Abstract
Development and optimisation of alternative strategies to reduce the use of classic chemical inputs for protection against diseases in vineyard is becoming a necessity. Among these strategies, one of the most promising consists in the stimulation and/or potentiation of the grapevine defence responses by the means of elicitors. Elicitors are highly diverse molecules both in nature and origins. This review aims at providing an overview of the current knowledge on these molecules and will highlight their potential efficacy from the laboratory in controlled conditions to vineyards. Recent findings and concepts (especially on plant innate immunity) and the new terminology (microbe-associated molecular patterns, effectors, etc.) are also discussed in this context. Other objectives of this review are to highlight the difficulty of transferring elicitors use and results from the controlled conditions to the vineyard, to determine their practical and effective use in viticulture and to propose ideas for improving their efficacy in non-controlled conditions.
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References
Adrian M, Trouvelot S, Gamm M, Poinssot B, Héloir M-C, Daire X (2012) Activation of grapevine defense mechanisms: theoretical and applied approaches. In: Mérillon JM, Ramawat Kishan G (eds) Plant defence: biological control. Springer, Dordrecht, pp 313–331
Allegre M, Héloir M-C, Trouvelot S, Daire X, Pugin A, Wendehenne D, Adrian M (2009) Are grapevine stomata involved in the elicitor-induced protection against downy mildew? Mol Plant-Microbe Interact 22:977–986
Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543
Aveline N (2010) Solutions alternatives : le point en 2009. Cahier d'actualité de l'Institut Français de la Vigne et du Vin. Institut Français de la Vigne et du Vin, Bordeaux, pp 4–7
Aveline N, Riffard A, Tite A, Lejealle S, Cluzet S, Corio-Costet M-F (2011) Evaluation d'un outil innovant pour étudier la stimulation des défenses de la vigne au vignoble, 4ème Conférence Internationale sur les Méthodes Alternatives en Protection des Cultures. Association Française de Protection des Plantes, Lille, pp 394–401
Aziz A, Poinssot B, Daire X, Adrian M, Bezier A, Lambert B, Joubert J-M, Pugin A (2003) Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol Plant-Microbe Interact 16:1118–1128
Aziz A, Heyraud A, Lambert B (2004) Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 218:767–774
Aziz A, Trotel-Aziz P, Dhuicq L, Jeandet P, Couderchet M, Vernet G (2006) Chitosan oligomers and copper sulfate induce grapevine defense reactions and resistance to gray mold and downy mildew. Phytopathology 96:1188–1194
Aziz A, Gauthier A, Bézier A, Poinssot B, Joubert J-M, Pugin A, Heyraud A, Baillieul F (2007) Elicitor and resistance-inducing activities of β-1,4 cellodextrins in grapevine, comparison with β-1,3 glucans and β-1,4 oligogalacturonides. J Exp Bot 58:1463–1472
Beckers GJM, Conrath U (2007) Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol 10:425–431
Belchi-Navarro S, Almagro L, Lijavetzky D, Bru R, Pedreno MA (2012) Enhanced extracellular production of trans-resveratrol in Vitis vinifera suspension cultured cells by using cyclodextrins and methyl jasmonate. Plant Cell Rep 31:81–89
Belchi-Navarro S, Almagro L, Sabater-Jara AB, Fernandez-Perez F, Bru R, Pedreno MA (2013) Early signaling events in grapevine cells elicited with cyclodextrins and methyl jasmonate. Plant Physiol Biochem 62:107–110
Belhadj A, Saigne C, Telef N, Cluzet S, Bouscaut J, Corio-Costet MF, Mérillon JM (2006) Methyl jasmonate induces defense responses in grapevine and triggers protection against Erysiphe necator. J Agric Food Chem 54:9119–9125
Belhadj A, Telef N, Cluzet S, Bouscaut J, Corio-Costet M-F, Mérillon J-M (2008) Ethephon elicits protection against Erysiphe necator in grapevine. J Agric Food Chem 56:5781–5787
Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406
Bony S, Gillet C, Bouchez A, Margoum C, Devaux A (2008) Genotoxic pressure of vineyard pesticides in fish: field and mesocosm surveys. Aquat Toxicol 89:197–203
Bru R, Selles S, Belchi-Navarro S, Pedreno MA (2006) Modified cyclodextrins are chemically defined glucan inducers of defense responses in grapevine cell cultures. J Agric Food Chem 54:65–71
Busam G, Junghanns KT, Kneusel RE, Kassemeyer HH, Matern U (1997a) Characterization and expression of caffeoyl-coenzyme A 3-O-methyltransferase proposed for the induced resistance response of Vitis vinifera L. Plant Physiol 115:1039–1048
Busam G, Kassemeyer HH, Matern U (1997b) Differential expression of chitinases in Vitis vinifera L. responding to systemic acquired resistance activators or fungal challenge. Plant Physiol 115:1029–1038
Caillot S, Rat S, Tavernier M-L, Michaud P, Kovensky J, Wadouachi A, Clément C, Baillieul F, Petit E (2012) Native and sulfated oligoglucuronans as elicitors of defence-related responses inducing protection against Botrytis cinerea of Vitis vinifera. Carbohydr Polym 87:1728–1736
Cesnik HB, Gregorcic A, Cus F (2008) Pesticide residues in grapes from vineyards included in integrated pest management in Slovenia. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25(4):438–443
Chang X, Nick P (2012) Defence signalling triggered by Flg22 and harpin is integrated into a different stilbene output in Vitis cells. PLoS One 7(7):e40446
Chang X, Heene E, Qiao F, Nick P (2011) The phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cell. PLoS One 6(10):e26405
Cohen Y, Reuveni M, Baider A (1999) Local and systemic activity of BABA (DL-3-aminobutyric acid) against Plasmopara viticola in grapevines. Eur J Plant Pathol 105:351–361
Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959
Compant S, Nowak J, Coenye T, Clément C, Ait Barka E (2008) Diversity and occurrence of Burkholderia spp. in the natural environment. FEMS Microbiol Rev 32:607–626
Conrath U (2009) Priming of induced plant defense responses. In: Loon LCV (ed) Advances in botanical research. Academic, Burlington, pp 361–395
Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531
Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19:1062
Corio-Costet M-F, Dufour M-C, Cigna J, Abadie P, Chen W-J (2011) Diversity and fitness of Plasmopara viticola isolates resistant to QoI fungicides. Eur J Plant Pathol 129:315–329
Dagostin S, Schärer H-J, Pertot I, Tamm L (2011) Are there alternatives to copper for controlling grapevine downy mildew in organic viticulture? Crop Protect 30:776–788
Daire X, Jacob S, Crozier P (2008) Evaluation de méthodes de lutte complémentaire de la lutte fongicide contre les maladies de la vigne, Matinée Technique du BIVB : « Réduction des intrants et alternatives à la lutte chimique : les enjeux de la viticulture de demain ». Bureau Interprofessionnel des Vins de Bourgogne, Beaune, pp 7–20
Delaunois B, Cordelier S, Conreux A, Clément C, Jeandet P (2009) Molecular engineering of resveratrol in plants. Plant Biotechnol J 7:2–12
Derckel JP, Legendre L, Audran J, Haye B, Lambert B (1996) Chitinases of the grapevine (Vitis vinifera L): five isoforms induced in leaves by salicylic acid are constitutively expressed in other tissues. Plant Sci 119:31–37
Derckel J-P, Audran J-C, Haye B, Lambert B, Legendre L (1998) Characterization, induction by wounding and salicylic acid, and activity against Botrytis cinerea of chitinases and β-1,3-glucanases of ripening grape berries. Physiol Plant 104:56–64
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548
Dufour MC, Fontaine S, Montarry J, Corio-Costet MF (2011) Assessment of fungicide resistance and pathogen diversity in Erysiphe necator using quantitative real-time PCR assays. Pest Manag Sci 67:60–69
Dufour M, Lambert C, Bouscaut J, Mérillon J, Corio-Costet M (2013) Benzothiadiazole-primed defence responses and enhanced differential expression of defence genes in Vitis vinifera infected with biotrophic pathogens Erysiphe necator and Plasmopara viticola. Plant Pathol 62:370–382
Elmer PAG, Reglinski T (2006) Biosuppression of Botrytis cinerea in grapes. Plant Pathol 55:155–177
Ferreira RB, Monteiro SS, Piçarra-Pereira MA, Teixeira AR (2004) Engineering grapevine for increased resistance to fungal pathogens without compromising wine stability. Trends Biotechnol 22:168–173
Flamini R, De Rosso M (2006) Mass spectrometry in the analysis of grape and wine proteins. Expert Rev Proteomics 3:321–331
Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant-Microbe Interact 19:711
González Álvarez M, Noguerol-Pato R, González-Barreiro C, Cancho-Grande B, Simal-Gándara J (2012) Changes of the sensorial attributes of white wines with the application of new anti-mildew fungicides under critical agricultural practices. Food Chem 130:139–146
Hamiduzzaman MM, Jakab G, Barnavon L, Neuhaus J-M, Mauch-Mani B (2005) β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol Plant-Microbe Interact 18:819–829
Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791
Harm A, Kassemeyer H-H, Seibicke T, Regner F (2011) Evaluation of chemical and natural resistance inducers against downy mildew (Plasmopara viticola) in grapevine. Am J Enol Vitic 62:184–192
Iriti M, Rossoni M, Borgo M, Faoro F (2004) Benzothiadiazole enhances resveratrol and anthocyanin biosynthesis in grapevine, meanwhile improving resistance to Botrytis cinerea. J Agric Food Chem 52:4406–4413
Iriti M, Rossoni M, Borgo M, Ferrara L, Faoro F (2005) Induction of resistance to gray mold with benzothiadiazole modifies amino acid profile and increases proanthocyanidins in grape: primary versus secondary metabolism. J Agric Food Chem 53:9133–9139
Jacobs D, Robinson (1999) Induction of different pathogenesis-related cDNAs in grapevine infected with powdery mildew and treated with ethephon. Plant Pathol 48:325–336
Jermini M, Blaise P, Gessler C (2010) Quantitative effect of leaf damage caused by downy mildew (Plasmopara viticola) on growth and yield quality of grapevine ‘Merlot’ (Vitis vinifera). Vitis 49:77–85
Klarzynski O, Fritig B (2001) Stimulation of plant natural defenses. C R Acad Sci III 324:953–963
Komarek M, Cadkova E, Chrastny V, Bordas F, Bollinger JC (2010) Contamination of vineyard soils with fungicides: a review of environmental and toxicological aspects. Environ Int 36:138–151
Krisa S, Larronde F, Budzinski H, Decendit A, Deffieux G, Mérillon J-M (1999) Stilbene production by Vitis vinifera cell suspension cultures: methyl jasmonate induction and 13C biolabeling. J Nat Prod 62:1688–1690
Laquitaine L, Gomes E, Francois J, Marchive C, Pascal S, Hamdi S, Atanassova R, Delrot S, Coutos-Thevenot P (2006) Molecular basis of ergosterol-induced protection of grape against Botrytis cinerea: induction of type I LTP promoter activity, WRKY, and stilbene synthase gene expression. Mol Plant-Microbe Interact 19:1103–1112
Lisidowati F, Melchior F, Hohmann F, Schwer B, Kindl H (1991) Induction of stilbene synthase by Botrytis cinerea in cultured grapevine cells. Planta 183:307–314
Loulakakis KA (1997) Genomic organization and expression of an osmotin-like gene in Vitis vinifera L. Vitis 36:157–158
Malet JC (2011) Les enjeux de l'expérimentation dans le cadre de la mise en oeuvre de moyens de lutte alternatifs, 4ème Conférence Internationale sur les Méthodes Alternatives en Protection des Cultures. Association Française de Protection des Plantes, Lille, pp 44–48
Martinez-Esteso MJ, Sellés-Marchart S, Vera-Urbina JC, Pedreño MA, Bru-Martinez R (2009) Changes of defense proteins in the extracellular proteome of grapevine (Vitis vinifera cv. Gamay) cell cultures in response to elicitors. J Proteomics 73:331–341
Martinez-Esteso MJ, Selles-Marchart S, Vera-Urbina JC, Pedreno MA, Bru-Martinez R (2011) DIGE analysis of proteome changes accompanying large resveratrol production by grapevine (Vitis vinifera cv. Gamay) cell cultures in response to methyl-beta-cyclodextrin and methyl jasmonate elicitors. J proteomics 74:1421–1436
Milanovic V, Comitini F, Ciani M (2013) Grape berry yeast communities: influence of fungicide treatments. Int J Food Microbiol 161:240–246
Mohamed N, Lherminier J, Farmer MJ, Fromentin J, Béno N, Houot V, Milat ML, Blein JP (2007) Defense responses in grapevine leaves against Botrytis cinerea induced by application of a Pythium oligandrum strain or its elicitin, oligandrin, to roots. Phytopathology 97:611
Molot B (2007) Solutions alternatives : qu'en attendre ? Euroviti, Montpellier, pp 113–116
Palmieri MC, Perazzolli M, Matafora V, Moretto M, Bachi A, Pertot I (2012) Proteomic analysis of grapevine resistance induced by Trichoderma harzianum T39 reveals specific defence pathways activated against downy mildew. J Exp Bot 63:6237–6251
Panigai L, Grosman J, Coconier Y, Vincent G (2011) Techniques de production intégrée présumées à faible risque utilisables en viticulture, 4ème Conférence Internationale sur les Méthodes Alternatives en Protection des Cultures. Association Française de Protection des Plantes, Lille, pp 806–815
Perazzolli M, Dagostin S, Ferrari A, Elad Y, Pertot I (2008) Induction of systemic resistance against Plasmopara viticola in grapevine by Trichoderma harzianum T39 and benzothiadiazole. Biol Control 47:228–234
Perazzolli M, Roatti B, Bozza E, Pertot I (2011) Trichoderma harzianum T39 induces resistance against downy mildew by priming for defense without costs for grapevine. Biol Control 58:74–82
Perez-Garcia A, Romero D, de Vicente A (2011) Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr Opin Biotechnol 22:187–193
Petit A-N, Wojnarowiez G, Panon M-L, Baillieul F, Clément C, Fontaine F, Vaillant-Gaveau N (2009) Botryticides affect grapevine leaf photosynthesis without inducing defense mechanisms. Planta 229:497–506
Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316
Pinto KM, Cordeiro do Nascimento L, Cintra de Souza Gomes E, Florêncio da Silva H, Janaina dos Reis M (2012) Efficiency of resistance elicitors in the management of grapevine downy mildew Plasmopara viticola: epidemiological, biochemical and economic aspects. Eur J Plant Pathol 134:745–754
Poinssot B, Vandelle E, Bentéjac M, Adrian M, Levis C, Brygoo Y, Garin J, Sicilia F, Coutos-Thévenot P, Pugin A (2003) The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant-Microbe Interact 16:553–564
Polesani M, Bortesi L, Ferrarini A, Zamboni A, Fasoli M, Zadra C, Lovato A, Pezzotti M, Delledonne M, Polverari A (2010) General and species-specific transcriptional responses to downy mildew infection in a susceptible (Vitis vinifera) and a resistant (V. riparia) grapevine species. BMC Genomics 11:117
Qiao F, Chang XL, Nick P (2010) The cytoskeleton enhances gene expression in the response to the harpin elicitor in grapevine. J Exp Bot 61:4021–4031
Renault AS, Deloire A, Bierne J (1996) Pathogenesis-related proteins in grapevines induced by salicylic acid and Botrytis cinerea. Vitis 35:49–52
Repka V (2001) Elicitor-stimulated induction of defense mechanisms and defense gene activation in grapevine cell suspension cultures. Biol Plant 44:555–565
Repka V (2006) Early defence responses induced by two distinct elicitors derived from a Botrytis cinerea in grapevine leaves and cell suspensions. Biol Plant 50:94–106
Repka V, Fischerova I, Silharova K (2004) Methyl jasmonate is potent elicitor of multiple defense responses in grapevine leaves and cell-suspension cultures. Biol Plant 48:273–283
Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343
Sanchez L, Courteaux B, Hubert J, Kauffmann S, Renault JH, Clement C, Baillieul F, Dorey S (2012) Rhamnolipids elicit defense responses and induce disease resistance against biotrophic, hemibiotrophic, and necrotrophic pathogens that require different signaling pathways in Arabidopsis and highlight a central role for salicylic acid. Plant Physiol 160:1630–1641
Schreck E, Gontier L, Dumat C, Geret F (2012) Ecological and physiological effects of soil management practices on earthworm communities in French vineyards. Eur J Soil Biol 52:8–15
Slaughter A, Hamiduzzaman M, Gindro K, Neuhaus J-M, Mauch-Mani B (2008) β-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. Eur J Plant Pathol 122:185–195
Tassoni A, Fornalè S, Franceschetti M, Musiani F, Michael AJ, Perry B, Bagni N (2005) Jasmonates and Na-orthovanadate promote resveratrol production in Vitis vinifera cv Barbera cell cultures. New Phytol 166:895–905
Toffolatti SL, Venturini G, Maffi D, Vercesi A (2012) Phenotypic and histochemical traits of the interaction between Plasmopara viticola and resistant or susceptible grapevine varieties. BMC Plant Biol 12:124
Trotel-Aziz P, Couderchet M, Vernet G, Aziz A (2006) Chitosan stimulates defense reactions in grapevine leaves and inhibits development of Botrytis cinerea. Eur J Plant Pathol 114:405–413
Trouvelot S, Varnier AL, Allègre M, Mercier L, Baillieul F, Arnould C, Gianinazzi-Pearson V, Klarzynski O, Joubert JM, Pugin A, Daire X (2008) A β-1,3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Mol Plant-Microbe Interact 21:232–243
Tsakirakis A, Tsatsakis A, Tsakalof A, Kasiotis K, Machera K, Charistou A (2012) Operator exposure during fungicide applications in vineyards. Toxicol Lett 211(Supplement):S174
Vandelle E, Poinssot B, Wendehenne D, Bentéjac M, Pugin A (2006) Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Mol Plant-Microbe Interact 19:429–440
Varnier AL, Sanchez L, Vatsa P, Boudesocque L, Garcia-Brugger A, Rabenoelina F, Sorokin A, Renault JH, Kauffmann S, Pugin A, Clement C, Baillieul F, Dorey S (2009) Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. Plant Cell Environ 32:178–193
Vatsa P, Sanchez L, Clément C, Baillieul F, Dorey S (2010) Rhamnolipid biosurfactants as new players in animal and plant defense against microbes. Int J Mol Sci 11:5095–5108
Vezzulli S, Civardi S, Ferrari F, Bavaresco L (2007) Methyl jasmonate treatment as a trigger of resveratrol synthesis in cultivated grapevine. Am J Enol Vitic 58:530–533
Vidal J, Gomez C, Cutanda M, Shresth B, Bouquet A, Thomas M, Torregrosa L (2010) Use of gene transfer technology for functional studies in grapevine. Aust J Grape Wine R 16:138–151
Acknowledgments
Bertrand Delaunois PhD thesis was supported through the project VINEAL2 by the ‘Region Champagne Ardenne’ and by ‘Comité Champagne’ (Epernay, France). Giovanni Farace post-doctoral position was funded by the INTERREG IV program France-Wallonie-Vlaanderen (Phytobio project). We are grateful to Institut Français de la Vigne et du Vin (Bordeaux, France) and to Bureau Interprofessionnel des Vins de Bourgogne (Beaune, France) for experimental data on fogging station and vineyard trials, respectively.
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Responsible editor: Philippe Garrigues
Bertrand Delaunois, Giovanni Farace, Stéphan Dorey and Sylvain Cordelier contributed equally to the work.
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Delaunois, B., Farace, G., Jeandet, P. et al. Elicitors as alternative strategy to pesticides in grapevine? Current knowledge on their mode of action from controlled conditions to vineyard. Environ Sci Pollut Res 21, 4837–4846 (2014). https://doi.org/10.1007/s11356-013-1841-4
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DOI: https://doi.org/10.1007/s11356-013-1841-4
Keywords
- Elicitor
- MAMP
- Plant innate immunity
- Induced resistance
- Grapevine
- Plant pathogens