Abstract
An extract from Botrytis cinerea culture filtrate was sprayed on grapevine plants (Vitis vinifera) to investigate its potential to stimulate defense reactions. The extract triggered the induction of genes encoding pathogenesis-related (PR) proteins as chitinases (CHIT), polygalacturonase-inhibiting protein (PGIP), serine proteinase inhibitor (PIN), and enzymes involved in phytoalexin synthesis as phenylalanine ammonia-lyase (PAL) and stilbene synthase (STS). Correlated to the up-regulation of these latter genes, stilbene content increased in treated leaves. Consequently, treatment of grapevine leaves with the fungal extract triggered protection toward Plasmopara viticola and Erysiphe necator, the causal agents of grapevine downy and powdery mildews, respectively. Disease severity was significantly reduced in elicited plants, approximately 61 % for downy mildew and 83 % for powdery mildew. This approach could represent a valuable strategy to protect grapevine from diseases as an alternative or complementary method to the use of pesticides.
Abbreviations
- Bc:
-
Botrytis cinerea
- BTH:
-
Benzothiadiazole
- CHIT:
-
Chitinase
- Ct:
-
Cycle threshold
- DP:
-
Degree of polymerization
- DW:
-
Dry weight
- HPLC:
-
High-performance liquid chromatography
- INA:
-
2,6-Dichloroisonicotinic acid
- MS:
-
Mass spectrometry
- NMR:
-
Nuclear magnetic resonance
- OGs:
-
Oligogalacturonides
- PAL:
-
Phenylalanine ammonia-lyase
- PG:
-
Endopolygalacturonase
- PGIP:
-
Polygalacturonase-inhibiting protein
- PIN:
-
Serine proteinase inhibitor
- PR:
-
Pathogenesis-related
- RT-qPCR:
-
Reverse transcription quantitative polymerase chain reaction
- SA:
-
Salicylic acid
- STS:
-
Stilbene synthase
- TFA:
-
Trifluoroacetic acid
References
Adrian M, Jeandet P, Bessis R, Joubert JM (1996) Induction of phytoalexin (resveratrol) synthesis in grapevine leaves treated with aluminum chloride (AlCl3). J Agric Food Chem 44:1979–1981
Adrian M, Jeandet P, Veneau J, Weston LA, Bessis R (1997) Biological activity of resveratrol, a stilbenic compound from grapevines, against Botrytis cinerea, the causal agent for gray mold. J Chem Ecol 23:1689–1702
Akagi A, Engelberth J, Stotz HU (2010) Interaction between polygalacturonase-inhibiting protein and jasmonic acid during defense activation in tomato against Botrytis cinerea. Eur J Plant Pathol 128:423–428
Arrieta-Montiel M, Lyznik A, Woloszynska M, Janska H, Tohme J, Mackenzie S (2001) Tracing evolutionary and developmental implications of mitochondrial stoichiometric shifting in the common bean. Genetics 158:851–864
Aziz A, Poinssot B, Daire X, Adrian M, Bézier A, Lambert B, Joubert JM, 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, 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 JM, 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 α-1,4 oligogalacturonides. J Exp Bot 58:1463–1472
Bavaresco L, Mattivi F, de Rosso M, Flamini R (2012) Effects of elicitors, viticultural factors, and enological practices on resveratrol and stilbenes in Grapevine and Wine. Mini-Rev Med Chem 12:1366–1381
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 MF, Mérillon JM (2008a) Ethephon elicits protection against Erysiphe necator in grapevine. J Agric Food Chem 56:5781–5787
Belhadj A, Telef N, Saigne C, Cluzet S, Barrieu F, Hamdi S, Mérillon JM (2008b) Effect of methyl jasmonate in combination with carbohydrates on gene expression of PR proteins, stilbene and anthocyanin accumulation in grapevine cell cultures. Plant Physiol Biochem 46:493–499
Benhamou N, Nicole M (1999) Cell biology of plant immunization against microbial infection: the potential of induced resistance in controlling plant diseases. Plant Physiol Biochem 37:703–719
Bézier A, Lambert B, Baillieul F (2002) Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea. Eur J Plant Pathol 108:111–120
Bock CH, Brenneman TB, Hotchkiss MW, Wood BW (2012) Evaluation of a phosphite fungicide to control pecan scab in the southeastern USA. Crop Prot 36:58–64
Borie B, Jeandet P, Parize A, Bessis R, Adrian M (2004) Resveratrol and stilbene synthase mRNA production in grapevine leaves treated with biotic and abiotic phytoalexin elicitors. Am J Enol Vitic 55:60–64
Bouarab K, Potin P, Correa J, Kloareg B (1999) Sulfated oligosaccharides mediate the interaction between a marine red alga and its green algal pathogenic endophyte. Plant Cell 11:1635–1650
Brunner F, Stintzi A, Fritig B, Legrand M (1998) Substrate specificities of tobacco chitinases. Plant J 14:225–234
Busam G, Kassemeyer HH, Matern U (1997) Differential expression of chitinases in Vitis vinifera L. Responding to systemic acquired resistance activators or fungal challenge. Plant Physiol 115:1029–1038
Caprari C, Mattei B, Basile ML, Salvi G, Crescenzi V, De Lorenzo G, Cervone F (1996) Mutagenesis of endopolygalacturonase from Fusarium moniliforme: histidine residue 234 is critical for enzymatic and macerating activities and not for binding to polygalacturonase-inhibiting protein (PGIP). Mol Plant Microbe Interact 9:617–624
Cardinale F, Jonak C, Ligterink W, Niehaus K, Boller T, Hirt H (2000) Differential activation of four specific MAPK pathways by distinct elicitors. J Biol Chem 275:36734–36740
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116
Chen PJ, Senthilkumar R, Jane WN, He Y, Tian Z, Yeh KW (2014) Transplastomic Nicotiana benthamiana plants expressing multiple defence genes encoding protease inhibitors and chitinase display broad-spectrum resistance against insects, pathogens and abiotic stresses. Plant Biotechnol J 12:503–515
Cluzet S, Torregrosa C, Jacquet C, Lafitte C, Fournier J, Mercier L, Salamagne S, Briand X, Esquerré-Tugayé MT, Dumas B (2004) Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva spp. Plant Cell Environ 27:917–928
Colas S, Afoufa-Bastien D, Jacquens L, Clément C, Baillieul F, Mazeyrat-Gourbeyre F, Monti-Dedieu L (2012) Expression and in situ localization of two major PR proteins of grapevine berries during development and after UV-C exposition. PLoS One. doi:10.1371/journal.pone.0043681
Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3:31–40
Corio-Costet MF (2012) Fungicide resistance in Plasmopara viticola in France and anti-resistance measures. CAB international 2012. In: Thind TS (ed), Fungicide Resistance in crop protection : Risk and management, pp 157–171
Corio-Costet MF, Dufour MC, Cluzet S, Lambert C, Merdinoglu D (2012) BioMolChem: a tool to assess the defense status of grapevines after stimulations or not of cultivar or resistant genotypes, from genes to the field. Acta Horticult 1009:53–60
Côté F, Hahn MG (1994) Oligosaccharins: structures and signal transduction. Plant Mol Biol 26:1379–1411
Côté F, Ham KS, Hahn MG, Bergmann CW (1998) Oligosaccharide elicitors in host-pathogen interactions. Generation, perception, and signal transduction. Subcell Biochem 29:385–432
Coutos-Thévenot P, Poinssot B, Bonomelli A, Yean H, Breda C, Buffard D, Esnault R, Hain R, Boulay M (2001) In vitro tolerance to Botrytis cinerea of grapevine 41B rootstock in transgenic plants expressing the stilbene synthase Vst1 gene under the control of a pathogen-inducible PR 10 promoter. J Exp Bot 52:901–910
D’Ovidio R, Mattei B, Roberti S, Bellincampi D (2004) Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Biochim Biophys Acta Protein Proteomics 1696:237–244
Dai GH, Andary C, Mondolot-Cosson L, Boubals D (1995) Involvement of phenolic compounds in the resistance of grapevine callus to downy mildew (Plasmopara viticola). Eur J Plant Pathol 101:541–547
Davies C, Robinson SP (2000) Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. Plant Physiol 122:803–812
De León IP, Montesano M (2013) Activation of defense mechanisms against pathogens in mosses and flowering plants. Int J Mol Sci 14:3178–3200
De Lorenzo G, Ferrari S (2002) Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Curr Opin Plant Biol 5:295–299
Delaunois B, Farace G, Jeandet P, Clément C, Baillieul F, Dorey S, Cordelier S (2014) 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
Délye C, Corio-Costet MF (1998) Origin of primary infections of grape by Uncinula necator: RAPD analysis discriminates two biotypes. Mycol Res 102:283–288
Derckel JP, Audran JC, 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
Dercks W, Creasy LL (1989) Influence of fosetyl-Al on phytoalexin accumulation in the Plasmopara viticola-grapevine interaction. Physiol Mol Plant Pathol 34:203–213
Dixon RA (2011) Chris lamb: a visionary leader in plant science. Annu Rev Plant Physiol Plant Mol Biol 49:31–45
Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7:1085–1097
Doares SH, Syrovets T, Weiler EW, Ryan CA (1995) Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Natl Acad Sci U S A 92:4095–4098
Douillet-Breuil AC, Jeandet P, Adrian M, Bessis R (1999) Changes in the phytoalexin content of various Vitis spp. in response to ultraviolet C elicitation. J Agric Food Chem 47:4456–4461
Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167
Dufour MC, Corio-Costet MF (2013) Variability in the sensitivity of biotrophic grapevine pathogens (Erysiphe necator and Plasmopara viticola) to acibenzolar-S methyl and two phosphonates. Eur J Plant Pathol 136:247–259
Dufour MC, Lambert C, Bouscaut J, Mérillon JM, Corio-Costet MF (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
Ebel J (1998) Oligoglucoside elicitor-mediated activation of plant defense. Bioessays 20:569–576
Ebel J, Cosio EG (1994) Elicitors of plant defense responses. Int Rev Cytol 148:1–36
Fanizza G, Bisignano V, Pollastro S, Miazzi M, Faretra F (1995) Effects of polysaccharides from Botryotinia fuckeliana (Botrytis cinerea) on in vitro culture of table and wine grapes (Vitis vinifera). Vitis 34:41–44
Fu Y, Yin H, Wang W, Wang M, Zhang H, Zhao X, Du Y (2011) β-1,3-Glucan with different degree of polymerization induced different defense responses in tobacco. Carbohydr Polym 86:774–782
Giannakis C, Bucheli CS, Skene KGM, Robinson SP, Steele Scott N (1998) Chitinase and β-1,3-glucanase in grapevine leaves: a possible defence against powdery mildew infection. Aust J Grape Wine Res 4:14–22
Gressel J (2011) Low pesticide rates may hasten the evolution of resistance by increasing mutation frequencies. Pest Manag Sci 67:253–257
Grison R, Grezes-Besset B, Schneider M, Lucante N, Olsen L, Leguay JJ, Toppan A (1996) Field tolerance to fungal pathogens of Brassica napus constitutively expressing a chimeric chitinase gene. Nat Biotechnol 14:643–646
Guo J, Du G, Chen J, Chen X, Li X (2011) Oligosaccharides act as elicitors to protect plant against crop disease based on knowledge of plant defense response mechanism. In: Hertsburg CT (ed) Sugar Beet Crops Growth Fertil Yield, 197 pp
Gus-Mayer S, Naton B, Hahlbrock K, Schmelzer E (1998) Local mechanical stimulation induces components of the pathogen defense response in parsley. Proc Natl Acad Sci U S A 95:8398–8403
Inui H, Yamaguchi Y, Hirano S (1997) Elicitor actions of N-acetylchitooligosaccharides and laminarioligosaccharides for chitinase and l-phenylalanine ammonia-lyase induction in rice suspension culture. Biosci Biotechnol Biochem 61:975–978
Jacobs AK, Dry IB, Robinson SP (1999) Induction of different pathogenesis, related cDNAs in grapevine infected with powdery mildew and treated with ethephon. Plant Pathol 48:325–336
Jaulneau V, Lafitte C, Corio-Costet MF, Stadnik MJ, Salamagne S, Briand X, Esquerré-Tugayé MT, Dumas B (2011) An Ulva armoricana extract protects plants against three powdery mildew pathogens. Eur J Plant Pathol 131:393–401
Jeandet P, Bessis R, Maume BF, Meunier P, Peyron D, Trollat P (1995) Effect of enological practices on the resveratrol isomer content of wine. J Agric Food Chem 43:316–319
Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M (2002) Phytoalexins from the vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agric Food Chem 50:2731–2741
Jeandet P, Clément C, Courot E, Cordelier S (2013) Modulation of phytoalexin biosynthesis in engineered plants for disease resistance. Int J Mol Sci 14:14136–14170
Kambiranda D, Katam R, Basha SM, Siebert S (2014) ITRAQ-based quantitative proteomics of developing and ripening muscadine grape berry. J Proteome Res 13:555–569
Klarzynski O, Plesse B, Joubert JM, Yvin JC, Kopp M, Kloareg B, Fritig B (2000) Linear β-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol 124:1027–1037
Kortekamp A, Zyprian E (2003) Characterization of Plasmopara-resistance in grapevine using in vitro plants. J Plant Physiol 160:1393–1400
Lambert C, Khiook ILK, Lucas S, Télef-Micouleau N, Mérillon JM, Cluzet S (2013) A faster and a stronger defense response: one of the key elements in grapevine explaining its lower level of susceptibility to esca? Phytopathology 103:1028–1034
Langcake P, Pryce RJ (1976) The production of resveratrol by Vitis vinifera and other members of the Vitaceae as a response to infection or injury. Physiol Plant Pathol 9:77–86
Langcake P, Pryce RJ (1977a) A new class of phytoalexins from grapevines. Experientia 33:151–152
Langcake P, Pryce RJ (1977b) The production of resveratrol and the viniferins by grapevines in response to ultraviolet irradiation. Phytochemistry 16:1193–1196
Leroux P, Chapeland F, Desbrosses D, Gredt M (1999) Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Prot 18:687–697
Lyon GD, Heilbronn J, Forrest RS, Johnston DJ (1992) The biochemical basis of resistance of potato to soft rot bacteria. Neth J Plant Pathol 98:127–133
Malacarne G, Zulini L, Vrhovsek U, Cestaro A, Stefanini M, Moser C, Mattivi F, Velasco R, Delledonne M (2009) Metabolic and transcriptional changes in resistant and susceptible genotypes of a grapevine population segregating for the resistance to Plasmopara viticola. Acta Horticult 827:635–640
Mauch-Mani B, Métraux J-P (1998) Salicylic acid and systemic acquired resistance to pathogen attack. Ann Bot 82:535–540
Melchior F, Kindl H (1990) Grapevine stilbene synthase cDNA only slightly differing from chalcone synthase cDNA is expressed in Escherichia coli into a catalytically active enzyme. FEBS Lett 268:17–20
Melchior F, Kindl H (1991) Coordinate- and elicitor-dependent expression of stilbene synthase and phenylalanine ammonia-lyase genes in Vitis cv. Optima. Arch Biochem Biophys 288:552–557
Mishra AK, Sharma K, Misra RS (2012) Elicitor recognition, signal transduction and induced resistance in plants. J Plant Interact 7:95–120
Mithofer A, Fliegmann J, Neuhaus-Url G, Schwarz H, Ebel J (2000) The hepta-β-glucoside elicitor-binding proteins from legumes represent a putative receptor family. Biol Chem 381:705–713
Nirala NK, Das DK, Srivastava PS, Sopory SK, Upadhyaya KC (2010) Expression of a rice chitinase gene enhances antifungal potential in transgenic grapevine (Vitis vinifera L.). Vitis J Grapevine Res 49:181–187
Pautot V, Holzer FM, Walling LL (1991) Differential expression of tomato proteinase inhibitor I and II genes during bacterial pathogen invasion and wounding. Mol Plant Microbe Interact 4:284–292
Pawlus AD, Waffo-Téguo P, Shaver J, Mérillon JM (2012) Stilbenoid chemistry from wine and the genus Vitis, a review. J Int Sci Vigne Vin 46:57–111
Pezet R, Perret C, Jean-Denis JB, Tabacchi R, Gindro K, Viret O (2003) δ-Viniferin, a resveratrol dehydrodimer: one of the major stilbenes synthesized by stressed grapevine leaves. J Agric Food Chem 51:5488–5492
Pezet R, Gindro K, Viret O, Spring JL (2004a) Glycosylation and oxidative dimerization of resveratrol are respectively associated to sensitivity and resistance of grapevine cultivars to downy mildew. Physiol Mol Plant Pathol 65:297–303
Pezet R, Gindro K, Viret O, Richter H (2004b) Effects of resveratrol, viniferins and pterostilbene on Plasmopara viticola zoospore mobility and disease development. Vitis J Grapevine Res 43:145–148
Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580
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
Prasad K, Bhatnagar-Mathur P, Waliyar F, Sharma KK (2013) Overexpression of a chitinase gene in transgenic peanut confers enhanced resistance to major soil borne and foliar fungal pathogens. J Plant Biochem Biotechnol 22:222–233
Rasul S, Dubreuil-Maurizi C, Lamotte O, Koen E, Poinssot B, Alcaraz G, Wendehenne D, Jeandroz S (2012) Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ 35:1483–1499
Regev-Shoshani G, Shoseyov O, Bilkis I, Kerem Z (2003) Glycosylation of resveratrol protects it from enzymic oxidation. Biochem J 374:157–163
Renault AS, Deloire A, Bierne J (1996) Pathogenesis-related proteins in grapevines induced by salicylic acid and Botrytis cinerea. Vitis 35:49–52
Reuveni M (1998) Relationships between leaf age, peroxidase and β-1,3-glucanase activity, and resistance to downy mildew in grapevines. J Phytopathol 146:525–530
Revina TA, Gerasimova NG, Kladnitskaya GV, Chalenko GI, Valueva TA (2008) Effect of proteinaceous proteinase inhibitors from potato tubers on the growth and development of phytopathogenic microorganisms. Appl Biochem Microbiol 44:89–92
Richter H, Pezet R, Viret O, Gindro K (2005) Characterization of 3 new partial stilbene synthase genes out of over 20 expressed in Vitis vinifera during the interaction with Plasmopara viticola. Physiol Mol Plant Pathol 67:248–260
Rivière C, Pawlus AD, Mérillon J-M (2012) Natural stilbenoids: distribution in the plant kingdom and chemotaxonomic interest in Vitaceae. Nat Prod Rep 29:1317–1333
Robert N, Ferran J, Breda C, Coutos-Thévenot P, Boulay M, Buffard D, Esnault R (2001) Molecular characterization of the incompatible interaction of Vitis vinifera leaves with Pseudomonas syringae pv. pisi: expression of genes coding for stilbene synthase and class 10 PR protein. Eur J Plant Pathol 107:249–261
Robert N, Roche K, Lebeau Y, Breda C, Esnault R, Buffard D, Buffard D (2002) Expression of grapevine chitinase genes in berries and leaves infected by fungal or bacterial pathogens. Plant Sci 162:389–400
Robinson SP, Jacobs AK, Dry IB (1997) A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol 114:771–778
Romero-Pérez AI, Lamuela-Raventós RM, Andrés-Lacueva C, De La Carmen TBM (2001) Method for the quantitative extraction of resveratrol and piceid isomers in grape berry skins. Effect of powdery mildew on the stilbene content. J Agric Food Chem 49:210–215
Rouhier P, Kopp M, Begot V, Bruneteau M, Fritig B (1995) Structural features of fungal beta-d-glucans for the efficient inhibition of the initiation of virus infection on Nicotiana tabacum. Phytochemistry 39:57–62
Saindrenan P, Barchietto T, Avelino J, Bompeix G (1988) Effects of phosphite on phytoalexin accumulation in leaves of cowpea infected with Phytophthora cryptogea. Physiol Mol Plant Pathol 32:425–435
Salzman RA, Tikhonova I, Bordelon BP, Hasegawa PM, Bressan RA (1998) Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape. Plant Physiol 117:465–472
Schöppner A, Kindl H (1984) Purification and properties of a stilbene synthase from induced cell suspension cultures of peanut. J Biol Chem 259:6806–6811
Schröder G, Brown JW, Schröder J (1988) Molecular analysis of resveratrol synthase. cDNA, genomic clones and relationship with chalcone synthase. Eur J Biochem 172:161–169
Sharp JK, Valent B, Albersheim P (1984) Purification and partial characterization of a beta-glucan fragment that elicits phytoalexin accumulation in soybean. J Biol Chem 259:11312–11320
Shen X, Du Q, Xu Y, Lu Y (2012) Stimulation of trans-resveratrol biosynthesis in Vitis vinifera cv. Kyoho cell suspension cultures by 2, 3-dihydroxypropyl jasmonate elicitation. Electron J Biotechnol 15:3
Sparvoli F, Martin C, Scienza A, Gavazzi G, Tonelli C (1994) Cloning and molecular analysis of structural genes involved in flavonoid and stilbene biosynthesis in grape (Vitis vinifera L.). Plant Mol Biol 24:743–755
Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annu Rev Plant Physiol Plant Mol Biol 35:235–270
Tattersall DB, Van Heeswijck R, Høj PB (1997) Identification and characterization of a fruit-specific, thaumatin-like protein that accumulates at very high levels in conjunction with the onset of sugar accumulation and berry softening in grapes. Plant Physiol 114:759–769
Ten Have A, Mulder W, Visser J, Van Kan JAL (1998) The endopolygalacturonase gene Bcpg1 is required to full virulence of Botrytis cinerea. Mol Plant Microbe Interact 11:1009–1016
Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, Maeder MN, Métraux JP, Mauch-Mani B (2005) Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987–999
Trouvelot S, Varnier AL, Allègre M et al (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
Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97
Vander P, Våain KM, Domard A, El Gueddari NE, Moerschbacher BM (1998) Comparison of the ability of partially n-acetylated chitosans and chitooligosaccharides to elicit resistance reactions in wheat leaves. Plant Physiol 118:1353–1359
Waffo Teguo P, Decendit A, Krisa S, Deffieux G, Vercauteren J, Mérillon JM (1996) The accumulation of stilbene glycosides in Vitis vinifera cell suspension cultures. J Nat Prod 59:1189–1191
Wang X, Zhu X, Tooley P, Zhang X (2013) Cloning and functional analysis of three genes encoding polygalacturonase-inhibiting proteins from Capsicum annuum and transgenic CaPGIP1 in tobacco in relation to increased resistance to two fungal pathogens. Plant Mol Biol 81:379–400
Wiese W, Vornam B, Krause E, Kindl H (1994) Structural organization and differential expression of three stilbene synthase genes located on a 13 kb grapevine DNA fragment. Plant Mol Biol 26:667–677
Winer J, Jung CKS, Shackel I, Williams PM (1999) Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270:41–49
Zimmerli L, Jakab G, Métraux JP, Mauch-Mani B (2000) Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proc Natl Acad Sci U S A 97:12920–12925
Acknowledgments
The authors thank the “Conseil Interprofessionnel des Vins de la Région de Bergerac” for financial support, Mr. Jérôme Jolivet and Mr. Sébastien Gambier for plant care and technical assistance, and Dr. Marc Fermaud and Dr. Pascal Lecomte for scientific advice.
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Saigne-Soulard, C. et al. (2014). Oligosaccharides from Botrytis cinerea and Elicitation of Grapevine Defense. In: Ramawat, K., Mérillon, JM. (eds) Polysaccharides. Springer, Cham. https://doi.org/10.1007/978-3-319-03751-6_8-1
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