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. 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.
1 Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes-ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;
Jani
J
Kelloniemi
1 Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes-ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;
Sophie
S
Trouvelot
1 Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes-ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;
Marie-Claire
MC
Héloir
2 INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;
Adeline
A
Simon
2 INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;
Bérengère
B
Dalmais
1 Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes-ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;|3 UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;
Patrick
P
Frettinger
2 INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;
Agnès
A
Cimerman
4 INRA, UMR 1065 Santé et Agroécologie du Vignoble, 33882 Villenave d'Ornon, France;
Marc
M
Fermaud
4 INRA, UMR 1065 Santé et Agroécologie du Vignoble, 33882 Villenave d'Ornon, France;
Jean
J
Roudet
5 PartnerChip, 2 rue G. Crémieux, 91000 Evry, France;
Sylvain
S
Baulande
3 UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;
Christophe
C
Bruel
3 UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;
Mathias
M
Choquer
5 PartnerChip, 2 rue G. Crémieux, 91000 Evry, France;
Linhdavanh
L
Couvelard
5 PartnerChip, 2 rue G. Crémieux, 91000 Evry, France;
Mathilde
M
Duthieuw
6 Università degli Studi di Verona, Dipartimento di Biotecnologie, Strada Le Grazie 15, 37134 Verona, Italy;
Alberto
A
Ferrarini
7 University of Jaume I, Plant Physiology Section, CAMN, Castellón, 12071, Spain.
Victor
V
Flors
2 INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;
Pascal
P
Le Pêcheur
4 INRA, UMR 1065 Santé et Agroécologie du Vignoble, 33882 Villenave d'Ornon, France;
Elise
E
Loisel
2 INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;
Guillaume
G
Morgant
3 UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;
Nathalie
N
Poussereau
2 INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;
Jean-Marc
JM
Pradier
3 UMR 5240 MAP, Université Lyon 1-CNRS-Bayer CropScience, Villeurbanne, France;
Christine
C
Rascle
1 Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes-ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;
Lucie
L
Trdá
1 Université de Bourgogne, UMR 1347 Agroécologie, Pôle Interactions Plantes Micro-organismes-ERL CNRS 6300, 17 rue Sully, 21000 Dijon, France;
Benoit
B
Poinssot
2 INRA, UMR 1290 BIOGER, Avenue Lucien Brétignières, 78850 Grignon, France;
Muriel
M
Viaud
D020171:Botrytis / Q000235:genetics* / Q000472:pathogenicity; D002473:Cell Wall / Q000235:genetics / Q000378:metabolism / Q000382:microbiology; D003517:Cyclopentanes / Q000378:metabolism; D060467:Disease Resistance / Q000235:genetics*; D005638:Fruit / Q000235:genetics* / Q000254:growth & development / Q000382:microbiology; D020869:Gene Expression Profiling / Q000379:methods; D018507:Gene Expression Regulation, Developmental; D015966:Gene Expression Regulation, Fungal; D018506:Gene Expression Regulation, Plant; D063990:Gene Ontology; D054884:Host-Pathogen Interactions / Q000235:genetics; D020411:Oligonucleotide Array Sequence Analysis; D054883:Oxylipins / Q000378:metabolism; D010935:Plant Diseases / Q000235:genetics* / Q000382:microbiology; D017382:Reactive Oxygen Species / Q000378:metabolism; D000077185:Resveratrol; D020133:Reverse Transcriptase Polymerase Chain Reaction; D012459:Salicylates / Q000378:metabolism; D012717:Sesquiterpenes / Q000378:metabolism; D013267:Stilbenes / Q000378:metabolism; D014774:Virulence / Q000235:genetics; D027843:Vitis / Q000235:genetics* / Q000254:growth & development / Q000382:microbiology; D000094162:Phytoalexins
D003517:Cyclopentanes; D054883:Oxylipins; D017382:Reactive Oxygen Species; D012459:Salicylates; D012717:Sesquiterpenes; D013267:Stilbenes; C011006:jasmonic acid; D000077185:Resveratrol; D000094162:Phytoalexins