine Quality

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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                31 January 2017
                2017
                : 8
                : 53
                Affiliations
                [1] 1Centre National de la Recherche Scientifique, Institut des Sciences de la Vigne et du Vin, UMR Ecophysiologie et Génomique Fonctionnelle de la Vigne Villenave d'Ornon, France
                [2] 2Institut National de la Recherche Agronomique (INRA), Institut des Sciences de la Vigne et du Vin, UMR Ecophysiologie et Génomique Fonctionnelle de la Vigne Villenave d'Ornon, France
                [3] 3Université de Bordeaux, Institut des Sciences de la Vigne et du Vin, UMR Ecophysiologie et Génomique Fonctionnelle de la Vigne Villenave d'Ornon, France
                Author notes

                Edited by: José Tomás Matus, Centre for Research in Agricultural Genomics (CRAG), Spain

                Reviewed by: Alessandro Vannozzi, University of Padua, Italy; Claudio Pastenes, University of Chile, Chile

                *Correspondence: David Lecourieux david.lecourieux@ 123456inra.fr

                This article was submitted to Crop Science and Horticulture, a section of the journal Frontiers in Plant Science

                †Present Address: Christian Kappel, Institut für Biochemie und Biologie, Universität Potsdam, Potsdam, Germany;

                Jérémy Pillet, Laboratorio de Bioquímica y Biotecnología Vegetal, Universidad de Málaga, Málaga, Spain

                ‡These authors have contributed equally to this work.

                Article
                10.3389/fpls.2017.00053
                5281624
                28197155
                9e9308b7-72b6-4bf7-9e63-533d780f1601
                Copyright © 2017 Lecourieux, Kappel, Pieri, Charon, Pillet, Hilbert, Renaud, Gomès, Delrot and Lecourieux.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 27 October 2016
                : 10 January 2017
                Page count
                Figures: 6, Tables: 1, Equations: 0, References: 161, Pages: 23, Words: 17682
                Funding
                Funded by: Agence Nationale de la Recherche 10.13039/501100001665
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                grapevine,berry development,microclimate,high temperature,microarrays,metabolomics/metabolite profiling,climate change

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