The sterol-binding activity of PATHOGENESIS-RELATED PROTEIN 1 reveals the mode of action of an antimicrobial protein

Plant Journal

Volumn 89, Issue 3, 2017, Pages 502-509

  Gamir, Jordi ^a   Darwiche, Rabih ^a   van't Hof, Pieter ^a   Choudhary, Vineet ^a,b   Stumpe, Michael ^a   Schneiter, Roger ^a   Mauch, Felix ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

antimicrobial protein; CAP protein; Phytophthora; plant immunity; PR 1; sterol binding

Indexed keywords

ALCOHOLS; BINDING SITES; BINS; BIOCHEMISTRY; MICROORGANISMS; PATHOGENS; PLANTS (BOTANY);

ANTIMICROBIAL PROTEINS; CAP PROTEINS; PHYTOPHTHORA; PLANT IMMUNITIES; STEROL BINDING;

PROTEINS;

BIOCHEMISTRY; PATHOGENS; PROTEINS;

ANTIINFECTIVE AGENT; CHOLESTEROL; PLANT PROTEIN; PROTEIN BINDING; STEROL;

DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOBLOTTING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PHYTOPHTHORA; PLANT; PLANT DISEASE; TOBACCO; TOMATO;

ANTI-INFECTIVE AGENTS; CHOLESTEROL; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; IMMUNOBLOTTING; LYCOPERSICON ESCULENTUM; PHYTOPHTHORA; PLANT DISEASES; PLANT PROTEINS; PLANTS; PROTEIN BINDING; STEROLS; TOBACCO;

EID: 85011693973     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13398     Document Type: Article

References (27)

1. Alexander, D., Goodman, R.M., Gut-Rella, M., Glascock, C., Weymann, K., Friedrich, L., Maddox, D., Ahl-Goy, P., Luntz, T. and Ward, E. (1993) Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesis-related protein 1a. Proc. Natl Acad. Sci. USA, 90, 7327–7331.
2. Asojo, O.A., Goud, G., Dhar, K., Loukas, A., Zhan, B., Deumic, V., Liu, S., Borgstahl, G.E. and Hotez, P.J. (2005) X-ray structure of Na-ASP-2, a pathogenesis-related-1 protein from the nematode parasite, Necator americanus, and a vaccine antigen for human hookworm infection. J. Mol. Biol. 346, 801–814.
3. Cantacessi, C., Campbell, B.E., Visser, A. et al. (2009) A portrait of the “SCP/TAPS” proteins of eukaryotes – developing a framework for fundamental research and biotechnological outcomes. Biotechnol. Adv. 27, 376–388.
4. Choudhary, V. and Schneiter, R. (2012) Pathogen-Related Yeast (PRY) proteins and members of the CAP superfamily are secreted sterol-binding proteins. Proc. Natl Acad. Sci. USA, 109, 16882–16887.
5. Cordier, C., Pozo, M.J., Barea, J.M., Gianinazzi, S. and Gianinazzi-Pearson, V. (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol. Microbe Interact. 11, 1017–1028.
6. Erwin, D.C. and Ribeiro, O.K. (1996) Culture, physiology, and genetics of Phytophthora species. In Phytophthora Diseases Worldwide (Erwin, D.C. and Ribeiro, O.K., eds). St Paul, Minesota: The American Phytopathological Society, pp. 42–95.
7. Fernández, C., Szyperski, T., Bruyère, T., Ramage, P., Mösinger, E. and Wüthrich, K. (1997) NMR solution structure of the pathogenesis-related protein P14a. J. Mol. Biol. 266, 576–593.
8. Gianinazzi, S., Martin, C. and Vallée, J.C. (1970) Hypersensibilité aux virus, température et protéines solubles chez le Nicotiana Xanthi n.c. Apparition de nouvelles macromolécules lors de la répression de la synthèse virale. C.R. Hebd. Seances Acad. Sci., Ser. D, Sci. Nat. D270, 2383–2386.
9. Gibbs, G.M., Roelants, K. and O'Bryan, M.K. (2008) The CAP superfamily: cysteine-rich secretory proteins, antigen 5, and pathogenesis-related 1 proteins–roles in reproduction, cancer, and immune defense. Endocr. Rev. 29, 865–897.
10. Gonzales, R.A. and Parks, L.W. (1981) Lack of specificity in accumulation of sterols by Phytophthora cactorum. Lipids, 16, 384–388.
11. Im, Y.J., Raychaudhuri, S., Prinz, W.A. and Hurley, J.H. (2005) Structural mechanism for sterol sensing and transport by OSBP-related proteins. Nature, 437, 154–158.
12. Kauffmann, S., Legrand, M., Geoffroy, P. and Fritig, B. (1987) Biological function of pathogenesis-related proteins: four PR proteins of tobacco have 1,3-beta-glucanase activity. EMBO J. 6, 3239–3212.
13. Kiba, A., Nishihara, M., Nakatsuka, T. and Yamamura, S. (2007) Pathogenesis-related protein 1 homologue is an antifungal protein in Wasabia japonica leaves and confers resistance to Botrytis cinerea in transgenic tobacco. Plant Biotech. 24, 247–253.
14. Legrand, M., Kauffmann, S., Geoffroy, P. and Fritig, B. (1987) Biological function of pathogenesis-related proteins: four tobacco pathogenesis-related proteins are chitinases. Proc. Natl Acad. Sci. USA, 84, 6750–6754.
15. Li, J., Du, L., Liu, X., Du, S., Huang, X. and Jiang, J. (2009) Expression and purification of tobacco PR-1a protein for function analysis. Asian J. Chem. 21, 3697–3707.
16. Lu, J., Robert, C.A., Riemann, M., Cosme, M., Mène-Saffrané, L., Massana, J., Stout, M.J., Lou, Y., Gershenzon, J. and Erb, M. (2015) Induced jasmonate signaling leads to contrasting effects on root damage and herbivore performance. Plant Physiol. 167, 1100–1116.
17. Mauch, F. and Staehelin, L.A. (1989) Functional implications of the subcellular localization of ethylene-induced chitinase and ß-1,3-glucanase in bean leaves. Plant Cell, 1, 447–457.
18. Nes, W.D. (1987) Biosynthesis and requirement for sterols in the growth and reproduction of Oomycetes. In Ecology and Metabolism of Plant Lipids (Fuller, G. and Nes, W.D., eds). Washington, DC: ACS Symposium Series; American Chemical Society, pp. 304–328.
19. Niderman, T., Genetet, I., Bruyère, T., Gees, R., Stintzi, A., Legrand, M., Fritig, B. and Mösinger, 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 Physiol. 108, 17–27.
20. Rauscher, M., Adám, A.L., Wirtz, S., Guggenheim, R., Mendgen, K. and Deising, H.B. (1999) PR-1 protein inhibits the differentiation of rust infection hyphae in leaves of acquired resistant broad bean. Plant J. 19, 625–633.
21. Roetschi, A., Si-Ammour, A., Belbahri, L., Mauch, F. and Mauch-Mani, B. (2001) Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J. 28, 293–305.
22. Serrano, R.L., Kuhn, A., Hendricks, A., Helms, J.B., Sinning, I. and Groves, M.R. (2004) Structural analysis of the human Golgi-associated plant pathogenesis related protein GAPR-1 implicates dimerization as a regulatory mechanism. J. Mol. Biol. 339, 173–183.
23. Szypersk, T., Fernandez, C., Mumenthaler, C. and Wüthrich, K. (1998) Structure comparison of human glioma pathogenesis-related protein GliPR and the plant pathogenesis-related protein P14a indicates a functional link between the human immune system and a plant defense system. Proc. Natl Acad. Sci. USA, 95, 2262–2266.
24. Van Loon, L.C. and Van Kammen, A. (1970) Polyacrylamide disk electrophoresis of the soluble proteins from Nicotiana tabacum var. Samsun and Samsun NN. II. Changes in protein constitution after infection with tobacco mosaic virus. Virology, 40, 190–211.
25. Van Loon, L.C. and Van Strien, E.A. (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55, 85–97.
26. Van Loon, L.C., Rep, M. and Pieterse, C.M. (2006) Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135–162.
27. Zhu, F., Xu, M., Wang, S., Jia, S., Zhang, P., Lin, H. and Xi, D. (2012) Prokaryotic expression of pathogenesis related protein 1 gene from Nicotiana benthamiana: antifungal activity and preparation of its polyclonal antibody. Biotechnol. Lett. 34, 919–924.