Functional analysis of the Nep1-like proteins from Plasmopara viticola

References

• Dodds P, Rathjen J. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet. 2010;11:539–12. doi:10.1038/nrg2812.
   PubMed Web of Science ®Google Scholar
• Katagiri F, Tsuda K. Understanding the plant immune system. Mol Plant Microbe Interact. 2010;23(12):1531–1536. doi:10.1094/MPMI-04-10-0099.
   PubMed Web of Science ®Google Scholar
• Thomma BPHJ, Nürnberger T, Joosten MHAJ. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell. 2011;23(1):4–15. doi:10.1105/tpc.110.082602.
   PubMed Web of Science ®Google Scholar
• Bigeard J, Colcombet J, Hirt H. Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant. 2015;8(4):521–539. doi:10.1016/j.molp.2014.12.022.
   PubMed Web of Science ®Google Scholar
• Zipfel C. Plant pattern-recognition receptors. Trends Immunol. 2014;35(7):345–351. doi:10.1016/j.it.2014.05.004.
   PubMed Web of Science ®Google Scholar
• Felix G, Duran JD, Volko S, Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant Journal. 1999;18(3):265–276. doi:10.1046/j.1365-313X.1999.00265.x.
   PubMed Web of Science ®Google Scholar
• Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell. 2004;16(12):3496–3507. doi:10.1105/tpc.104.026765.
   PubMed Web of Science ®Google Scholar
• Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, Kemmerling B, Götz F, Glawischnig E, Lee J, Felix G, et al. Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in arabidopsis. Journal Biol Chem. 2007;282(44):32338. doi:10.1074/jbc.M704886200.
   PubMed Web of Science ®Google Scholar
• Gijzen M, Nürnberger T. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry. 2006;67(16):1800–1807. doi:10.1016/j.phytochem.2005.12.008.
   PubMed Web of Science ®Google Scholar
• Oome S, Raaymakers TM, Cabral A, Samwel S, Böhm H, Albert I, Nürnberger T, Van Den Ackerveken G. Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis. Proc Natl Acad, U S A. 2014;111(47):16955–16960. doi:10.1073/pnas.1410031111.
   PubMed Web of Science ®Google Scholar
• Böhm H, Albert I, Oome S, Raaymakers TM, Van Den Ackerveken G, Nürnberger T, Birch P. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis. PLoS Pathog. 2014;10(11):e1004491. doi:10.1371/journal.ppat.1004491.
   PubMed Web of Science ®Google Scholar
• Bailey BA. Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. Phytopathology. 1995;85(10):1250–1255. doi:10.1094/Phyto-85-1250.
   Web of Science ®Google Scholar
• Fellbrich G, Blume B, Brunner F, Hirt H, Kroj T, Ligterink W, Romanski A, Nurnberger T. Phytophthora parasitica elicitor-induced reactions in cells of petroselinum crispum. Plant Cell Physiol. 2000;41(6):692–701. doi:10.1093/pcp/41.6.692.
   PubMed Web of Science ®Google Scholar
• Fellbrich G, Romanski A, Varet A, Blume B, Brunner F, Engelhardt S, Felix G, Kemmerling B, Krzymowska M, Nürnberger T. NPP1, a Phytophthora‐ associated trigger of plant defense in parsley and Arabidopsis. Plant J. 2002;32(3):375–390. doi:10.1046/j.1365-313X.2002.01454.x.
   PubMed Web of Science ®Google Scholar
• Bae H, Kim MS, Sicher RC, Bae HJ, Bailey BA. Necrosis- and ethylene-inducing peptide from Fusarium oxysporum induces a complex cascade of transcripts associated with signal transduction and cell death in Arabidopsis. Plant Physiol. 2006;141(3):1056–1067. doi:10.1104/pp.106.076869.
   PubMed Web of Science ®Google Scholar
• Kamoun SA. Catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol. 2006;44(1):41–60. doi:10.1146/annurev.phyto.44.070505.143436.
   PubMedGoogle Scholar
• Pemberton CL, Salmond GP. The Nep1-like proteins-a growing family of microbial elicitors of plant necrosis. Mol Plant Pathol. 2004;5(4):353–359. doi:10.1111/j.1364-3703.2004.00235.x.
   PubMed Web of Science ®Google Scholar
• Oome S. Van den Ackerveken G. Comparative and functional analysis of the widely occurring family of Nep1-Like proteins. Mol Plant Microbe Interact. 2014;27(10):1081–1094. doi:10.1094/MPMI-04-14-0118-R.
   PubMed Web of Science ®Google Scholar
• Cabral A, Oome S, Sander N, Küfner I, Nürnberger T, Van Den Ackerveken G. Nontoxic Nep1-like proteins of the downy mildew pathogen Hyaloperonospora arabidopsidis: repression of necrosis-inducing activity by a surface-exposed region. Mol Plant-Microbe Interact. 2012;25(5):697–708. doi:10.1094/MPMI-10-11-0269.
   PubMed Web of Science ®Google Scholar
• Motteram J, Küfner I, Deller S, Brunner F, Hammond-Kosack KE, Nürnberger T, Rudd JJ. Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain-containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola. Mol Plant Microbe Interact. 2009;22(7):790–799. doi:10.1094/MPMI-22-7-0790.
   PubMed Web of Science ®Google Scholar
• Dong S, Kong G, Qutob D. The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol Plant Microbe Interact. 2012;25(7):896–909. doi:10.1094/MPMI-01-12-0023-R.
   PubMed Web of Science ®Google Scholar
• Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009;60(1):379. doi:10.1146/annurev.arplant.57.032905.105346.
   PubMed Web of Science ®Google Scholar
• Qutob D, Kemmerling B, Brunner F, Kufner I, Engelhardt S, Gust AA, Luberacki B, Seitz HU, Stahl D, Rauhut T. Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell. 2006;18(12):3721–3744. doi:10.1105/tpc.106.044180.
   PubMed Web of Science ®Google Scholar
• Staats M, van Baarlen P, Schouten A, van Kan JA. Functional analysis of NLP genes from Botrytis elliptica. Mol Plant Pathol. 2007;8(2):209–214. doi:10.1111/j.1364-3703.2007.00382.x.
   PubMed Web of Science ®Google Scholar
• Küfner I, Ottmann C, Nürnberger T, Oecking C. Cytolytic toxins as triggers of plant immune response. Plant Signal Behav. 2009;4(10):977–979. doi:10.4161/psb.4.10.9669.
   PubMedGoogle Scholar
• Fang YL, Peng YL, Fan J. The Nep1-like protein family of Magnaporthe oryzae is dispensable for the infection of rice plants. Sci Rep. 2017;7(1):4372. doi:10.1038/s41598-017-04430-0.
   PubMedGoogle Scholar
• Zhou BJ, Jia PS, Gao F, Guo HS. Molecular characterization and functional analysis of a necrosis- and ethylene-inducing, protein-encoding gene family from Verticillium dahliae. Molecular Plant-microbe Interactions. 2012;25(7):964. doi:10.1094/MPMI-12-11-0319.
   PubMed Web of Science ®Google Scholar
• Kanneganti TD, Huitema E, Cakir C, Kamoun S. Synergistic interactions of the plant cell death pathways induced by Phytophthora infestans Nep1-like protein PiNPP1.1 and INF1 elicitin. Molecular Plant-microbe Interactions. 2006;19(8):854–863. doi:10.1094/MPMI-19-0854.
   PubMed Web of Science ®Google Scholar
• Qutob D, Kamoun S, Gijzen M. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant Journal. 2002;32(3):361–373. doi:10.1046/j.1365-313X.2002.01439.x.
   PubMed Web of Science ®Google Scholar
• Amsellem Z, Cohen BA, Gressel J. Engineering hypervirulence in a mycoherbicidal fungus for efficient weed control. Nat Biotechnol. 2002;20(10):1035–1039. doi:10.1038/nbt743.
   PubMed Web of Science ®Google Scholar
• Ottmann C, Luberacki B, Kufner I, Koch W, Brunner F, Weyand M, Mattinen L, Pirhonen M, Anderluh G, Seitz HU. A common toxin fold mediates microbial attack and plant defense. Proceedings of the National Academy of Sciences. 2009;106(25):10359–10364. doi:10.1073/pnas.0902362106.
   PubMed Web of Science ®Google Scholar
• Pemberton CL, Whitehead NA, Sebaihia M, Bell KS, Hyman LJ, Harris SJ, Matlin AJ, Robson ND, Birch PRJ, Carr JP. Novel quorum-sensing-controlled genes in Erwinia carotovora subsp. carotovora: identification of a fungal elicitor homologue in a soft-rotting bacterium. Molecular Plant-microbe Interactions. 2005;18(4):343–353. doi:10.1094/MPMI-18-0343.
   PubMed Web of Science ®Google Scholar
• Yin L, Li XL, Xiang J, Qu JJ, Zhang YL, Dry IB, Lu J. Characterization of the secretome of Plasmopara viticola by de novo transcriptome analysis. Physiol Mol Plant Pathol. 2015;91:1–10. doi:10.1016/j.pmpp.2015.05.002.
   Web of Science ®Google Scholar
• Yin L, An YH, Qu JJ, Li XL, Zhang YL, Dry IB, Wu H, Lu J. Genome sequence of Plasmopara viticola and insight into the pathogenic mechanism. Sci Rep. 2017;7:1–12.
   PubMed Web of Science ®Google Scholar
• Xiang J, Li XL, Wu J, Yin L, Zhang YL, Lu J. Studying the mechanism of Plasmopara viticola RxLR effectors on suppressing plant immunity. Front Microbiol. 2016;7:709. doi:10.3389/fmicb.2016.00709.
   PubMed Web of Science ®Google Scholar
• Lan X, Liu Y, Song S, Yin L, Xiang J, Qu J, Lu J. Plasmopara viticola effector PvRXLR131 suppresses plant immunity by targeting plant receptor-like kinase inhibitor BKI1. Mol Plant Pathol. 2019;20(6):765–783. doi:10.1111/mpp.12790.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar
• Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–425.
   PubMed Web of Science ®Google Scholar
• Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol. 2000;42(6):819–832. doi:10.1023/A:1006496308160.
   PubMed Web of Science ®Google Scholar
• Zhang M, Meng Y, Wang Q, Liu D, Quan J, Hardham AR, Shan W. PnPMA1, an atypical plasma membrane H+-ATPase, is required for zoospore development in Phytophthora parasitica. Fungal Biol. 2012;116(9):1013–1023. doi:10.1016/j.funbio.2012.07.006.
   PubMed Web of Science ®Google Scholar
• Xiang J, Li XL, Yin L, Liu YX, Zhang YL, Qu JJ, Lu J. A candidate RxLR effector from Plasmopara viticola can elicit immune responses in Nicotiana benthamiana. BMC Plant Biol. 2017;17(1):1–14. doi:10.1186/s12870-017-1016-4.
   PubMedGoogle Scholar
• Yu X, Tang J, Wang Q, Ye W, Tao K, Duan S, Lu C, Yang X, Dong S, Zheng X, et al. The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol. 2012;196(1):247–260. doi:10.1111/j.1469-8137.2012.04241.x.
   PubMed Web of Science ®Google Scholar
• Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium‐mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735–743. doi:10.1046/j.1365-313x.1998.00343.x.
   PubMed Web of Science ®Google Scholar
• Schumacher S, Grosser K, Voegele RT, Kassemeyer HH, Fuchs R. Identification and characterization of Nep1-like proteins from the grapevine downy mildew pathogen Plasmopara viticola. Front Plant Sci. 2020;11:65. doi:10.3389/fpls.2020.00065.
   PubMed Web of Science ®Google Scholar
• Schouten A, Van Baarlen P, Van Kan JA. Phytotoxic Nep1‐like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytol. 2008;177(2):493–505. doi:10.1111/j.1469-8137.2007.02274.x.
   PubMed Web of Science ®Google Scholar
• Kamoun S, Van West P, Vleeshouwers VG, De Groot KE, Govers F. Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell. 1998;10(9):1413–1425. doi:10.1105/tpc.10.9.1413.
   PubMed Web of Science ®Google Scholar
• Villela‐Dias C, Camillo LR, de Oliveira GA, Sena JAL, Santiago AS, de Sousa STP, Mendes JS, Pirovani CP, Alvim FC, Costa MGC. Nep1-like protein from Moniliophthora perniciosa induces a rapid proteome and metabolome reprogramming in cells of Nicotiana benthamiana. Physiol Plant. 2014;150(1):1–17. doi:10.1111/ppl.12061.
   PubMed Web of Science ®Google Scholar
• Teh CY, Pang CL, Tor XY, Ho PY, Lim YY, Namasivayam P, Ho CL. Molecular cloning and functional analysis of a necrosis and ethylene inducing protein (NEP) from Ganoderma boninense. Physiol Mol Plant Pathol. 2019;106:42–48. doi:10.1016/j.pmpp.2018.12.003.
   Web of Science ®Google Scholar
• Bolton MD. Primary metabolism and plant defense—fuel for the fire. Molecular Plant-microbe Interactions. 2009;22(5):487–497. doi:10.1094/MPMI-22-5-0487.
   PubMed Web of Science ®Google Scholar
• Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol. 2005;43:205–227. doi:10.1146/annurev.phyto.43.040204.135923.
   PubMed Web of Science ®Google Scholar
• Lee S, Ishiga Y, Clermont K, Mysore KS. Coronatine inhibits stomatal closure and delays hypersensitive response cell death induced by nonhost bacterial pathogens. PeerJ 2013;1:e34. doi:10.7717/peerj.34.
   PubMed Web of Science ®Google Scholar
• Mattinen L, Tshuikina M, Mae A, Pirhonen M. Identification and characterization of Nip, necrosis-inducing virulence protein of Erwinia carotovora subsp. carotovora. Mol Plant Microbe Interact. 2004;17(12):1366–1375. doi:10.1094/MPMI.2004.17.12.1366.
   PubMed Web of Science ®Google Scholar
• Arenas YC, Kalkman ERIC, Schouten A, Dieho M, Vredenbregt P, Uwumukiza B, Ruiz MO, van Kan JAL. Functional analysis and mode of action of phytotoxic Nep1-like proteins of Botrytis cinerea. Physiol Mol Plant Pathol. 2010;74(5–6):376–386. doi:10.1016/j.pmpp.2010.06.003.
   Web of Science ®Google Scholar
• Feng BZ, Zhu XP, Fu L, Lv RF, Storey D, Tooley P, Zhang XG. Characterization of necrosis-inducing NLP proteins in Phytophthora capsici. BMC Plant Biol. 2004;14:1–19.
   Google Scholar
• Chen XR, Xing YP, Li YP, Tong YH, Xu JY. RNA-Seq reveals infection-related gene expression changes in Phytophthora capsici. PLoS One. 2013;8(9):e74588. doi:10.1371/journal.pone.0074588.
   PubMed Web of Science ®Google Scholar
• Newman MA, Sundelin T, Nielsen JT, Erbs G. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci. 2013;4:139. doi:10.3389/fpls.2013.00139.
   PubMed Web of Science ®Google Scholar
• Baroncelli R, Amby DB, Zapparata A, Sarrocco S, Vannacci G, Le Floch G, Harrison RJ, Holub E, Sukno SA, Sreenivasaprasad S. Gene family expansions and contractions are associated with host range in plant pathogens of the genus Colletotrichum. BMC Genomics. 2016;17(1):555. doi:10.1186/s12864-016-2917-6.
   PubMedGoogle Scholar