Biological effects of oomycetes elicitins

https://doi.org/10.17221/21/2019-PPSCitation:Janků M., Činčalová L., Luhová L., Lochman J., Petřivalský M. (2020): Biological effects of oomycetes elicitins. Plant Protect. Sci., 56: 1-8.
download PDF

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.

References:
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. https://doi.org/10.1007/s10327-013-0495-x
 
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. https://doi.org/10.1016/j.jplph.2007.06.011
 
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. https://doi.org/10.1016/S0981-9428(01)01283-9
 
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. https://doi.org/10.1016/S1360-1385(02)02284-7
 
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. https://doi.org/10.1016/S0969-2126(96)00150-5
 
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. https://doi.org/10.1110/ps.8.6.1191
 
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. https://doi.org/10.1111/j.1469-8137.2011.03788.x
 
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 https://doi.org/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 https://doi.org/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. https://doi.org/10.1094/MPMI.2001.14.3.326
 
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. https://doi.org/10.1111/nph.14137
 
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. https://doi.org/10.1104/pp.99.3.843
 
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. https://doi.org/10.1093/jxb/err427
 
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. https://doi.org/10.1094/MPMI-09-17-0217-R
 
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 https://doi.org/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. https://doi.org/10.1002/pro.5560061101
 
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. https://doi.org/10.1023/A:1008395001008
 
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. https://doi.org/10.1073/pnas.0705306104
 
Hendrix J.W. (1970): Sterols in growth and reproduction of fungi. Annual Review of Phytopathology, 8: 111–130. https://doi.org/10.1146/annurev.py.08.090170.000551
 
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. https://doi.org/10.1093/molbev/msj039
 
Jones J.D.G., Dangl J.L. (2006): The plant immune system. Nature, 444: 323–329. https://doi.org/10.1038/nature05286
 
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. https://doi.org/10.1094/MPMI-6-015
 
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. https://doi.org/10.1094/MPMI.1997.10.1.13
 
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. https://doi.org/10.1111/j.1439-0434.2008.01489.x
 
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. https://doi.org/10.1094/MPMI-9-0696
 
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. https://doi.org/10.1111/pce.12295
 
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. https://doi.org/10.1094/MPMI.2000.13.8.821
 
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 https://doi.org/10.1016/S0014-5793(97)01193-9
 
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. https://doi.org/10.1093/jxb/eru265
 
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. https://doi.org/10.1007/BF00019323
 
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. https://doi.org/10.1091/mbc.12.9.2825
 
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. https://doi.org/10.1111/mpp.12176
 
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. https://doi.org/10.1099/00221287-144-12-3343
 
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. https://doi.org/10.1094/MPMI-12-14-0405-R
 
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. https://doi.org/10.1016/j.plaphy.2011.01.008
 
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. https://doi.org/10.1007/s000180050491
 
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. https://doi.org/10.2307/3870566
 
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. https://doi.org/10.1111/j.1432-1033.1989.tb21084.x
 
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. https://doi.org/10.1093/jxb/erw284
 
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. https://doi.org/10.1007/s00425-018-3036-1
 
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. https://doi.org/10.1111/j.1364-3703.2006.00340.x
 
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. https://doi.org/10.3389/fpls.2016.00059
 
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. https://doi.org/10.1111/j.1364-3703.2006.00355.x
 
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. https://doi.org/10.1105/tpc.002295
 
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. https://doi.org/10.1111/pce.12271
 
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. https://doi.org/10.1093/pcp/pcj044
 
Yu L.M. (1995): Elicitins from Phytophthora and basic resistance in tobacco. Proceedings of the National Academy of Sciences USA, 92: 4088–4094. https://doi.org/10.1073/pnas.92.10.4088
 
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. https://doi.org/10.1038/nature10427
 
download PDF

© 2020 Czech Academy of Agricultural Sciences