PR1-mediated defence via C-terminal peptide release is targeted by a fungal pathogen effector.
Parastagonospora nodorum
CAPE1
Septoria nodorum blotch
SnTox3
effector-triggered susceptibility
pathogenesis-related 1 (PR-1)
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
received:
23
07
2020
accepted:
24
11
2020
pubmed:
6
12
2020
medline:
15
5
2021
entrez:
5
12
2020
Statut:
ppublish
Résumé
The effector SnTox3 from Parastagonospora nodorum elicits a strong necrotic response in susceptible wheat and also interacts with wheat pathogenesis-related protein 1 (TaPR-1), although the function of this interaction in disease is unclear. Here, we dissect TaPR1 function by studying SnTox3-TaPR1 interaction and demonstrate the dual functionality of SnTox3. We utilized site-directed mutagenesis to identify an SnTox3 variant, SnTox3
Substances chimiques
Fungal Proteins
0
Peptides
0
Plant Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3467-3480Informations de copyright
© 2020 The Authors New Phytologist © 2020 New Phytologist Trust.
Références
Almagro Armenteros JJ, Tsirigos KD, Sonderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H. 2019. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nature Biotechnology 37: 420-423.
Bartels S, Lori M, Mbengue M, van Verk M, Klauser D, Hander T, Boni R, Robatzek S, Boller T. 2013. The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. Journal of Experimental Botany 64: 5309-5321.
Breen S, Williams SJ, Outram M, Kobe B, Solomon PS. 2017. Emerging insights into the functions of pathogenesis-related protein 1. Trends in Plant Science 22: 871-879.
Breen S, Williams SJ, Winterberg B, Kobe B, Solomon PS. 2016. Wheat PR-1 proteins are targeted by necrotrophic pathogen effector proteins. The Plant Journal 88: 13-25.
Chen YL, Lee CY, Cheng KT, Chang WH, Huang RN, Nam HG, Chen YR. 2014. Quantitative peptidomics study reveals that a wound-induced peptide from PR-1 regulates immune signaling in tomato. The Plant Cell 26: 4135-4148.
Chien PS, Nam HG, Chen YR. 2015. A salt-regulated peptide derived from the CAP superfamily protein negatively regulates salt-stress tolerance in Arabidopsis. Journal of Experimental Botany 66: 5301-5313.
Eschenfeldt WH, Lucy S, Millard CS, Joachimiak A, Mark ID. 2009. A family of LIC vectors for high-throughput cloning and purification of proteins. Methods in Molecular Biology 498: 105-115.
Gamir J, Darwiche R, van't Hof P, Choudhary V, Stumpe M, Schneiter R, Mauch F. 2017. The sterol-binding activity of PATHOGENESIS-RELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein. The Plant Journal 89: 502-509.
Hander T, Fernandez-Fernandez AD, Kumpf RP, Willems P, Schatowitz H, Rombaut D, Staes A, Nolf J, Pottie R, Yao P et al. 2019. Damage on plants activates Ca2+-dependent metacaspases for release of immunomodulatory peptides. Science 363: eaar7486.
Huffaker A, Pearce G, Ryan CA. 2006. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proceedings of the National Academy of Sciences, USA 103: 10098-10103.
Jones J, Dangl J. 2006. The plant immune system. Nature 444: 323-329.
Lincoln JE, Sanchez JP, Zumstein K, Gilchrist DG. 2018. Plant and animal PR1 family members inhibit programmed cell death and suppress bacterial pathogens in plant tissues. Molecular Plant Pathology 19: 2111-2123.
Liu Z, Faris JD, Oliver RP, Tan KC, Solomon PS, McDonald MC, McDonald BA, Nunez A, Lu S, Rasmussen JB et al. 2009. SnTox3 acts in effector triggered susceptibility to induce disease on wheat carrying the Snn3 gene. PLoS Pathogens 5: e1000581.
Liu Z, Gao Y, Kim YM, Faris JD, Shelver WL, de Wit PJ, Xu SS, Friesen TL. 2016. SnTox1, a Parastagonospora nodorum necrotrophic effector, is a dual-function protein that facilitates infection while protecting from wheat-produced chitinases. New Phytologist 211: 1052-1064.
Liu Z, Zhang Z, Faris JD, Oliver RP, Syme R, McDonald MC, McDonald BA, Solomon PS, Lu S, Shelver WL et al. 2012. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS Pathogens 8: e1002467.
Lobstein J, Emrich CA, Jeans C, Faulkner M, Riggs P, Berkmen M. 2012. SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm. Microbial Cell Factories 11: 56.
Lu S, Faris JD, Sherwood R, Friesen TL, Edwards MC. 2014. A dimeric PR-1-type pathogenesis-related protein interacts with ToxA and potentially mediates ToxA-induced necrosis in sensitive wheat. Molecular Plant Pathology 15: 650-663.
McDonald MC, Solomon PS. 2018. Just the surface: advances in the discovery and characterization of necrotrophic wheat effectors. Current Opinion in Microbiology 46: 14-18.
Niderman T, Genetet I, Bruyere T, Gees R, Stintzi A, Legrand M, Fritig B, Mosinger E. 1995. Pathogenesis-related PR-1 proteins are antifungal. Isolation and characterization of three 14-kilodalton proteins of tomato and of a basic PR-1 of tobacco with inhibitory activity against Phytophthora infestans. Plant Physiology 108: 17-27.
O'Leary BM, Rico A, McCraw S, Fones HN, Preston GM. 2014. The infiltration-centrifugation technique for extraction of apoplastic fluid from plant leaves using Phaseolus vulgaris as an example. Journal of Visualized Experiments 19: 52113.
Oliver RP, Friesen TL, Faris JD, Solomon PS. 2012. Stagonospora nodorum: from pathology to genomics and host resistance. Annual Review of Phytopathology 50: 23-43.
Oliver RP, Solomon PS. 2010. New developments in pathogenicity and virulence of necrotrophs. Current Opinion in Microbiology 13: 415-419.
Outram MA, Sung Y, Yu D, Dagvadorj B, Rima SA, Jones D, Ericsson D, Sperschneider J, Solomon PS, Kobe Bet al. 2020. The crystal structure of SnTox3 from the necrotrophic fungus Parastagonospora nodorum reveals a unique effector fold and insights into Kex2 protease processing of fungal effectors. bioRxiv. doi: 10.1101/2020.05.27.120113.
Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nature Protocols 1: 2856-2860.
Tang J, Han Z, Sun Y, Zhang H, Gong X, Chai J. 2015. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Research 25: 110-120.
Tyanova S, Temu T, Cox J. 2016. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nature Protocols 11: 2301-2319.
van Loon LC, Rep M, Pieterse CM. 2006. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44: 135-162.
Van Loon LC, Van Kammen A. 1970. Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. "Samsun" and "Samsun NN". II. Changes in protein constitution after infection with tobacco mosaic virus. Virology 40: 190-211.
Van Loon LC, Van Strien EA. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 55: 85-97.
Wiedemann C, Bellstedt P, Gorlach M. 2013. CAPITO-a web server-based analysis and plotting tool for circular dichroism data. Bioinformatics 29: 1750-1757.
Woloshuk CP, Meulenhoff JS, Sela-Buurlage M, van den Elzen PJ, Cornelissen BJ. 1991. Pathogen-induced proteins with inhibitory activity toward Phytophthora infestans. The Plant Cell 3: 619-628.
Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. 2010. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. The Plant Cell 22: 508-522.
Yang G, Tang L, Gong Y, Xie J, Fu Y, Jiang D, Li G, Collinge DB, Chen W, Cheng J. 2018. A cerato-platanin protein SsCP1 targets plant PR1 and contributes to virulence of Sclerotinia sclerotiorum. New Phytologist 217: 739-755.
Zhang WJ, Pedersen C, Kwaaitaal M, Gregersen PL, Morch SM, Hanisch S, Kristensen A, Fuglsang AT, Collinge DB, Thordal-Christensen H. 2012. Interaction of barley powdery mildew effector candidate CSEP0055 with the defence protein PR17c. Molecular Plant Pathology 13: 1110-1119.
Zhang X, Nguyen N, Breen S, Outram MA, Dodds PN, Kobe B, Solomon PS, Williams SJ. 2017. Production of small cysteine-rich effector proteins in Escherichia coli for structural and functional studies. Molecular Plant Pathology 18: 141-151.
Ziemann S, van der Linde K, Lahrmann U, Acar B, Kaschani F, Colby T, Kaiser M, Ding Y, Schmelz E, Huffaker A et al. 2018. An apoplastic peptide activates salicylic acid signalling in maize. Nature Plants 4: 172-180.