Recognition of Elicitors in Grapevine: From MAMP and DAMP Perception to Induced Resistance
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
31620151
PubMed Central
PMC6760519
DOI
10.3389/fpls.2019.01117
Knihovny.cz E-zdroje
- Klíčová slova
- Damage-Associated Molecular Pattern (DAMP), Induced Resistance (IR), Microbe-Associated Molecular Pattern (MAMP), Pattern Recognition Receptor (PRR), Vitis vinifera, defense responses, innate immunity,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
In a context of a sustainable viticulture, the implementation of innovative eco-friendly strategies, such as elicitor-triggered immunity, requires a deep knowledge of the molecular mechanisms underlying grapevine defense activation, from pathogen perception to resistance induction. During plant-pathogen interaction, the first step of plant defense activation is ensured by the recognition of microbe-associated molecular patterns, which are elicitors directly derived from pathogenic or beneficial microbes. Vitis vinifera, like other plants, can perceive elicitors of different nature, including proteins, amphiphilic glycolipid, and lipopeptide molecules as well as polysaccharides, thanks to their cognate pattern recognition receptors, the discovery of which recently began in this plant species. Furthermore, damage-associated molecular patterns are another class of elicitors perceived by V. vinifera as an invader's hallmark. They are mainly polysaccharides derived from the plant cell wall and are generally released through the activity of cell wall-degrading enzymes secreted by microbes. Elicitor perception and subsequent activation of grapevine immunity end in some cases in efficient grapevine resistance against pathogens. Using complementary approaches, several molecular markers have been identified as hallmarks of this induced resistance stage. This review thus focuses on the recognition of elicitors by Vitis vinifera describing the molecular mechanisms triggered from the elicitor perception to the activation of immune responses. Finally, we discuss the fact that the link between elicitation and induced resistance is not so obvious and that the formulation of resistance inducers remains a key step before their application in vineyards.
Agroécologie Agrosup Dijon CNRS INRA Univ Bourgogne Univ Bourgogne Franche Comté Dijon France
Laboratory of Plant Pathology Department of Biotechnology University of Verona Verona Italy
UniLaSalle AGHYLE Research Unit UP 2018 C101 Rouen France
Unité RIBP EA 4707 SFR Condorcet FR CNRS 3417 University of Reims Champagne Ardenne Reims France
Zobrazit více v PubMed
Adrian M., Trouvelot S., Gamm M., Poinssot B., Héloir M. C., Daire X., (2012). “Activation of grapevine defense mechanisms: theoretical and applied approaches,” in Progress in biological control, plant defence: biological control, vol. 12 Ed. Ramawat J. M. K. (Dordrecht: Springer; ), 313–331. 10.1007/978-94-007-1933-0_13 DOI
Ait Barka E., Belarbi A., Hachet C., Nowak J., Audran J. (2000). Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol. Lett. 186, 91–95. 10.1111/j.1574-6968.2000.tb09087.x PubMed DOI
Ait Barka E., Nowak J., Clement C. (2006). Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 72, 7246–7252. 10.1128/AEM.01047-06 PubMed DOI PMC
Alexandrova M., Bazzi C., Holst O. (2000). Protective effect of bacterial lipopolysaccharides in the grapevine-Agrobacterium vitis interaction. Vitis 39, 67–70.
Aziz A., Gauthier A., Bezler A., Poinssot B., Joubert J. M., Pugin A., et al. (2007). Elicitor and resistance-inducing activities of beta-1,4 cellodextrins in grapevine, comparison with beta-1,3 glucans and alpha-1,4 oligogalacturonides. J. Exp. Bot. 58, 1463–1472. 10.1093/jxb/erm008 PubMed DOI
Aziz A., Poinssot B., Daire X., Adrian M., Bezier A., Lambert B., et al. (2003). Laminarin elicits defense responses in grapevine and induces protection against Botrytis cinerea and Plasmopara viticola. Mol. Plant-Microbe Interact. 16, 1118–1128. 10.1094/MPMI.2003.16.12.1118 PubMed DOI
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. 10.1094/PHYTO-96-1188 PubMed DOI
Bacic A., Fincher G. B., Stone B. A., (2009). Chemistry, biochemistry, and biology of 1-3 beta glucans and related polysaccharides. (Elsevier, Burlington,. MA, USA: Academic Press; ).
Baker L. G., Specht C. A., Donlin M. J., Lodge J. K. (2007). Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans. Eukaryot Cell 6, 855–867. 10.1128/EC.00399-06 PubMed DOI PMC
Banani H., Roatti B., Ezzahi B., Giovannini O., Gessler G., Pertot I., et al. (2014). Characterization of resistance mechanisms activated by Trichoderma harzianum T39 and benzothiadiazole to downy mildew in different grapevine cultivars. Plant Pathol. 63, 334–343. 10.1111/ppa.12089 DOI
Barber M. S., Bertram R. E., Ride J. P. (1989). Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol. Mol. Plant Pathol. 34, 3–12. 10.1016/0885-5765(89)90012-X DOI
Bauer Z., Gomez-Gomez L., Boller T., Felix G. (2001). Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. J. Biol. Chem. 276, 45669–45676. 10.1074/jbc.M102390200 PubMed DOI
Benedetti M., Pontiggia D., Raggi S., Cheng Z., Scaloni F., Ferrari S., et al. (2015). Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns. Proc. Natl. Acad. Sci. U. S. A. 112, 5533–5538. 10.1073/pnas.1504154112 PubMed DOI PMC
Benedetti M., Verrascina I., Pontiggia D., Locci F., Mattei B., De Lorenzo G., et al. (2018). Four Arabidopsis berberine bridge enzyme-like proteins are specific oxidases that inactivate the elicitor-active oligogalacturonides. Plant J. 94, 260–273. 10.1111/tpj.13852 PubMed DOI
Berry M. C., McGhee G. C., Zhao Y., Sundin G. W. (2009). Effect of a waaL mutation on lipopolysaccharide composition, oxidative stress survival, and virulence in Erwinia amylovora. FEMS Microbiol. Lett. 291, 80–87. 10.1111/j.1574-6968.2008.01438.x PubMed DOI
Binet M. N., Bourque S., Lebrun-Garcia A., Chiltz A., Pugin A. (1998). Comparison of the effects of cryptogein and oligogalacturonides on tobacco cells and evidence of different forms of desensitization induced by these elicitors. Plant Sci. 137, 33–41. 10.1016/S0168-9452(98)00132-0 DOI
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. 10.1146/annurev.arplant.57.032905.105346 PubMed DOI
Bordiec S., Paquis S., Lacroix H., Dhondt S., Ait Barka E., Kauffmann S., et al. (2011). Comparative analysis of defence responses induced by the endophytic plant growth-promoting rhizobacterium Burkholderia phytofirmans strain PsJN and the non-host bacterium Pseudomonas syringae pv. pisi in grapevine cell suspensions. J. Exp. Bot. 62, 595–603. 10.1093/jxb/erq291 PubMed DOI
Boutrot F., Zipfel C. (2017). Function, discovery, and exploitation of plant pattern recognition receptors for broad-spectrum disease resistance. Annu. Rev. Phytopathol. 55, 257–286. 10.1146/annurev-phyto-080614-120106 PubMed DOI
Bozsoki Z., Cheng J., Feng F., Gysel K., Vinther M., Andersen K. R., et al. (2017). Receptor-mediated chitin perception in legume roots is functionally separable from Nod factor perception. Proc. Natl. Acad. Sci. U. S. A. 114, E8118–E8127. 10.1073/pnas.1706795114 PubMed DOI PMC
Braun S. G., Meyer A., Holst O., Pühler A., Niehaus K. (2005). Characterization of the Xanthomonas campestris pv. campestris lipopolysaccharide substructures essential for elicitation of an oxidative burst in tobacco cells. Mol. Plant Microbe Interact. 18, 674–681. 10.1094/MPMI-18-0674 PubMed DOI
Brulé D., Villano C., Davies L. J., Trdá L., Claverie J., Héloir M. C., et al. (2019). The grapevine (Vitis vinifera) LysM receptor kinases VvLYK1-1 and VvLYK1-2 mediate chitooligosaccharide-triggered immunity. Plant Biotechnol. J. 17, 812–825. 10.1111/pbi.13017 PubMed DOI PMC
Brutus A., Sicilia F., Macone A., Cervone F., De Lorenzo G. (2010). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Sci. U. S. A. 107, 9452–9457. 10.1073/pnas.1000675107 PubMed DOI PMC
Cabrera J. C., Boland A., Messiaen J., Cambier P., Van Cutsem P. (2008). Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18, 473–482. 10.1093/glycob/cwn027 PubMed DOI
Cao Y., Liang Y., Tanaka K., Nguyen C. T., Jedrzejczak R. P., Joachimiak A., et al. (2014). The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 3, 03766. 10.7554/eLife.03766 PubMed DOI PMC
Caroff M., Karibian D. (2003). Structure of bacterial lipopolysaccharides. Carbohydr. Res. 338, 2431–2447. 10.1016/j.carres.2003.07.010 PubMed DOI
Casida J. E. (2009). Pest toxicology: the primary mechanisms of pesticide action. Chem. Res. Toxicol. 22, 609–619. 10.1021/tx8004949 PubMed DOI
Cervone F., De Lorenzo G., Degrà L., Salvi G. (1987). Elicitation of necrosis in Vigna unguiculata Walp. by homogeneous Aspergillus niger endo-polygalacturonase and by alpha-d-galacturonate oligomers. Plant Physiol. 85, 626–630. 10.1104/pp.85.3.626 PubMed DOI PMC
Chalal M., Winkler J. B., Gourrat K., Trouvelot S., Adrian M., Schnitzler J. P., et al. (2015). Sesquiterpene volatile organic compounds (VOCs) are markers of elicitation by sulfated laminarine in grapevine. Front. Plant Sci. 6, 350. 10.3389/fpls.2015.00350 PubMed DOI PMC
Chinchilla D., Bauer Z., Regenass M., Boller T., Felix G. (2006). The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18, 465–476. 10.1105/tpc.105.036574 PubMed DOI PMC
Claverie J., Balacey S., Lemaître-Guillier C., Brulé D., Chiltz A., Granet L., et al. (2018). The cell wall-derived xyloglucan is a new DAMP triggering plant immunity in Vitis vinifera and Arabidopsis thaliana. Front. Plant Sci. 9, 1725. 10.3389/fpls.2018.01725 PubMed DOI PMC
Clifford J. C., Rapicavoli J. N., Roper M. C. (2013). A rhamnose-rich O-antigen mediates adhesion, virulence, and host colonization for the xylem-limited phytopathogen Xylella fastidiosa. Mol. Plant Microbe Interact. 26, 676–685. 10.1094/MPMI-12-12-0283-R PubMed DOI
Compant S., Reiter B., Sessitsch A., Nowak J., Clement C., Ait Barka E. (2005). Endophytic colonization of Vitis vinifera L. by plant growth promoting bacterium Burkholderia sp strain PsJN. Appl. Environ. Microbiol. 71, 1685–1693. 10.1128/AEM.71.4.1685-1693.2005 PubMed DOI PMC
Conrath U. (2011). Molecular aspects of defence priming. Trends Plant Sci. 16, 524–531. 10.1016/j.tplants.2011.06.004 PubMed DOI
Conrath U., Beckers G. J. M., Flors V., Garcia-Agustin P., Jakab G., Mauch F., et al. (2006). Priming: getting ready for battle. Mol. Plant-Microbe Interact. 19, 1062–1071. 10.1094/MPMI-19-1062 PubMed DOI
Davidsson P., Broberg M., Kariola T., Sipari N., Pirhonen M., Palva E. T. (2017). Short oligogalacturonides induce pathogen resistance-associated gene expression in Arabidopsis thaliana. BMC Plant Biol. 17, 19. 10.1186/s12870-016-0959-1 PubMed DOI PMC
Decreux A., Thomas A., Spies B., Brasseur R., Van Cutsem P., Messiaen J. (2006). In vitro characterization of the homogalacturonan-binding domain of the wall-associated kinase WAK1 using site-directed mutagenesis. Phytochemistry 67, 1068–1079. 10.1016/j.phytochem.2006.03.009 PubMed DOI
Delaunois B., Farace G., Jeandet P., Clément C., Baillieul F., Dorey S., et al. (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. Int. 21, 4837–4846. 10.1007/s11356-013-1841-4 PubMed DOI
Deleu M., Paquot M., Nylander T. (2005). Fengycin interaction with lipid monolayers at the air-aqueous interface-implications for the effect of fengycin on biological membranes. J. Colloid Interface Sci. 283, 358–365. 10.1016/j.jcis.2004.09.036 PubMed DOI
Deleu M., Paquot M., Nylander T. (2008). Effect of fengycin, a lipopeptide produced by Bacillus subtilis, on model biomembranes. Biophys. J. 94, 2667–2679. 10.1529/biophysj.107.114090 PubMed DOI PMC
Delteil A., Gobbato E., Cayrol B., Estevan J., Michel-Romiti C., Dievart A., et al. (2016). Several wall-associated kinases participate positively and negatively in basal defense against rice blast fungus. BMC Plant Biol. 16, 17. 10.1186/s12870-016-0711-x PubMed DOI PMC
Denoux C., Galletti R., Mammarella N., Gopalan S., Werck D., De Lorenzo G., et al. (2008). Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1, 423–445. 10.1093/mp/ssn019 PubMed DOI PMC
Derckel J. P., Baillieul F., Manteau S., Audran J. C., Haye B., Lambert B., et al. (1999). Differential induction of grapevine defenses by two strains of Botrytis cinerea. Phytopathology 89, 197–203. 10.1094/PHYTO.1999.89.3.197 PubMed DOI
Desaki Y., Kouzai Y., Ninomiya Y., Iwase R., Shimizu Y., Seko K., et al. (2018). OsCERK1 plays a crucial role in the lipopolysaccharide-induced immune response of rice. New Phytol. 217, 1042–1049. 10.1111/nph.14941 PubMed DOI
Desaki Y., Miya A., Venkatesh B., Tsuyumu S., Yamane H., Kaku H., et al. (2006). Bacterial lipopolysaccharides induce defense responses associated with programmed cell death in rice cells. Plant Cell Physiol. 47, 1530–1540. 10.1093/pcp/pcl019 PubMed DOI
Di Lorenzo F., Palmigiano A., Silipo A., Desaki Y., Garozzo D., Lanzetta R., et al. (2016). The structure of the lipooligosaccharide from Xanthomonas oryzae pv. Oryzae: the causal agent of the bacterial leaf blight in rice. Carbohydr. Res. 427, 38–43. 10.1016/j.carres.2016.03.026 PubMed DOI
Diener A. C., Ausubel F. M. (2005). Resistance To Fusarium Oxysporum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 171, 305–321. 10.1534/genetics.105.042218 PubMed DOI PMC
dos Santos H. P., Purgatto E., Mercier H., Buckeridge M. S. (2004). The control of storage xyloglucan mobilization in cotyledons of Hymenaea courbaril. Plant Physiol. 135, 287–299. 10.1104/pp.104.040220 PubMed DOI PMC
El Hadrami A., Adam L. R., El Hadrami I., Daayf F. (2010). Chitosan in plant protection. Mar. Drugs 8, 968–987. 10.3390/md8040968 PubMed DOI PMC
Enkerli J., Felix G., Boller T. (1999). The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiol. 121, 391–397. 10.1104/pp.121.2.391 PubMed DOI PMC
Farace G., Fernandez O., Jacquens L., Coutte F., Krier F., Jacques P., et al. (2015). Cyclic lipopeptides from Bacillus subtilis activate distinct patterns of defence responses in grapevine. Mol. Plant Pathol. 16, 177–187. 10.1111/mpp.12170 PubMed DOI PMC
Felix G., Duran J. D., Volko S., Boller T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265–276. 10.1046/j.1365-313X.1999.00265.x PubMed DOI
Fernandez O., Theocharis A., Bordiec S., Feil R., Jacquens L., Clement C., et al. (2012). Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol. Plant-Microbe Interact. 25, 496–504. 10.1094/MPMI-09-11-0245 PubMed DOI
Ferrari S., Galletti R., Denoux C., De Lorenzo G., Ausubel F. M., Dewdney J. (2007). Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires Phytoalexin Deficient 3. Plant Physiol. 144, 367–379. 10.1104/pp.107.095596 PubMed DOI PMC
Fry S. C., Aldington S., Hetherington P. R., Aitken J. (1993). Oligosaccharides as signals and substrates in the plant cell wall. Plant Physiol. 103, 1–5. 10.1104/pp.103.1.1 PubMed DOI PMC
Furman-Matarasso N., Cohen E., Du Q., Chejanovsky N., Hanania U., Avni A. (1999). A point mutation in the ethylene-inducing xylanase elicitor inhibits the beta-1-4-endoxylanase activity but not the elicitation activity. Plant Physiol. 121, 345–351. 10.1104/pp.121.2.345 PubMed DOI PMC
Galletti R., Denoux C., Gambetta S., Dewdney J., Ausubel F. M., De Lorenzo G., et al. (2008). The AtrbohD-Mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol. 148, 1695–1706. 10.1104/pp.108.127845 PubMed DOI PMC
Galletti R., Ferrari S., De Lorenzo G. (2011). Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against . Plant Physiol. 157, 804–814. 10.1104/pp.111.174003 PubMed DOI PMC
Garcia-Brugger A., Lamotte O., Vandelle E., Bourque S., Lecourieux D., Poinssot B., et al. (2006). Early signaling events induced by elicitors of plant defenses. Mol. Plant-Microbe Interact. 19, 711–724. 10.1094/MPMI-19-0711 PubMed DOI
Gauthier A. (2009). Comparaison de différents éliciteurs des réactions de défense de la vigne: étude du mode d’action de la laminarine sulfatée, un inducteur de résistance à P. viticola. PhD Thesis. Dijon (F): Univ. Bourgogne.
Gauthier A., Lamotte O., Reboutier D., Bouteau F., Pugin A., Wendehenne D. (2007). Cryptogein-induced anion effluxes: electrophysiological properties and analysis of the mechanisms through which they contribute to the elicitor-triggered cell death. Plant Signal Behav. 2, 86–95. 10.4161/psb.2.2.4015 PubMed DOI PMC
Gauthier A., Trouvelot S., Kelloniemi J., Frettinger P., Wendehenne D., Daire X., et al. (2014). The sulfated laminarin triggers a stress transcriptome before priming the SA- and ROS-dependent defenses during grapevine’s induced resistance against Plasmopara viticola. PLoS One 9, e88145. 10.1371/journal.pone.0088145 PubMed DOI PMC
Gimenez-Ibanez S., Ntoukakis V., Rathjen J. P. (2009). The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis . Plant Signal Behav. 4, 539–541. 10.4161/psb.4.6.8697 PubMed DOI PMC
Gomez-Gomez L., Boller T. (2000). FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis . Mol. Cell 5, 1003–1011. 10.1016/S1097-2765(00)80265-8 PubMed DOI
Gramegna G., Modesti V., Savatin D. V., Sicilia F., Cervone F., De Lorenzo G. (2016). GRP-3 and KAPP, encoding interactors of WAK1, negatively affect defense responses induced by oligogalacturonides and local response to wounding. J. Exp. Bot. 67, 1715–1729. 10.1093/jxb/erv563 PubMed DOI PMC
Gust A. A., Felix G. (2014). Receptor like proteins associate with SOBIR1-type of adaptors to form bimolecular receptor kinases. Curr. Opin. Plant Biol. 21, 104–111. 10.1016/j.pbi.2014.07.007 PubMed DOI
Hadwiger L. A. (2013). Multiple effects of chitosan on plant systems: solid science or hype. Plant Sci. 208, 42–49. 10.1016/j.plantsci.2013.03.007 PubMed DOI
Haile Z. M., Pilati S., Sonego P., Malacarne G., Vrhovsek U., Engelen K., et al. (2017). Molecular analysis of the early interaction between the grapevine flower and Botrytis cinerea reveals that prompt activation of specific host pathways leads to fungus quiescence. Plant Cell Environ. 40, 1409–1428. 10.1111/pce.12937 PubMed DOI
Harkenrider M., Sharma R., De Vleesschauwer D., Tsao L., Zhang X., Chern M., et al. (2016). Overexpression of rice wall-associated kinase 25 (OsWAK25) alters resistance to bacterial and fungal pathogens. PLoS One 11, e0147310. 10.1371/journal.pone.0147310 PubMed DOI PMC
Hayafune M., Berisio R., Marchetti R., Silipo A., Kayama M., Desaki Y., et al. (2014). Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc. Natl. Acad. Sci. U. S. A. 111, E404–E413. 10.1073/pnas.1312099111 PubMed DOI PMC
He Z. H., Cheeseman I., He D., Kohorn B. D. (1999). A cluster of five cell wall-associated receptor kinase genes, Wak1-5, are expressed in specific organs of Arabidopsis . Plant Mol. Biol. 39, 1189–1196. 10.1023/A:1006197318246 PubMed DOI
He Z. H., Fujiki M., Kohorn B. D. (1996). A cell wall-associated, receptor-like protein kinase. J. Biol. Chem. 271, 19789–19793. 10.1074/jbc.271.33.19789 PubMed DOI
Henry G., Deleu M., Jourdan E., Thonart P., Ongena M. (2011). The bacterial lipopeptide surfactin targets the lipid fraction of the plant plasma membrane to trigger immune-related defence responses. Cell Microbiol. 13, 1824–1837. 10.1111/j.1462-5822.2011.01664.x PubMed DOI
Hurni S., Scheuermann D., Krattinger S. G., Kessel B., Wicker T., Herren G., et al. (2015). The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proc. Natl. Acad. Sci. U. S. A. 112, 8780–8785. 10.1073/pnas.1502522112 PubMed DOI PMC
Jeandroz S., Wipf D., Stuehr D. J., Lamattina L., Melkonian M., Tian Z., et al. (2016). Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Sci. Signal 9, re2. 10.1126/scisignal.aad4403 PubMed DOI
Johnson J. M., Thürich J., Petutschnig E. K., Altschmied L., Meichsner D., Sherameti I., et al. (2018). A Poly(A) ribonuclease controls the cellotriose-based interaction between Piriformospora indica and its host Arabidopsis . Plant Physiol. 176, 2496–2514. 10.1104/pp.17.01423 PubMed DOI PMC
Joubert D. A., Kars I., Wagemakers L., Bergmann C., Kemp G., Vivier M. A., et al. (2007). A polygalacturonase-inhibiting protein from grapevine reduces the symptoms of the endopolygalacturonase BcPG2 from Botrytis cinerea in Nicotiana benthamiana leaves without any evidence for in vitro interaction. Mol. Plant Microbe Interact. 20, 392–402. 10.1094/MPMI-20-4-0392 PubMed DOI
Joubert D. A., Slaughter A. R., Kemp G., Becker J. V., Krooshof G. H., Bergmann C., et al. (2006). The grapevine polygalacturonase-inhibiting protein (VvPGIP1) reduces Botrytis cinerea susceptibility in transgenic tobacco and differentially inhibits fungal polygalacturonases. Transgenic Res. 15, 687–702. 10.1007/s11248-006-9019-1 PubMed DOI
Jourdan E., Henry G., Duby F., Dommes J., Barthelemy J., Thonart P., et al. (2009). insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol. Plant-Microbe Interact. 22, 456–468. 10.1094/MPMI-22-4-0456 PubMed DOI
Kaku H., Nishizawa Y., Ishii-Minami N., Akimoto-Tomiyama C., Dohmae N., Takio K., et al. (2006). Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Nat. Acad. Sci. U.S.A. 103, 11086–11091. 10.1073/pnas.0508882103 PubMed DOI PMC
Kalunke R. M., Tundo S., Benedetti M., Cervone F., De Lorenzo G., D’Ovidio R. (2015). An update on polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein that protects crop plants against pathogens. Front. Plant Sci. 6, 146. 10.3389/fpls.2015.00146 PubMed DOI PMC
Kars I., Krooshof G. H., Wagemakers L., Joosten R., Benen J. A., van Kan J. A. (2005). Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J. 43, 213–225. 10.1111/j.1365-313X.2005.02436.x PubMed DOI
Khalil M. S., Badawy M. E. (2012). Nematicidal activity of a biopolymer chitosan at different molecular weights against root-knot nematode, Meloidogyne incognita. Plant Prot. Sci. 48, 170–178. 10.17221/46/2011-PPS DOI
Klarzynski O., Plesse B., Joubert J. M., Yvin J. C., Kopp M., Kloareg B., et al. (2000). Linear beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol. 124, 1027–1037. 10.1104/pp.124.3.1027 PubMed DOI PMC
Kunz C., Vandelle E., Rolland S., Poinssot B., Bruel C., Cimerman A., et al. (2006). Characterization of a new, nonpathogenic mutant of Botrytis cinerea with impaired plant colonization capacity. New Phytol. 170, 537–550. 10.1111/j.1469-8137.2006.01682.x PubMed DOI
Kutschera A., Dawid C., Gisch N., Schmid C., Raasch L., Gerster T., et al. (2019). Bacterial medium-chain 3-hydroxy fatty acid metabolites trigger immunity in Arabidopsis plants. Science 364, 178–181. 10.1126/science.aau1279 PubMed DOI
Kutschera A., Ranf S. (2019). The multifaceted functions of lipopolysaccharide in plant-bacteria interactions. Biochimie 159, 93–98. 10.1016/j.biochi.2018.07.028 PubMed DOI
Lamotte O., Gould K., Lecourieux D., Sequeira-Legrand A., Lebrun-Garcia A., Durner J., et al. (2004). Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol. 135, 516–529. 10.1104/pp.104.038968 PubMed DOI PMC
Lecourieux D., Mazars C., Pauly N., Ranjeva R., Pugin A. (2002). Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14, 2627–2641. 10.1105/tpc.005579 PubMed DOI PMC
Lemaître-Guillier C., Hovasse A., Schaeffer-Reiss C., Recorbet G., Poinssot B., Trouvelot S., et al. (2017). Proteomics towards the understanding of elicitor induced resistance of grapevine against downy mildew. J. Proteomics 156, 113–125. 10.1016/j.jprot.2017.01.016 PubMed DOI
Lenarčič T., Albert I., Böhm H., Hodnik V., Pirc K., Zavec A. B., et al. (2017). Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins. Science 358, 1431–1434. 10.1126/science.aan6874 PubMed DOI
Lerouge I., Vanderleyden J. (2002). O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol. Rev. 26, 17–47. 10.1111/j.1574-6976.2002.tb00597.x PubMed DOI
Li C. H., Wang K. C., Hong Y. H., Chu T. H., Chu Y. J., Chou I. C., et al. (2014). Roles of different forms of lipopolysaccharides in Ralstonia solanacearum pathogenesis. Mol. Plant Microbe Interact. 27, 471–478. 10.1094/MPMI-08-13-0248-R PubMed DOI
Li H., Zhou S. Y., Zhao W. S., Su S. C., Peng Y. L. (2009). A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol. Biol. 69, 337–346. 10.1007/s11103-008-9430-5 PubMed DOI
Li Y., Héloir M. C., Zhang X., Geissler M., Trouvelot S., Jacquens L., et al. (2019). Surfactin and fengycin contribute to the protection of a Bacillus subtilis strain against grape downy mildew by both direct effect and defense stimulation. Mol. Plant Pathol. 20(8), 1037–1050 10.1111/mpp.12809 PubMed DOI PMC
Lo Piccolo S., Ferraro V., Alfonzo A., Settanni L., Ercolini D., Burruano S., et al. (2010). Presence of endophytic bacteria in Vitis vinifera leaves as detected by fluorescence in situ hybridization. Ann. Microbiol. 60, 161–167. 10.1007/s13213-010-0023-6 DOI
Locci F., Benedetti M., Pontiggia D., Citterico M., Caprari C., Mattei B., et al. (2019). An Arabidopsis berberine bridge enzyme-like protein specifically oxidizes cellulose oligomers and plays a role in immunity. Plant J. 98, 540–554. 10.1111/tpj.14237 PubMed DOI
Luna E., Pastor V., Robert J., Flors V., Mauch-Mani B., Ton J. (2011). Callose deposition: a multifaceted plant defense response. Mol. Plant Microbe Interact. 24, 183–193. 10.1094/MPMI-07-10-0149 PubMed DOI
Luzuriaga-Loaiza W. P., Schellenberger R., De Gaetano Y., Obounou Akong F., Villaume S., Crouzet J., et al. (2018). Synthetic rhamnolipid bolaforms trigger an innate immune response in Arabidopsis thaliana. Sci. Rep. 8, 8534. 10.1038/s41598-018-26838-y PubMed DOI PMC
Maget-Dana R., Ptak M. (1990). Iturin lipopeptides: interactions of mycosubtilin with lipids in planar membranes and mixed monolayers. Biochim. Biophys. Acta 1023, 34–40. 10.1016/0005-2736(90)90006-A PubMed DOI
Melotto M., Underwood W., Koczan J., Nomura K., He S. Y. (2006). Plant stomata function in innate immunity against bacterial invasion. Cell 126, 969–980. 10.1016/j.cell.2006.06.054 PubMed DOI
Miya A., Albert P., Shinya T., Desaki Y., Ichimura K., Shirasu K., et al. (2007). CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Nat. Acad. Sci. U.S.A. 104, 19613–19618. 10.1073/pnas.0705147104 PubMed DOI PMC
Moerschbacher B. M., Mierau M., Graeßner B., Noll U., Mort A. J. (1999). Small oligomers of galacturonic acid are endogenous suppressors of disease resistance reactions in wheat leaves. J. Exp. Bot. 50, 605–612. 10.1093/jxb/50.334.605 DOI
Monnier N., Furlan A., Botcazon C., Dahi A., Mongelard G., Cordelier S., et al. (2018). Rhamnolipids From Pseudomonas aeruginosa are elicitors triggering Brassica napus protection against Botrytis cinerea without physiological disorders. Front. Plant Sci. 9, 1170. 10.3389/fpls.2018.01170 PubMed DOI PMC
Monnier N., Furlan A. L., Buchoux S., Deleu M., Dauchez M., Rippa S., et al. (2019). Exploring the dual interaction of natural rhamnolipids with plant and fungal biomimetic plasma membranes through biophysical studies. Int. J. Mol. Sci. 20(5), 1009. 10.3390/ijms20051009 PubMed DOI PMC
Moscatiello R., Mariani P., Sanders D., Maathuis F. J. M. (2006). Transcriptional analysis of calcium-dependent and calcium-independent signalling pathways induced by oligogalacturonides. J. Exp. Bot. 57, 2847–2865. 10.1093/jxb/erl043 PubMed DOI
Mueller K., Bittel P., Chinchilla D., Jehle A., Albert M., Boller T., et al. (2012). Chimeric FLS2 receptors reveal the basis for differential flagellin perception in Arabidopsis and tomato. Plant Cell 24, 2213–2224. 10.1105/tpc.112.096073 PubMed DOI PMC
Mélida H., Sopeña-Torres S., Bacete L., Garrido-Arandia M., Jordá L., López G., et al. (2018). Non-branched β-1,3-glucan oligosaccharides trigger immune responses in Arabidopsis . Plant J. 93, 34–49. 10.1111/tpj.13755 PubMed DOI
Ménard R., Alban S., de Ruffray P., Jamois F., Franz G., Fritig B., et al. (2004). Beta-1,3 glucan sulfate, but not beta-1,3 glucan, induces the salicylic acid signaling pathway in tobacco and Arabidopsis . Plant Cell 16, 3020–3032. 10.1105/tpc.104.024968 PubMed DOI PMC
Ménard R., de Ruffray P., Fritig B., Yvin J. C., Kauffmann S. (2005). Defense and resistance-inducing activities in tobacco of the sulfated beta-1,3 glucan PS3 and its synergistic activities with the unsulfated molecule. Plant Cell Physiol. 46, 1964–1972. 10.1093/pcp/pci212 PubMed DOI
Nanni I. M., Pirondi A., Contaldo N., Collina M. (2016). Screening of sensitivity to mandipropamid of Plasmopara viticola populations from Italian vineyards by molecular and biological methods. Lett. Appl. Microbiol. 63, 268–273. 10.1111/lam.12613 PubMed DOI
Nasir M. N., Lins L., Crowet J. M., Ongena M., Dorey S., Dhondt-Cordelier S., et al. (2017). Differential interaction of synthetic glycolipids with biomimetic plasma membrane lipids correlates with the plant biological response. Langmuir 33, 9979–9987. 10.1021/acs.langmuir.7b01264 PubMed DOI
Norman C., Vidal S., Palva E. T. (1999). Oligogalacturonide-mediated induction of a gene involved in jasmonic acid synthesis in response to the cell-wall-degrading enzymes of the plant pathogen Erwinia carotovora. Mol. Plant Microbe Interact. 12, 640–644. 10.1094/MPMI.1999.12.7.640 PubMed DOI
Nunes da Silva M., Cardoso A. R., Ferreira D., Brito M., Pintado M. E., Vasconcelos M. W. (2014). Chitosan as a biocontrol agent against the pinewood nematode (Bursaphelenchus xylophilus). For. Pathol. 44, 420–423. 10.1111/efp.12136 DOI
Ongena M., Jacques P. (2008). Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol. 16, 115–125. 10.1016/j.tim.2007.12.009 PubMed DOI
Paris F., Krzyżaniak Y., Gauvrit C., Jamois F., Domergue F., Joubès J., et al. (2016). An ethoxylated surfactant enhances the penetration of the sulfated laminarin through leaf cuticle and stomata, leading to increased induced resistance against grapevine downy mildew. Physiol. Plant 156, 338–350. 10.1111/ppl.12394 PubMed DOI
Park R. D., Jo K. J., Jo Y. Y., Jin Y. L., Kim K. Y., Shim J. H., et al. (2002). Variation of antifungal activities of chitosans on plant pathogens. J. Microbiol. Biotechnol. 12, 84–88.
Pauly M., Keegstra K. (2016). Biosynthesis of the plant cell wall matrix polysaccharide xyloglucan. Annu. Rev. Plant Biol. 67, 235–259. 10.1146/annurev-arplant-043015-112222 PubMed DOI
Petrocelli S., Tondo M. L., Daurelio L. D., Orellano E. G. (2012). Modifications of Xanthomonas axonopodis pv. citri lipopolysaccharide affect the basal response and the virulence process during citrus canker. PLoS One 7, e40051. 10.1371/journal.pone.0040051 PubMed DOI PMC
Petutschnig E., Jones A., Serazetdinova L., Lipka U., Lipka V. (2010). The Lysin Motif Receptor-like Kinase (LysM-RLK) CERK1 is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 285, 28902–28911. 10.1074/jbc.M110.116657 PubMed DOI PMC
Poinssot B. (2002). Caractérisation des réactions de défense de la vigne et identification d’éliciteurs: l’endopolygalacturonase 1 de Botrytis cinerea, une fonction d’avirulence pour un facteur de virulence. PhD Thesis. Dijon (F): Univ. Bourgogne.
Poinssot B., Vandelle E., Bentéjac M., Adrian M., Levis C., Brygoo Y., et al. (2003). The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol. Plant Microbe Interact. 16, 553–564. 10.1094/MPMI.2003.16.6.553 PubMed DOI
Poupin M. J., Timmermann T., Vega A., Zuñiga A., González B. (2013). Effects of the plant growth-promoting bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana . PLoS One 8, e69435. 10.1371/journal.pone.0069435 PubMed DOI PMC
Rabea E. I., Badawy M. E., Stevens C. V., Smagghe G., Steurbaut W. (2003). Chitosan as antimicrobial agent: applications and mode of action. Biomacromolecules 4, 1457–1465. 10.1021/bm034130m PubMed DOI
Ranf S., Gisch N., Schäffer M., Illig T., Westphal L., Knirel Y. A., et al. (2015). A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nat. Immunol. 16, 426–433. 10.1038/ni.3124 PubMed DOI
Ranf S., Scheel D., Lee J. (2016). Challenges in the identification of microbe-associated molecular patterns in plant and animal innate immunity: a case study with bacterial lipopolysaccharide. Mol. Plant Pathol. 17, 1165–1169. 10.1111/mpp.12452 PubMed DOI PMC
Rapicavoli J. N., Blanco-Ulate B., Muszyński A., Figueroa-Balderas R., Morales-Cruz A., Azadi P., et al. (2018). Lipopolysaccharide O-antigen delays plant innate immune recognition of Xylella fastidiosa. Nat. Commun. 9, 390. 10.1038/s41467-018-02861-5 PubMed DOI PMC
Rasul S., Dubreuil-Maurizi C., Lamotte O., Koen E., Poinssot B., Alcaraz G., et al. (2012). Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ. 35, 1483–1499. 10.1111/j.1365-3040.2012.02505.x PubMed DOI
Ren H., Endo H., Hayashi T. (2001). The superiority of organically cultivated vegetables to general ones regarding antimutagenic activities. Mutat. Res. 496, 83–88. 10.1016/S1383-5718(01)00229-7 PubMed DOI
Robatzek S., Bittel P., Chinchilla D., Kochner P., Felix G., Shiu S. H., et al. (2007). Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol. Biol. 64, 539–547. 10.1007/s11103-007-9173-8 PubMed DOI
Rosli H. G., Zheng Y., Pombo M. A., Zhong S., Bombarely A., Fei Z., et al. (2013). Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biol. 14, R139. 10.1186/gb-2013-14-12-r139 PubMed DOI PMC
Rotblat B., Enshell-Seijffers D., Gershoni J. M., Schuster S., Avni A. (2002). Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J. 32, 1049–1055. 10.1046/j.1365-313X.2002.01490.x PubMed DOI
Saintenac C., Lee W. S., Cambon F., Rudd J. J., King R. C., Marande W., et al. (2018). Wheat receptor-kinase-like protein Stb6 controls gene-for-gene resistance to fungal pathogen Zymoseptoria tritici. Nat. Genet. 50, 368–374. 10.1038/s41588-018-0051-x PubMed DOI
Sanchez L., Courteaux B., Hubert J., Kauffmann S., Renault J. H., Clément C., et al. (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. 10.1104/pp.112.201913 PubMed DOI PMC
Shang-Guan K., Wang M., Htwe N. M. P. S., Li P., Li Y., Qi F., et al. (2018). Lipopolysaccharides trigger two successive bursts of reactive oxygen species at distinct cellular locations. Plant Physiol. 176, 2543–2556. 10.1104/pp.17.01637 PubMed DOI PMC
Shimizu T., Nakano T., Takamizawa D., Desaki Y., Ishii-Minami N., Nishizawa Y., et al. (2010). Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204–214. 10.1111/j.1365-313X.2010.04324.x PubMed DOI PMC
Silipo A., Molinaro A., Sturiale L., Dow J. M., Erbs G., Lanzetta R., et al. (2005). The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestris. J. Biol. Chem. 280, 33660–33668. 10.1074/jbc.M506254200 PubMed DOI
Simpson S. D., Ashford D. A., Harvey D. J., Bowles D. J. (1998). Short chain oligogalacturonides induce ethylene production and expression of the gene encoding aminocyclopropane 1-carboxylic acid oxidase in tomato plants. Glycobiology 8, 579–583. 10.1093/glycob/8.6.579 PubMed DOI
Sivaguru M., Ezaki B., He Z. H., Tong H., Osawa H., Baluska F., et al. (2003). Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis . Plant Physiol. 132, 2256–2266. 10.1104/pp.103.022129 PubMed DOI PMC
Souza C. A., Li S., Lin A. Z., Boutrot F., Grossmann G., Zipfel C., et al. (2017). Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses. Plant Physiol. 173, 2383–2398. 10.1104/pp.16.01680 PubMed DOI PMC
Sun F., Zhang P., Guo M., Yu W., Chen K. (2013). Burdock fructooligosaccharide induces fungal resistance in postharvest Kyoho grapes by activating the salicylic acid-dependent pathway and inhibiting browning. Food Chem. 138, 539–546. 10.1016/j.foodchem.2012.10.058 PubMed DOI
Sun W., Dunning F., Pfund C., Weingarten R., Bent A. (2006). Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18, 764–779. 10.1105/tpc.105.037648 PubMed DOI PMC
Takai R., Isogai A., Takayama S., Che F. (2008). Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol. Plant-Microbe Interact. 21, 1635–1642. 10.1094/MPMI-21-12-1635 PubMed DOI
Takeda T., Furuta Y., Awano T., Mizuno K., Mitsuishi Y., Hayashi T. (2002). Suppression and acceleration of cell elongation by integration of xyloglucans in pea stem segments. Proc. Natl. Acad. Sci. U. S. A. 99, 9055–9060. 10.1073/pnas.132080299 PubMed DOI PMC
ten Have A., Breuil W. O., Wubben J. P., Visser J., van Kan J. A. (2001). Botrytis cinerea endopolygalacturonase genes are differentially expressed in various plant tissues. Fungal Genet. Biol. 33, 97–105. 10.1006/fgbi.2001.1269 PubMed DOI
ten Have A., Mulder W., Visser J., van Kan J. A. (1998). The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol. Plant Microbe Interact. 11, 1009–1016. 10.1094/MPMI.1998.11.10.1009 PubMed DOI
ten Have A., Tenberge K. B., Benen J. A. E., Tudzynski P., Visser J., van Kan J. A. L., (2002). “The contribution of cell wall degrading enzymes to pathogenesis of fungal plant pathogens,” in Agricultural Applications. Springer Berlin Heidelberg. Ed. Kempken F. (Berlin, Heidelberg: Springer; ), 341–358. 10.1007/978-3-662-03059-2_17 DOI
Theocharis A., Bordiec S., Fernandez O., Paquis S., Dhondt-Cordelier S., Baillieul F., et al. (2012). Burkholderia phytofirmans PsJN primes Vitis vinifera L. Mol. Plant-Microbe Interact. 25, 241–249. 10.1094/MPMI-05-11-0124 PubMed DOI
Tikhonov V. E., Stepnova E. A., Babak V. G., Yamskov I. A., Palma-Guerrero J., Jansson H.-B., et al. (2006). Bactericidal and antifungal activities of a low molecular weight chitosan and its N-/2(3)-(dodec-2-enyl)succinoyl/-derivatives. Carbohydr. Polym. 64, 66–72. 10.1016/j.carbpol.2005.10.021 DOI
Trdá L. (2014). Identification et caractérisation du récepteur à la flagelline (VvFLS2) et recherche du récepteur aux chito-oligosaccharides chez la vigne. Dijon (F): PhD Thesis Univ. Bourgogne.
Trdá L., Boutrot F., Claverie J., Brulé D., Dorey S., Poinssot B. (2015). Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline. Front. Plant Sci. 6, 219. 10.3389/fpls.2015.00219 PubMed DOI PMC
Trdá L., Fernandez O., Boutrot F., Héloir M. C., Kelloniemi J., Daire X., et al. (2014). The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol. 201, 1371–1384. 10.1111/nph.12592 PubMed DOI
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. 10.1007/s10658-006-0005-5 DOI
Trouvelot S., Héloir M. C., Poinssot B., Gauthier A., Paris F., Guillier C., et al. (2014). Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Front. Plant Sci. 5, 592. 10.3389/fpls.2014.00592 PubMed DOI PMC
Trouvelot S., Varnier A. L., Allègre M., Mercier L., Baillieul F., Arnould C., et al. (2008). A beta-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. 10.1094/MPMI-21-2-0232 PubMed DOI
van Aubel G., Buonatesta R., Van Cutsem P. (2014). COS-OGA: a novel oligosaccharidic elicitor that protects grapes and cucumbers against powdery mildew. Crop Prot. 65, 129–137. 10.1016/j.cropro.2014.07.015 DOI
van der Hoorn R. A., Kamoun S. (2008). From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20, 2009–2017. 10.1105/tpc.108.060194 PubMed DOI PMC
Vandelle E., Poinssot B., Wendehenne D., Bentejac M., Pugin A. (2006). Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kin in BcPG1-elicited grapevine defenses. Mol. Plant-Microbe Interact. 19, 429–440. 10.1094/MPMI-19-0429 PubMed DOI
Vargas-Rechia C., Reicher F., Rita Sierakowski M., Heyraud A., Driguez H., Linart Y. (1998). Xyloglucan octasaccharide XXLGol derived from the seeds of Hymenaea courbaril acts as a signaling molecule. Plant Physiol. 116, 1013–1021. 10.1104/pp.116.3.1013 PubMed DOI PMC
Varnier A. L., Sanchez L., Vatsa P., Boudesocque L., Garcia-Brugger A., Rabenoelina F., et al. (2009). Bacterial rhamnolipids are novel MAMPs conferring resistance to Botrytis cinerea in grapevine. Plant Cell Environ. 32, 178–193. 10.1111/j.1365-3040.2008.01911.x PubMed DOI
Vasiukova N. I., Zinov’eva S. V., Il’inskaia L. I., Perekhod E. A., Chalenko G. I., Gerasimova N. G., et al. (2001). Modulation of plant resistance to diseases by water-soluble chitosan. Prikl. Biokhim. Mikrobiol. 37, 115–122. PubMed
Vatsa P., Sanchez L., Clement 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. 10.3390/ijms11125095 PubMed DOI PMC
Vetter M., Kronholm I., He F., Haweker H., Reymond M., Bergelson J., et al. (2012). Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol. Biol. Evol. 29, 1655–1667. 10.1093/molbev/mss011 PubMed DOI
Wagner T. A., Kohorn B. D. (2001). Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13, 303–318. 10.1105/tpc.13.2.303 PubMed DOI PMC
Walters D. R., Fountaine J. M. (2009). Practical application of induced resistance to plant diseases: an appraisal of effectiveness under field conditions. J. Agric. Sci. 147, 523–535. 10.1017/S0021859609008806 DOI
Walters D. R., Ratsep J., Havis N. D. (2013). Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64, 1263–1280. 10.1093/jxb/ert026 PubMed DOI
Wan J., Zhang X., Neece D., Ramonell K., Clough S., Kim S., et al. (2008). A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis . Plant Cell 20, 471–481. 10.1105/tpc.107.056754 PubMed DOI PMC
Wang X., Tu M., Wang D., Liu J., Li Y., Li Z., et al. (2018). CRISPR/Cas9-mediated efficient targeted mutagenesis in grape in the first generation. Plant Biotechnol. J. 16, 844–855. 10.1111/pbi.12832 PubMed DOI PMC
Wendehenne D., Lamotte O., Frachisse J., Barbier-Brygoo H., Pugin A. (2002). Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell 14, 1937–1951. 10.1105/tpc.002295 PubMed DOI PMC
Whitney S. E., Wilson E., Webster J., Bacic A., Reid J. S., Gidley M. J. (2006). Effects of structural variation in xyloglucan polymers on interactions with bacterial cellulose. Am. J. Bot. 93, 1402–1414. 10.3732/ajb.93.10.1402 PubMed DOI
Wiesel L., Newton A. C., Elliott I., Booty D., Gilroy E. M., Birch P. R., et al. (2014). Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front. Plant Sci. 5, 655. 10.3389/fpls.2014.00655 PubMed DOI PMC
Yang P., Praz C., Li B., Singla J., Robert C. A. M., Kessel B., et al. (2019). Fungal resistance mediated by maize wall-associated kinase ZmWAK-RLK1 correlates with reduced benzoxazinoid content. New Phytol. 221, 976–987. 10.1111/nph.15419 PubMed DOI
Zeng W., He S. Y. (2010). A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol. 153, 1188–1198. 10.1104/pp.110.157016 PubMed DOI PMC
Zhang L., Kars I., Essenstam B., Liebrand T. W., Wagemakers L., Elberse J., et al. (2014). Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein responsiveness to Botrytis polygalacturonases1. Plant Physiol. 164, 352–364. 10.1104/pp.113.230698 PubMed DOI PMC
Zhang L., van Kan J. A. L. (2013). Pectin as a barrier and nutrient source for fungal plant pathogens. Agric. Appl. pp, 361–375. 10.1007/978-3-642-36821-9_14 DOI
Zhang N., Zhang B., Zuo W., Xing Y., Konlasuk S., Tan G., et al. (2017). Cytological and molecular characterization of ZmWAK-mediated head-smut resistance in maize. Mol. Plant Microbe Interact. 30, 455–465. 10.1094/MPMI-11-16-0238-R PubMed DOI
Zhang S., Chen C., Li L., Meng L., Singh J., Jiang N., et al. (2005). Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiol. 139, 1107–1124. 10.1104/pp.105.069005 PubMed DOI PMC
Zhang X., Zhou Y., Li Y., Fu X., Wang Q. (2017). Screening and characterization of endophytic Bacillus for biocontrol of grapevine downy mildew. Crop Prot. 96, 173–179. 10.1016/j.cropro.2017.02.018 DOI
Zipfel C., Robatzek S., Navarro L., Oakeley E. J., Jones J. D. G., Felix G., et al. (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767. 10.1038/nature02485 PubMed DOI
Zou Y., Wang S., Zhou Y., Bai J., Huang G., Liu X., et al. (2018). Transcriptional regulation of the immune receptor FLS2 controls the ontogeny of plant innate immunity. Plant Cell 30, 2779–2794. 10.1105/tpc.18.00297 PubMed DOI PMC
Zuniga A., Poupin M., Donoso R., Ledger T., Guiliani N., Gutierrez R., et al. (2013). Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol. Plant-Microbe Interact. 26, 546–553. 10.1094/MPMI-10-12-0241-R PubMed DOI
Zuo W., Chao Q., Zhang N., Ye J., Tan G., Li B., et al. (2015). A maize wall-associated kinase confers quantitative resistance to head smut. Nat. Genet. 47, 151–157. 10.1038/ng.3170 PubMed DOI