Biological effects of oomycetes elicitinsů M., Činčalová L., Luhová L., Lochman J., Petřivalský M. (2020): Biological effects of oomycetes elicitins. Plant Protect. Sci., 56: 1-8.
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Successful plant defence responses to pathogen challenges are based on fast and specific pathogen recognition and plant reaction mechanisms. Elicitins, proteinaceous elicitors secreted by the Phytophthora and Pythium species, were first described in Phytophthora culture filtrates as proteins able to induce a hypersensitive response (HR) and resistance in tobacco at low concentrations. Later, they were classified as microbial-associated molecular patterns (MAMPs) able to induce defences in a variety of plant species. In this review, we present a comprehensive summary of the actual knowledge on the representative elicitins and their structure, perception and activation of plant signalling pathways. The current research of elicitins has been focused on a detailed understanding of the molecular mechanisms of the elicitin recognition by plant cells. Moreover, the possibility of elicitin involvement in the establishment and enhancement of plant host resistance to a broad spectrum of pathogens has been intensively studied.

Akino S., Takemoto D., Hosaka K. (2014): Phytophthora infestans: A review of past and current studies on potato late blight. Journal of General Plant Pathology, 80: 24–37.
Attard A., Gourgues M., Galiana E., Panabières F., Ponchet M., Keller H. (2008): Strategies of attack and defense in plant-oomycete interactions, accentuated for Phytophthora parasitica Dastur (syn. P. nicotianae Breda de Haan). Journal of Plant Physiology, 165: 83–94.
Benhamou N., Bélanger R.R., Rey P., Tirilly Y. (2001): Oligandrin, the elicitin-like protein produced by the mycoparasite Pythium oligandrum, induces systemic resistance to Fusarium crown and root rot in tomato plants. Plant Physiology and Biochemistry, 39: 681–696.
Blein J.P., Coutos-Thévenot P., Marion D., Ponchet M. (2002): From elicitins to lipid-transfer proteins: A new insight in cell signalling involved in plant defence mechanisms. Trends in Plant Science, 7: 293–296.
Boissy G., De La Fortelle E., Kahn R., Huet J.C., Bricogne G., Pernollet J.C., Brunie S. (1996): Crystal structure of a fungal elicitor secreted by Phytophthora cryptogea, a member of a novel class of plant necrotic proteins. Structure, 4: 1429–1439.
Boissy G., O'Donohue M., Gaudemer O., Perez V., Pernollet J.C., Brunie S. (1999): The 2.1 A structure of an elicitin-ergosterol complex: a recent addition to the Sterol Carrier Protein family. Protein Science, 8: 1191–1199.
Bourque S., Dutartre A., Hammoudi V., Blanc S., Dahan J., Jeandroz S., Pichereaux C., Rossignol M., Wendehenne D. (2011): Type-2 histone deacetylases as new regulators of elicitor-induced cell death in plants. New Phytologist, 192: 127–139.
Chaparro-Garcia A., Wilkinson R.C., Gimenez-Ibanez S., Findlay K., Coffey M.D., Zipfel C., Rathjen J.P., Kamoun S., Schornack S. (2011): The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS ONE, 6(1): e16608. doi: 10.1371/journal.pone.0016608
Chaparro-Garcia A., Schwizer S., Sklenar J., Yoshida K., Petre B., Bos J.I.B., Schornack S., Jones A.M.E., Bozkurt T.O., Kamoun S. (2015): Phytophthora infestans RXLR-WY effector AVR3a associates with dynamin-related protein 2 required for endocytosis of the plant pattern recognition receptor FLS2. PLoS ONE: 10(9): e0137071. doi: 10.1371/journal.pone.0137071
Colas V., Conrod S., Venard P., Keller H., Ricci P., Panabieres F. (2001): Elicitin genes expressed in vitro by certain tobacco isolates of Phytophthora parasitica are down regulated during compatible interactions. Molecular Plant-Microbe Interactions, 14: 326–335.
Dalio R.J.D., Magãlhaes D.M., Rodrigues C.M., Arena G.D., Oliveira T.S., Souza-Neto R.R., Picchi S.C., Martins P.M.M., Santos P.J.C., Maximo H.J., Pacheco I., De Souza A., Machado M. (2017): PAMPs, PRRs, effectors and R-genes associated with citrus-pathogen interactions. Annals of Botany, 119: 749–774.
Derevnina L., Dagdas Y.F., De la Concepcion J.C., Bialas A., Kellner R., Petre B., Domazakis E., Du J., Wu C.H., Lin X., Aguilera-Galvez C., Cruz-Mireles N., Vleeshouwers V.G.A.A, Kamoun S. (2016): Nine things to know about elicitins. New Phytologist, 212: 888–895.
Devergne J.-C., Bonnet P., Panabières F., Blein J.-P., Ricci P. (1992): Migration of the fungal protein cryptogein within tobacco plants. Plant Physiology, 99: 843–847.
Dokládal L., Obořil M., Stejskal K., Zdráhal Z., Ptáčková N., Chaloupková R., Damborský J., Kašparovský T., Jeandroz S., Žďárská M., Lochman J. (2012): Physiological and proteomic approaches to evaluate the role of sterol binding in elicitin-induced resistance. Journal of Experimental Botany, 63: 2203–2215.
Domazakis E., Wouters D., Visser R.G.F., Kamoun S., Joosten M.H.A.J., Vleeshouwers V.G.A.A. (2018): The ELR-SOBIR1 complex functions as a two-component receptor-like kinase to mount defense against Phytophthora infestans. Molecular Plant-Microbe Interactions, 31: 795–802.
Du J., Verzaux E., Chaparro-Garcia A., Bijsterbosch G., Keizer L.C., Zhou J., Liebrand T.W., Xie C., Govers F., Robatzek S. (2015): Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants, 1: 15034. doi: 10.1038/nplants.2015.34
Fefeu S., Bouaziz S., Huet J.C., Pernollet J.C., Guittet E. (1997): Three-dimensional solution structure of beta cryptogein, a beta elicitin secreted by a phytopathogenic fungus Phytophthora cryptogea. Protein Science: A Publication of the Protein Society, 6: 2279–2284.
Gooley P.R., Keniry M.A., Dimitrov R.A., Marsh D.E., Keizer D.W., Gayler K.R., Grant B.R. (1998): The NMR solution structure and characterization of pH dependent chemical shifts of the beta-elicitin, cryptogein. Journal of Biomolecular NMR, 12: 523–534.
Heese A., Hann D.R., Gimenez-Ibanez S., Jones A.M.E., He K., Li J., Schroeder J.I., Peck S.C., Rathjen J.P. (2007): The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proceedings of the National Academy of Sciences, 104: 12217–12222.
Hendrix J.W. (1970): Sterols in growth and reproduction of fungi. Annual Review of Phytopathology, 8: 111–130.
Jiang R.H.Y., Tyler B.M., Whisson S.C., Hardham A.R., Govers F. (2006): Ancient origin of elicitin gene clusters in Phytophthora genomes. Molecular Biology and Evolution, 23: 338–351.
Jones J.D.G., Dangl J.L. (2006): The plant immune system. Nature, 444: 323–329.
Kamoun S., Young M., Glasscock C., Tyler B.M. (1993): Extracellular protein elicitors from Phytophthora: Host-specificity and induction of resistance to bacterial and fungal phytopathogens. Molecular Plant-Microbe Interactions, 6: 15–25.
Kamoun S., van West P., de Jong A.J., de Groot K.E., Vleeshouwers V.G.A.A., Govers, F. (1997): A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Molecular Plant-Microbe Interactions, 10: 13–20.
Kawamura Y., Hase S., Takenaka S., Kanayama Y., Yoshioka H., Kamoun S., Takahashi H. (2009): INF1 elicitin activates jasmonic acid- and ethylene-mediated signalling pathways and induces resistance to bacterial wilt disease in tomato. Journal of Phytopathology, 157: 287–297.
Keller H., Bonnet P., Galiana E., Pruvot L., Friedrich L., Ryals J., Ricci P. (1996): Salicylic acid mediates elicitin-induced systemic acquired resistance, but not necrosis in tobacco. Molecular Plant-Microbe Interactions, 9: 696–703.
Kulik A., Noirot E., Grandperret V., Bourque S., Fromentin J., Salloignon P., Truntzer C., Dobrowolska G., Simon-Plas F., Wendehenne D. (2015): Interplays between nitric oxide and reactive oxygen species in cryptogein signalling. Plant, Cell and Environment, 38: 331–348.
Lecourieux-Ouaked F., Pugin A., Lebrun-Garcia A. (2000): Phosphoproteins involved in the signal transduction of cryptogein, an elicitor of defense reactions in tobacco. Molecular Plant-Microbe Interactions, 13: 821–829.
Mikeš V., Milat M-L., Ponchet M., Ricci P., Blein J-P. (1997) The fungal elicitor cryptogein is a sterol carrier protein. FEBS Letters, 416: 190–192
Noirot E., Der C., Lherminier J., Robert F., Moricová P., Kiêu K., Leborgne-Castel N., Simon-Plas F., Bouhidel K. (2014): Dynamic changes in the subcellular distribution of the tobacco ROS-producing enzyme RBOHD in response to the oomycete elicitor cryptogein. Journal of Experimental Botany, 65: 5011–5022.
O’Donohue M.J., Gousseau H., Huet J.C., Tepfer D., Pernollet J.C. (1995): Chemical synthesis, expression and mutagenesis of a gene encoding β-cryptogein, an elicitin produced by Phytophthora cryptogea. Plant Molecular Biology, 27: 577–586.
Osman H., Vauthrin S., Mikeš V., Milat M.L., Panabières F., Marais A., Brunie S., Maume B., Ponchet M., Blein J.P. (2001): Mediation of elicitin activity on tobacco is assumed by elicitin-sterol complexes. Molecular Biology of the Cell, 12: 2825–2834.
Ouyang Z., Li X., Huang L., Hong Y., Zhang Y., Zhang H., Li D., Song F. (2015): Elicitin-like proteins Oli-D1 and Oli-D2 from Pythium oligandrum trigger hypersensitive response in Nicotiana benthamiana and induce resistance against Botrytis cinerea in tomato. Molecular Plant Pathology, 16: 238–250.
Panabières F., Birch P.R.J., Unkles S.E., Ponchet M., Lacourt I., Venard P., Keller H., Allasia V., Ricci P., Duncan J.M. (1997): Heterologous expression of a basic elicitin from Phytophthora cryptogea in Phytophthora infestans increases its ability to cause leaf necrosis in tobacco. Microbiology, 144: 3343–3349.
Peng K., Wang C., Wu C., Huang C., Liou R.-F. (2015): Tomato SOBIR1/EVR homologs are involved in elicitin perception and plant defense against the oomycete pathogen Phytophthora parasitica. Molecular Plant Microbe Interactions, 28: 913–926.
Picard K., Ponchet M., Blein J.-P.P., Rey P., Tirilly Y., Benhamou N. (2000). Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrum induces resistance to Phytophthora parasitica infection in tomato plants. Plant Physiology, 124: 379–395.
Plešková V., Kašparovský T., Obořil M., Ptáčková N., Chaloupková R., Ladislav D., Damborský J., Lochman J. (2011): Elicitin-membrane interaction is driven by a positive charge on the protein surface: Role of Lys13 residue in lipids loading and resistance induction. Plant Physiology and Biochemistry, 49: 321–328.
Ponchet M., Panabières F., Milat M.L., Mikeš V., Montillet J.L., Suty L., Triantaphylides C., Tirilly Y., Blein J.P. (1999): Are elicitins cryptograms in plant-oomycete communications? Cellular and Molecular Life Sciences, 56: 1020–1047.
Pugin A., Frachisse J.M., Tavernier E., Bligny R., Gout E., Douce R., Guern J. (1997): Early events induced by the elicitor cryptogein in tobacco cells: Involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. The Plant Cell, 9: 2077–2091.
Ricci P., Bonnet P., Huet J.-C., Sallantin M., Beuvais-Cante F., Bruneteau M., Billard V., Michel G., Pernollet J.-C. (1989): Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. European Journal of Biochemistry, 183: 555–563.
Sandor R., Der C., Grosjean K., Anca I., Noirot E., Leborgne-Castel N., Lochman J., Simon-Plas F., Gerbeau-Pissot P. (2016): Plasma membrane order and fluidity are diversely triggered by elicitors of plant defence. Journal of Experimental Botany, 67: 5173–5185.
Satková P., Starý T., Plešková V., Zapletalová M., Kašparovský T., Činčalová-Kubienová L., Luhová L., Mieslerová B., Mikulík J., Lochman, J., Petřivalský M. (2017): Diverse responses of wild and cultivated tomato to BABA, oligandrin and Oidium neolycopersici infection. Annals of Botany, 119: 829–840.
Stanislas T., Bouyssie D., Rossignol M., Vesa S., Fromentin J., Morel J., Pichereaux C., Monsarrat B., Simon-Plas F. (2009): Quantitative proteomics reveals a dynamic association of proteins to detergent-resistant membranes upon elicitor signaling in tobacco. Molecular & Cellular Proteomics, 8: 2186–2198.
Starý T., Satková P., Piterková J., Mieslerová B., Luhová L., Mikulík J., Kašparovský T., Petřivalský M., Lochman J. (2018): The elicitin β-cryptogein’s activity in tomato is mediated by jasmonic acid and ethylene signalling pathways independently of elicitin–sterol interactions. Planta, 249: 739–749.
Takenaka S., Nakamura Y., Kono T., Sekiguchi H., Masunaka A., Takahashi H. (2006): Novel elicitin-like proteins isolated from the cell wall of the biocontrol agent Pythium oligandrum induce defence-related genes in sugar beet. Molecular Plant Pathology, 7: 325–339.
Uhlíková H., Obořil M., Klempová J., Šedo O., Zdráhal Z., Kašparovský T., Skládal P., Lochman J. (2016): Elicitin-induced distal systemic resistance in plants is mediated through the protein-protein interactions influenced by selected lysine residues. Frontiers in Plant Science, 7: 59.
Vleeshouwers V.G.A.A., Driesprong J.D., Kamphuis L.G., Torto-Alalibo T., Van’T Slot K.A.E., Govers F., Visser R.G.F., Jacobsen E., Kamoun S. (2006): Agroinfection-based high-throughput screening reveals specific recognition of INF elicitins in Solanum. Molecular Plant Pathology, 7: 499–510.
Wendehenne D., Lamotte O., Frachisse J.M., 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.
Xu J., Yang K.Y., Yoo S.J., Liu Y., Ren D., Zhang S. (2014): Reactive oxygen species in signalling the transcriptional activation of WIPK expression in tobacco. Plant, Cell and Environment, 37: 1614–1625.
Yamamoto-Katou A., Katou S., Yoshioka H., Doke N., Kawakita K. (2006): Nitrate reductase is responsible for elicitin-induced nitric oxide production in Nicotiana benthamiana. Plant and Cell Physiology, 47: 726–735.
Yu L.M. (1995): Elicitins from Phytophthora and basic resistance in tobacco. Proceedings of the National Academy of Sciences USA, 92: 4088–4094.
Yun B-W., Feechan A., Yin M., Saidi N.B.B., Le Bihan T., Yu M., Moore J.W., Kang J-G., Kwon E., Spoel S.H. (2011): S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature, 478: 264–268.
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