Alterations in Grapevine Leaf Metabolism Occur Prior to Esca Apoplexy Appearance.

Esca disease is one of the major grapevine trunk diseases in Europe and the etiology is complex, since several inhabiting fungi are identified to be associated with this disease. Among the foliar symptom expressions, the apoplectic form may be distinguished and characterized by sudden dieback of shoots, leaf drop, and shriveling of grape clusters in a few days that can ultimately induce the plant death. To further understand this drastic event, we conducted transcriptomic and metabolomic analyses to characterize responses of leaves during the period preceding symptom appearance (20 and 7 days before foliar symptom expression) and at the day of apoplexy expression. Transcriptomic and metabolomic analyses provide signatures for the apoplectic leaves and most changes concerning the metabolism of carbohydrates, amino acids, and phenylpropanoids. In deciphering glutathione-S-transferase (GST), its preferential location in phloem, correlated with the upregulation of GST genes and a decrease of the glutathione level, offers further support to the putative role of glutathione during apoplexy expression.

[1]  Franco Moritz,et al.  Characterization of poplar metabotypes via mass difference enrichment analysis. , 2017, Plant, cell & environment.

[2]  B. Poinssot,et al.  Metabolic Fingerprint of PS3-Induced Resistance of Grapevine Leaves against Plasmopara viticola Revealed Differences in Elicitor-Triggered Defenses , 2017, Front. Plant Sci..

[3]  E. Abou-Mansour,et al.  Changes in Plant Metabolism and Accumulation of Fungal Metabolites in Response to Esca Proper and Apoplexy Expression in the Whole Grapevine. , 2016, Phytopathology.

[4]  C. Clément,et al.  Pseudomonas fluorescens PTA-CT2 Triggers Local and Systemic Immune Response Against Botrytis cinerea in Grapevine. , 2015, Molecular plant-microbe interactions : MPMI.

[5]  F. Biasioli,et al.  Emission of volatile sesquiterpenes and monoterpenes in grapevine genotypes following Plasmopara viticola inoculation in vitro. , 2015, Journal of mass spectrometry : JMS.

[6]  R. Azevedo,et al.  Sulfur Metabolism and Stress Defense Responses in Plants , 2015, Tropical Plant Biology.

[7]  S. Trouvelot,et al.  Sesquiterpene volatile organic compounds (VOCs) are markers of elicitation by sulfated laminarine in grapevine , 2015, Front. Plant Sci..

[8]  G. Spangenberg,et al.  Flavonoids: a metabolic network mediating plants adaptation to their real estate , 2014, Front. Plant Sci..

[9]  C. Clément,et al.  Osmotic stress-induced polyamine oxidation mediates defence responses and reduces stress-enhanced grapevine susceptibility to Botrytis cinerea. , 2014, Journal of experimental botany.

[10]  Y. Helariutta,et al.  Phloem: the integrative avenue for resource distribution, signaling, and defense , 2013, Front. Plant Sci..

[11]  J. Mérillon,et al.  A faster and a stronger defense response: one of the key elements in grapevine explaining its lower level of susceptibility to Esca? , 2013, Phytopathology.

[12]  C. Plassard,et al.  Promoter-dependent expression of the fungal transporter HcPT1.1 under Pi shortage and its spatial localization in ectomycorrhiza. , 2013, Fungal genetics and biology : FG & B.

[13]  J. Gershenzon,et al.  A Common Fungal Associate of the Spruce Bark Beetle Metabolizes the Stilbene Defenses of Norway Spruce1[C][W][OA] , 2013, Plant Physiology.

[14]  E. Abou-Mansour,et al.  Grapevine trunk diseases: complex and still poorly understood , 2013 .

[15]  Bart Buyck,et al.  What if esca disease of grapevine were not a fungal disease? , 2012, Fungal Diversity.

[16]  A. van Dorsselaer,et al.  Physiological changes in green stems of Vitis vinifera L. cv. Chardonnay in response to esca proper and apoplexy revealed by proteomic and transcriptomic analyses. , 2012, Journal of proteome research.

[17]  F. Rabenoelina,et al.  Leaf stripe form of esca induces alteration of photosynthesis and defence reactions in presymptomatic leaves. , 2011, Functional plant biology : FPB.

[18]  H. Bouwmeester,et al.  Detection of diseased plants by analysis of volatile organic compound emission. , 2011, Annual review of phytopathology.

[19]  N. Hertkorn,et al.  Kendrick-Analogous Network Visualisation of Ion Cyclotron Resonance Fourier Transform Mass Spectra: Improved Options for the Assignment of Elemental Compositions and the Classification of Organic Molecular Complexity , 2011, European journal of mass spectrometry.

[20]  Steven J. M. Jones,et al.  Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen , 2011, Proceedings of the National Academy of Sciences.

[21]  A. M. Gil,et al.  NMR metabolomics of esca disease-affected Vitis vinifera cv. Alvarinho leaves. , 2010, Journal of experimental botany.

[22]  M. Boulay,et al.  Early events prior to visual symptoms in the apoplectic form of grapevine esca disease. , 2010, Phytopathology.

[23]  E. Gomès,et al.  A transcriptomic study of grapevine (Vitis vinifera cv. Cabernet-Sauvignon) interaction with the vascular ascomycete fungus Eutypa lata , 2010, Journal of experimental botany.

[24]  G. Conéjéro,et al.  Expression Analysis in Grapevine by In Situ Hybridization and Immunohistochemistry , 2010 .

[25]  Philippe Schmitt-Kopplin,et al.  The chemodiversity of wines can reveal a metabologeography expression of cooperage oak wood , 2009, Proceedings of the National Academy of Sciences.

[26]  S. Nardi,et al.  Esca in young and mature vineyards, and molecular diagnosis of the associated fungi , 2009, European Journal of Plant Pathology.

[27]  C. Foyer,et al.  Systemic effects on leaf glutathione metabolism and defence protein expression caused by esca infection in grapevines. , 2009, Functional plant biology : FPB.

[28]  G. Bruno,et al.  Effects of three esca-associated fungi on Vitis vinifera L.: IV. Diffusion through the xylem of metabolites produced by two tracheiphilous fungi in the woody tissue of grapevine leads to esca-like symptoms on leaves and berries , 2007 .

[29]  G. Mortier,et al.  qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data , 2007, Genome Biology.

[30]  M. Boulay,et al.  Alteration of photosynthesis in grapevines affected by esca. , 2006, Phytopathology.

[31]  Lalla Aicha Rifai,et al.  Évolution des teneurs en polyamines libres et conjuguées dans les feuilles de vigne (Vitis vinifera 'Cabernet Sauvignon') saine et atteinte d'eutypiose , 2005 .

[32]  T. Fujiwara,et al.  Cloning and characterization of the gene for a phloem-specific glutathione S-transferase from rice leaves. , 2004, Physiologia plantarum.

[33]  A. Bézier,et al.  Study of Defense-related Gene Expression in Grapevine Leaves and Berries Infected with Botrytis cinerea , 2002, European Journal of Plant Pathology.

[34]  E. Kuzniak,et al.  Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. , 2001, Plant science : an international journal of experimental plant biology.

[35]  R. Lamuela-Raventós,et al.  Method for the quantitative extraction of resveratrol and piceid isomers in grape berry skins. Effect of powdery mildew on the stilbene content. , 2001, Journal of agricultural and food chemistry.

[36]  V. Walbot,et al.  AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. , 2000, Plant physiology.

[37]  L. Mugnai,et al.  Esca (Black Measles) and Brown Wood-Streaking: Two Old and Elusive Diseases of Grapevines. , 1999, Plant disease.

[38]  M. Gonneau,et al.  A Nicotiana plumbaginifolia protein labeled with an azido cytokinin agonist is a glutathione S‐transferase , 1998 .

[39]  K. Marrs.  THE FUNCTIONS AND REGULATION OF GLUTATHIONE S-TRANSFERASES IN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[40]  A. Sturm,et al.  Cloning and Characterization of a Glutathione S-Transferase That Can Be Photolabeled with 5-Azido-indole-3-acetic Acid , 1995, Plant physiology.

[41]  U. Steiner,et al.  A glutathione S-transferase with glutathione-peroxidase activity from Arabidopsis thaliana. Molecular cloning and functional characterization. , 1993, European journal of biochemistry.