Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases

EMBO Journal

Volumn 21, Issue 24, 2002, Pages 6681-6688

  Brunner, Frédéric ^a   Rosahl, Sabine ^a   Lee, Justin ^a   Rudd, Jason J ^a   Geiler, Carola ^a   Kauppinen, Sakari ^b,c   Rasmussen, Grethe ^b   Scheel, Dierk ^a   Nürnberger, Thorsten ^a  

^a LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^b NOVOZYMES A S   (Denmark)

^c Exiqon AS   (Denmark)

Author keywords

Elicitor; Innate immunity; Pathogen associated molecular pattern; Phytophthora; Transglutaminase

Indexed keywords

FUNGAL PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN PEP 13; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; GENE ACTIVATION; GENE MUTATION; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNITY; NONHUMAN; PHYTOPHTHORA; POTATO; PRIORITY JOURNAL; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BLOTTING, NORTHERN; CONSERVED SEQUENCE; DNA MUTATIONAL ANALYSIS; DOSE-RESPONSE RELATIONSHIP, DRUG; MOLECULAR SEQUENCE DATA; MUTATION; PHYTOPHTHORA; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY, AMINO ACID; SOLANUM TUBEROSUM; TIME FACTORS; TRANSGLUTAMINASES;

ANIMALIA; FUNGI; PETROSELINUM CRISPUM; PHYTOPHTHORA; PHYTOPHTHORA SOJAE; SOLANUM TUBEROSUM;

EID: 0037121933     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf667     Document Type: Article

References (52)

1. Aderem, A. and Ulevitch, R. (2000) Toll-like receptors in the induction of the innate immune response. Nature, 406, 782-787.
2. Adini, A., Krugliak, M., Ginsburg, H., Li,L., Lavie, L. and Warburg, A. (2001) Transglutaminase in Plasmodium parasites: Activity and putative role in oocysts and blood stages. Mol. Biochem. Parasitol., 117, 161-168.
3. Aeschlimann, D. and Paulsson, M. (1994) Transglutaminases: Protein cross-linking enzymes in tissue and body fluids. Thromb. Haemost., 71, 402-415.
4. Ahvazi, B., Kim, H.C., Kee, S.H., Nemes, Z. and Steinert, P.M. (2002) Three-dimensional structure of the human transglutaminase 3 enzyme: Binding of calcium ions changes structure for activation. EMBO J., 21, 2055-2067.
5. Asai, T., Tena, G., Plotnikova, J., Willmann, M.R., Chiu, W.L., Gomez-Gomez, L., Boller, T., Ausubel, F.M. and Sheen, J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415, 977-983.
6. Blume, B., Nürnberger, T., Nass, N. and Scheel, D. (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell, 12, 1425-1440.
7. Boller, T. (1995) Chemoperception of microbial signals in plant cells. Annu. Rev. Plant Physiol. Plant Mol. Biol., 46, 189-214.
8. Cohn, J., Sessa, G. and Martin, G.B. (2001) Innate immunity in plants. Curr. Opin. Immunol., 13, 55-62.
9. Dalbøge, H. and Heldt-Hansen, H.P. (1994) A novel method for efficient expression cloning of fungal enzyme genes. Mol. Gen. Genet., 243, 253-260.
10. Dangl, J.L. and Jones, J.D.G. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
11. Dong, C., Davis, R.J. and Flavell, R.A. (2002) MAP kinases in the immune response. Annu. Rev. Immunol., 20, 55-72.
12. Dunsmuir, P., Bond, D., Lee, K.J., Gidoni, D. and Townsend, J. (1989) Stability of introduced genes and stability in expression. In Gelvin, S.B. and Schilperoort, R.A. (eds), Plant Molecular Biology Manual, Vol. 1. Kluwer Academic, Dordrecht, The Netherlands, pp. 1-17.
13. Eisenberg, D., Schwarz, E., Komarony, M. and Wall, R. (1984) Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol., 179, 125-142.
14. Erwin, D.C. and Ribeiro, O.K. (1996) Phytophthora Diseases Worldwide. The American Phytopathological Society Press, St Paul, MN.
15. Felix, G., Duran, J.D., Volko, S. and Boller, T. (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J., 18, 265-276.
16. Folk, J.E. (1980) Transglutaminases. Annu. Rev. Biochem., 49, 517-531.
17. Fuglsang, C.C., Berka, R.M., Wahleithner, J.A., Kauppinen, S., Shuster, J.R., Rasmussen, G., Halkier, T., Dalboge, H. and Henrissat, B. (2000) Biochemical analysis of recombinant fungal mutanases. A new family of α1.3-glucanases with novel carbohydrate-binding domains. J. Biol. Chem., 275, 2009-2018.
18. Göbel. C., Feussner, I., Schmidt, A., Scheel, D., Sanchez-Serrano, J.J., Hamberg, M. and Rosahl, S. (2001) Oxylipin profiling reveals the preferential stimulation of the 9-lipoxygenase pathway in elicitor-treated potato cells. J. Biol. Chem., 276, 6267-6273.
19. Gomez-Gomez, L. and Boller, T. (2000) FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell, 5, 1003-1011.
20. Govers, F. (2001) Misclassification of pest as 'fungus' puts vital research on wrong track. Nature, 411, 633.
21. Hahlbrock, K., Scheel, D., Logemann, E., Nürnberger, T., Parniske, M., Reinhold, S., Sacks, W.R. and Schmelzer, E. (1995) Oligopeptide elicitor-mediated defense gene activation in cultured parsley cells. Proc. Natl. Acad. Sci. USA, 92, 4150-4157.
22. Hayashi,F. et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature, 410, 1099-1103.
23. Heath, M. (2000) Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol., 3, 315-319.
24. Hoshino, K., Takeuchi, O., Kawai, T., Sanjo, H., Ogawa, T., Takeda, Y., Takeda, K. and Akira, S. (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J. Immunol., 162, 3749-3752.
25. Imler, J.-L. and Hoffmann, J.A. (2001) Toll receptors in innate immunity. Trends Cell Biol., 11, 304-311.
26. - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. USA, 94, 4800-4805.
27. Kamoun, S. (2001) Nonhost resistance to Phytophthora: Novel prospects for a classical problem. Curr. Opin. Plant Biol., 4, 295-300.
28. Kanaji, T., Ozaki, H., Takao, T., Kawajiri, H., Ide, H., Motoki, M. and Shimonishi, Y. (1993) Primary structure of microbial transglutaminase from Streptoverticillium sp. strain s-8112. J. Biol. Chem., 268, 11565-11572.
29. Kolomiets, M.V., Chen, H., Gladon, R.J., Brown, E.J. and Hannapel, D.J. (2000) A leaf lipoxygenase of potato induced specifically by pathogen infection. Plant Physiol., 124, 1121-1130.
30. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. and Hoffmann, J. (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell, 86, 973-983.
31. Ligterink, W., Kroj, T., zur Nieden, U., Hirt, H. and Scheel, D. (1997) Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science, 276, 2054-2057.
32. Liu, S., Cerione, R.A. and Clardy, J. (2002) Structural basis for the guanine nucleotide-binding activity of tissue transglutaminase and its regulation of transamidation activity. Proc. Natl. Acad. Sci. USA, 99, 2743-2747.
33. Medzhitov, R. and Janeway, C.A., Jr (1997) Innate immunity: The virtues of a nonclonal system of recognition. Cell, 91, 295-298.
34. Medzhitov, R., Preston-Hurlburt, P. and Janeway, C.A., Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature, 388, 323-324.
35. Melino, G. and Piacentini, M. (1998) Tissue transglutaminase in cell death: A downstream or multifunctional upstream effector? FEBS Lett., 430, 59-63.
36. Nennstiel, D., Scheel, D. and Nürnberger, T. (1998) Characterization and partial purification of an oligopeptide elicitor receptor from parsley (Petroselinum crispum). FEBS Lett., 431, 405-410.
37. Noguchi, K., Ishikawa, K., Yokoyama, K., Ohtsuka, T., Nio, N. and Suzuki, E. (2001) Crystal structure of red sea bream transglutaminase. J. Biol. Chem., 276, 12055-12059.
38. Nürnberger, T. and Brunner, F. (2002) Innate immunity in plants and animals: Emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr. Opin. Plant Biol., 5, 318-324.
39. Nürnberger, T. and Scheel, D. (2001) Signal transmission in the plant immune response. Trends Plant Sci., 6, 372-379.
40. Nürnberger, T., Nennstiel, D., Jabs, T., Sacks, W.R., Hahlbrock, K. and Scheel, D. (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell, 78, 449-460.
41. Ozinsky, A., Underhill, D.M., Fontenot, J.D., Hajjar, A.M., Smith, K.D., Wilson, C.B., Schroeder, L. and Aderem, A. (2000) The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA, 97, 13766-13771.
42. Parker, J.E., Schulte, W., Hahlbrock, K. and Scheel, D. (1991) An extracellular glycoprotein from Phytophthora megasperma f. sp. glycinea elicits phytoalexin synthesis in cultured parsley cells and protoplasts. Mol. Plant-Microbe Interact., 4, 19-27.
43. Poltorak, A. et al. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science, 282, 2085-2088.
44. Rohwer, F., Fritzemeier, K.H., Scheel, D. and Hahlbrock, K. (1987) Biochemical reactions of different tissue of potato (Solanum tuberosum) to zoospores or elicitors from Phytophthora infestans. Planta, 170, 556-561.
45. Rost, B. (1996) PredicProtein. Methods Enzymol., 266, 525-539.
46. Sacks, W.R., Nürnberger, T., Hahlbrock, K. and Scheel, D. (1995) Molecular characterization of nucleotide sequences encoding the extracellular glycoprotein elicitor from Phytophthora megasperma. Mol. Gen. Genet., 246, 45-55.
47. Slaughter, T.F., Achyuthan, K.E., Lai, T.-S. and Greenberg, C.S. (1992) A microtiter plate transglutaminase assay utilizing 5-(biotinamido) pentylamine as substrate. Anal. Biochem., 205, 166-171.
48. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796-815.
49. Tyler, B.M. (2002) Molecular basis of recognition between Phytophthora pathogens and their hosts. Annu. Rev. Phytopathol., 40, 137-167.
50. Underhill, D.M. and Ozinsky, A. (2002) Toll-like receptors: Key mediators of microbe detection. Curr. Opin. Immunol., 14, 103-110.
51. Usami, S., Banno, H., Ito, Y., Nishimama, R. and Machida, Y. (1995) Cutting activates a 46-kilodalton protein kinase in plants. Proc. Natl. Acad. Sci. USA, 92, 8660-8664.
52. 2+-permeable ion channel involved in pathogen defense. Proc. Natl. Acad. Sci. USA, 94, 2751-2755.