Analysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening

Mature grapevine berries at the harvesting stage (MB) are very susceptible to the gray mold fungus Botrytis cinerea, while veraison berries (VB) are not. We conducted simultaneous microscopic and transcriptomic analyses of the pathogen and the host to investigate the infection process developed by B...

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Main Authors: Jani Kelloniemi, Sophie Trouvelot, Marie-Claire Héloir, Adeline Simon, Bérengère Dalmais, Patrick Frettinger, Agnès Cimerman, Marc Fermaud, Jean Roudet, Sylvain Baulande, Christophe Bruel, Mathias Choquer, Linhdavanh Couvelard, Mathilde Duthieuw, Alberto Ferrarini, Victor Flors, Pascal Le Pêcheur, Elise Loisel, Guillaume Morgant, Nathalie Poussereau, Jean-Marc Pradier, Christine Rascle, Lucie Trdá, Benoit Poinssot, Muriel Viaud
Format: Article
Language:English
Published: The American Phytopathological Society 2015-11-01
Series:Molecular Plant-Microbe Interactions
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-02-15-0039-R
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author Jani Kelloniemi
Sophie Trouvelot
Marie-Claire Héloir
Adeline Simon
Bérengère Dalmais
Patrick Frettinger
Agnès Cimerman
Marc Fermaud
Jean Roudet
Sylvain Baulande
Christophe Bruel
Mathias Choquer
Linhdavanh Couvelard
Mathilde Duthieuw
Alberto Ferrarini
Victor Flors
Pascal Le Pêcheur
Elise Loisel
Guillaume Morgant
Nathalie Poussereau
Jean-Marc Pradier
Christine Rascle
Lucie Trdá
Benoit Poinssot
Muriel Viaud
author_facet Jani Kelloniemi
Sophie Trouvelot
Marie-Claire Héloir
Adeline Simon
Bérengère Dalmais
Patrick Frettinger
Agnès Cimerman
Marc Fermaud
Jean Roudet
Sylvain Baulande
Christophe Bruel
Mathias Choquer
Linhdavanh Couvelard
Mathilde Duthieuw
Alberto Ferrarini
Victor Flors
Pascal Le Pêcheur
Elise Loisel
Guillaume Morgant
Nathalie Poussereau
Jean-Marc Pradier
Christine Rascle
Lucie Trdá
Benoit Poinssot
Muriel Viaud
author_sort Jani Kelloniemi
collection DOAJ
description Mature grapevine berries at the harvesting stage (MB) are very susceptible to the gray mold fungus Botrytis cinerea, while veraison berries (VB) are not. We conducted simultaneous microscopic and transcriptomic analyses of the pathogen and the host to investigate the infection process developed by B. cinerea on MB versus VB, and the plant defense mechanisms deployed to stop the fungus spreading. On the pathogen side, our genome-wide transcriptomic data revealed that B. cinerea genes upregulated during infection of MB are enriched in functional categories related to necrotrophy, such as degradation of the plant cell wall, proteolysis, membrane transport, reactive oxygen species (ROS) generation, and detoxification. Quantitative-polymerase chain reaction on a set of representative genes related to virulence and microscopic observations further demonstrated that the infection is also initiated on VB but is stopped at the penetration stage. On the plant side, genome-wide transcriptomic analysis and metabolic data revealed a defense pathway switch during berry ripening. In response to B. cinerea inoculation, VB activated a burst of ROS, the salicylate-dependent defense pathway, the synthesis of the resveratrol phytoalexin, and cell-wall strengthening. On the contrary, in infected MB, the jasmonate-dependent pathway was activated, which did not stop the fungal necrotrophic process.
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spelling doaj.art-d3cb77687a764b13a174d734134ca5502022-12-22T03:02:27ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062015-11-0128111167118010.1094/MPMI-02-15-0039-RAnalysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry RipeningJani Kelloniemi0Sophie Trouvelot1Marie-Claire Héloir2Adeline Simon3Bérengère Dalmais4Patrick Frettinger5Agnès Cimerman6Marc Fermaud7Jean Roudet8Sylvain Baulande9Christophe Bruel10Mathias Choquer11Linhdavanh Couvelard12Mathilde Duthieuw13Alberto Ferrarini14Victor Flors15Pascal Le Pêcheur16Elise Loisel17Guillaume Morgant18Nathalie Poussereau19Jean-Marc Pradier20Christine Rascle21Lucie Trdá22Benoit Poinssot23Muriel Viaud24Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes–ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes–ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes–ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes–ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;INRA, UMR 1065 Santé et Agroécologie du Vignoble, 33882 Villenave d’Ornon, France;INRA, UMR 1065 Santé et Agroécologie du Vignoble, 33882 Villenave d’Ornon, France;PartnerChip, 2 rue G. Crémieux, 91000 Evry, France;UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;PartnerChip, 2 rue G. Crémieux, 91000 Evry, France;PartnerChip, 2 rue G. Crémieux, 91000 Evry, France;Università degli Studi di Verona, Dipartimento di Biotecnologie, Strada Le Grazie 15, 37134 Verona, Italy;University of Jaume I, Plant Physiology Section, CAMN, Castellón, 12071, SpainINRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;INRA, UMR 1065 Santé et Agroécologie du Vignoble, 33882 Villenave d’Ornon, France;INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes–ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes–ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;Mature grapevine berries at the harvesting stage (MB) are very susceptible to the gray mold fungus Botrytis cinerea, while veraison berries (VB) are not. We conducted simultaneous microscopic and transcriptomic analyses of the pathogen and the host to investigate the infection process developed by B. cinerea on MB versus VB, and the plant defense mechanisms deployed to stop the fungus spreading. On the pathogen side, our genome-wide transcriptomic data revealed that B. cinerea genes upregulated during infection of MB are enriched in functional categories related to necrotrophy, such as degradation of the plant cell wall, proteolysis, membrane transport, reactive oxygen species (ROS) generation, and detoxification. Quantitative-polymerase chain reaction on a set of representative genes related to virulence and microscopic observations further demonstrated that the infection is also initiated on VB but is stopped at the penetration stage. On the plant side, genome-wide transcriptomic analysis and metabolic data revealed a defense pathway switch during berry ripening. In response to B. cinerea inoculation, VB activated a burst of ROS, the salicylate-dependent defense pathway, the synthesis of the resveratrol phytoalexin, and cell-wall strengthening. On the contrary, in infected MB, the jasmonate-dependent pathway was activated, which did not stop the fungal necrotrophic process.https://apsjournals.apsnet.org/doi/10.1094/MPMI-02-15-0039-R
spellingShingle Jani Kelloniemi
Sophie Trouvelot
Marie-Claire Héloir
Adeline Simon
Bérengère Dalmais
Patrick Frettinger
Agnès Cimerman
Marc Fermaud
Jean Roudet
Sylvain Baulande
Christophe Bruel
Mathias Choquer
Linhdavanh Couvelard
Mathilde Duthieuw
Alberto Ferrarini
Victor Flors
Pascal Le Pêcheur
Elise Loisel
Guillaume Morgant
Nathalie Poussereau
Jean-Marc Pradier
Christine Rascle
Lucie Trdá
Benoit Poinssot
Muriel Viaud
Analysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening
Molecular Plant-Microbe Interactions
title Analysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening
title_full Analysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening
title_fullStr Analysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening
title_full_unstemmed Analysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening
title_short Analysis of the Molecular Dialogue Between Gray Mold (Botrytis cinerea) and Grapevine (Vitis vinifera) Reveals a Clear Shift in Defense Mechanisms During Berry Ripening
title_sort analysis of the molecular dialogue between gray mold botrytis cinerea and grapevine vitis vinifera reveals a clear shift in defense mechanisms during berry ripening
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-02-15-0039-R
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