Secretion of a fungal extracellular catalase by Claviceps purpurea during infection of rye: Putative role in pathogenicity and suppression of host defense

Phytopathology

Volumn 88, Issue 8, 1998, Pages 744-753

  Garre, Victoriano ^a,b   Tenberge, Klaus B ^a   Eising, Rainer ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

Active oxygen species; Host pathogen interaction; Immunogold localization

Indexed keywords

AMINOTRIAZOLE; APOPLAST; CATALASE; CYTOLOGY; DIAMINOBENZIDINE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME INHIBITOR; EPITOPE; HOST RESISTANCE; HYDROGEN PEROXIDE; IMMUNOGOLD LABELING; MYCOSIS; PATHOGENICITY; PLANT PATHOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; RYE; SECRETION;

CLAVICEPS PURPUREA; FUNGI; SECALE CEREALE;

EID: 0031850140     PISSN: 0031949X     EISSN: None     Source Type: Journal    
DOI: 10.1094/PHYTO.1998.88.8.744     Document Type: Article

References (65)

1. Apostol, I., Heinstein, P. F., and Low, P. S. 1989. Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Role in defense and signal transduction. Plant Physiol. 90:109-116.
2. Bestwick, C. S., Brown, I. R., Bennett, M. H. R., and Mansfield, J. W. 1997. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9:209-221.
3. Bradley, D. J., Kjellbom, P., and Lamb, C. J. 1992. Elicitor-and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell 70:21-30.
4. Brisson, L. F., Tenhaken, R., and Lamb, C. 1994. Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703-1712.
5. Brockmann, B., Smit, R., and Tudzynski, P. 1992. Characterization of an extracellular β-1,3-glucanase of Claviceps purpurea. Physiol. Mol. Plant Pathol. 40:191-201.
6. Carpita, N. C., and Gibeaut, D. M. 1993. Structural models of primary cell walls in flowering plants: Consistency of molecular structure with the physical properties of the walls during growth. Plant J. 3:1-30.
7. Chaga, G. S., Medin, A. S., Chaga, S. G., and Porath, J. O. 1992. Isolation and characterization of catalase from Penicillium chrysogenum. J. Chromatogr. 604:177-183.
8. Chary, P., and Natvig, D. O. 1989. Evidence for three differentially regulated catalase genes in Neurospora crasser. Effects of oxidative stress, heat shock, and development. J. Bacteriol. 171:2646-2652.
9. Clare, D. A., Duong, M. N., Darr, D., Archibald, F., and Fridovich, I. 1984. Effects of molecular oxygen on detection of Superoxide radical with nitroblue tetrazolium and on activity stains for catalase. Anal. Biochem. 140:5332-5337.
10. Desikan, R., Hancock, J. T., Coffey, M. J., and Neill, S. J. 1996. Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS (Fed. Eur. Biochem. Soc.) Lett. 382:213-217.
11. Doke, N. 1983. Involvement of Superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with the incompatible race of Phytophthora infestans and to hyphal cell wall components. Physiol. Plant Pathol. 23:345-357.
12. Dumas, B., Freyssinet, G., and Pallett, K. E. 1995. Tissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiol. 107:1091-1096.
13. Eising, R., Kleff, S., Ruholl, C., and Tenberge, K. B. 1996. Turnover of catalase in sunflower cotyledons. Pages 45-60 in: Proc. Int. Compositae Conf., Kew, 1994, vol. 2, Compositae: Biology and Utilization, P. D. S. Caligari and D. J. N. Hind, eds. Royal Botanic Gardens, Kew, United Kingdom.
14. Feierabend, J., Schaan, C., and Hertwig, B. 1992. Photoinactivation of catalase occurs under both high-and low-temperature stress conditions and accompanies photoinhibition of photosystem II. Plant Physiol. 100:1554-1561.
15. Forney, L. J., Reddy, C. A., and Pankratz, H. S. 1982. Ultrastructural localization of hydrogen peroxide production in ligninolytic Phanerochaete chrysosporium cells. Appl. Environ. Microbiol. 44:732-736.
16. Fraaije, M. W., Roubroeks, H. P., Hagen, W. R., and van Berkel, J. H. 1996. Purification and characterization of an intracellular catalase-peroxidase from Penicillium simplicissimum. Eur. J. Biochem. 235: 192-198.
17. Frederick, S. E., and Newcomb, E. H. 1969. Cytochemical localization of catalase in leaf microbodies (peroxisomes). J. Cell Biol. 43:343-353.
18. Garre, V., Müller, U., and Tudzynski, P. 1998. Cloning, characterization and targeted disruption of cpcatl, coding for an in planta secreted catalase of Claviceps purpurea. Mol. Plant-Microbe Interact. 11:772-783.
19. Gerhardt, B. 1978. Microbodies/Peroxisomen pflanzlicher Zellen. Morphologie, Biochemie, Funktion und Entwicklung eines Zellorganells. With an English Assessment. Cell Biology Monographs, Vol. 5. Springer-Verlag, Vienna.
20. Grabber, J. H., Ralph, J., Hatfield, R. D., Quideau, S., Kuster, T., and Pell, A. N. 1996. Dehydrogenation polymer-cell wall complexes as a model for lignified grass walls. J. Agric. Food Chem. 44:1453-1459.
21. Hambrock, A. 1996. Untersuchungen über pflanzliche Abwehrreaktionen bei der Interaktion von Claviceps purpurea (Fr.) Tul. mit Secale cereale L. Licht-und elektronenmikroskopische sowie biochemische Analysen. Ph.D. thesis. Westf. Wilhelms-Universität Münster, Münster, Germany.
22. Hammond-Kosack, K. E., and Jones, J. D. G. 1996. Resistance gene-dependent plant defense responses. Plant Cell 8:1773-1791.
23. Havir, E. A. 1992. The in vivo and in vitro inhibition of catalase from leaves of Nicotiana sylvestris by 3-amino-l,2,4-triazole. Plant Physiol. 99:533-537.
24. Herzog, V., and Fahimi, H. D. 1974. The effect of glutaraldehyde on catalase. J. Cell Biol. 60:303-311.
25. Kohle, H., Young, D. H., and Kauss, H. 1984. Physiological changes in suspension-cultured soybean cells elicited by treatment with chitosan. Plant Sci. Lett. 33:221-230.
26. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583-593.
27. Levy, E., Eyal, Z., and Hochman, A. 1992. Purification and characterization of a catalase-peroxidase from the fungus Septoria tritici. Arch. Biochem. Biophys. 296:321-327.
28. Low, P. S., and Merida, J. R. 1996. The oxidative burst in plant defense: Function and signal transduction. Physiol. Plant. 96:533-542.
29. Mandell, G. L. 1975. Catalase, Superoxide dismutase, and virulence of Staphylococcus aureus. In vitro and in vivo studies with emphasis on staphylococcal-leucocyte interaction. J. Clin. Invest. 55:561-566.
30. Mantle, P. G., and Nisbet, L. J. 1976. Differentiation of Claviceps purpurea in axenic culture. J. Gen. Microbiol. 93:321-334.
31. Mauch-Mani, B., and Slusarenko, A. J. 1996. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203-212.
32. Mehdy, M. C. 1994, Active oxygen species in plant defense against pathogens. Plant Physiol. 105:467-472.
33. Moerschbacher, B. M., Noll, U., Gorrichon, L., and Reisener, H.-J. 1990. Specific inhibition of lignification breaks hypersensitive resistance of wheat to stem rust. Plant Physiol. 93:465-470.
34. Müller, U., Tenberge, K. B., Oeser, B., and Tudzynski, P. 1997. Cell, probably encoding a cellobiohydrolase lacking the substrate binding domain, is expressed in the initial infection phase of Claviceps purpurea on Secale cereale. Mol. Plant-Microbe Interact. 10:268-279.
35. Mussell, H. W. 1973. Endopolygalacturonase: Evidence for involvement in Verticillium wilt of cotton. Phytopathology 63:62-70.
36. Navarro, R. E., Stringer, M. A., Hansberg, W., Timberlake, W. E., and Aguirre, J. 1996. catA, a new Aspergillus nidulans gene encoding a developmentally regulated catalase. Curr. Genet. 29:352-359.
37. Olsen, P. D., and Varner, J. E. 1993. Hydrogen peroxide and lignification. Plant J. 4:887-892.
38. Otte, O., and Barz, W. 1996. The elicitor-induced oxidative burst in cultured chickpea cells drives the rapid insolubilization of two cell wall structural proteins. Planta 200:238-246.
39. Peng, M., and Kuc, J. 1992. Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks. Phytopathology 82:696-699.
40. Platford, R. G., and Bernier, C. C. 1970. Resistance to Claviceps purpurea in spring and durum wheat. Nature 226:770.
41. Purdue, P. E., and Lazarow, P. B. 1996. Targeting of human catalase to peroxisomes is dependent upon a novel COOH-terminal peroxisomal targeting sequence. J. Cell Biol. 134:849-862.
42. Robertson, E. F., Dannelly, H. K., Malloy, P. J., and Reeves, H. C. 1987. Rapid isoelectric focusing in a vertical polyacrylamide minigel system. Anal. Biochem. 167:290-294.
43. Sandstrom, P. A., and Buttke, T. M. 1993. Autocrine production of extracellular catalase prevents apoptosis of the human CEM T-cell line in serum-free medium. Proc. Natl. Acad. Sci. U.S.A. 90:4708-4712.
44. Scandalios, J. G. 1993. Oxygen stress and Superoxide dismutases. Plant Physiol. 101:7-12.
45. Sherwood, R. T., and Vance, C. P. 1980. Resistance to fungal penetration in Gramineae. Phytopathology 70:273-279.
46. +-ATPase activity in spores, germ tubes, and haustoria of the rust fungus Uromyces viciae-fabae. Fungal Genet. Biol. 20:30-35.
47. Susani, M., Zimniak, P., Fessl, F., and Ruis, H. 1976. Localization of catalase A in vacuoles of Saccharomyces cerevisiae: Evidence for the vacuolar nature of isolated "yeast peroxisomes." Hoppe-Seyler's Z. Physiol. Chem. 357:961-970.
48. Swan, D. J., and Mantle, P. G. 1991. Parasitic interactions between Claviceps purpurea strains in wheat and an acute necrotic host response. Mycol. Res. 95:807-810.
49. Tenberge, K. B. Biology and life strategy of ergot fungi. In: Medicinal & Aromatic Plants - Industrial Profiles, vol. Claviceps, R. Hardman, V. Kren, and L. Cvak, eds. Harwood Academic Publishers, Chur, Switzerland. In press.
50. Tenberge, K. B. 1997. Molekulare Cytologie der Claviceps-Secale-Interaktion. Habilitation thesis. Westfälische Wilhelms-Universität, Münster, Germany.
51. Tenberge, K. B., and Eising, R. 1995. Immunogold labelling indicates high catalase concentrations in amorphous and crystalline inclusions of sunflower (Helianthus annuus L.) peroxisomes. Histochem. J. 27:184-195.
52. Tenberge, K. B., Homann, V., Oeser, B., and Tudzynski, P. 1996. Structure and expression of two polygalacturonase genes of Claviceps purpurea oriented in tandem and cytological evidence for pectinolytic enzyme activity during infection of rye. Phytopathology 86:1084-1097.
53. Tenberge, K. B., Ruholl, C., Heinze, M., and Eising, R. 1997. Purification and immuno-electron microscopical characterization of crystalline inclusions from plant peroxisomes. Protoplasma 196:142-154.
54. Tenberge, K. B., and Tudzynski, P. 1995. Der Mutterkompilz Claviceps purpurea auf Roggen: Affinitätscytochemische Untersuchungen einer Wirt-Parasit-Beziehung. Phytomedizin 25(3):51-52.
55. Tenhaken, R., Levine, A., Brisson, L. F., Dixon, R. A., and Lamb, C. 1995. Function of the oxidative burst in hypersensitive disease resistance. Proc. Natl. Acad. Sci. U.S.A. 92:4158-4163.
56. Thieringer, R., Shio, H., Han, Y., Cohen, G., and Lazarow, P. B. 1991. Peroxisomes in Saccharomyces cerevisiae: Immunofluorescence analysis and import of catalase A into isolated peroxisomes. Mol. Cell Biol. 11:510-522.
57. Trelease, R. N., Xie, W., Lee, M. S., and Mullen, R. T. 1996. Rat liver catalase is sorted to peroxisomes by its C-terminal tripeptide Ala-Asn-Leu, not by the internal Ser-Lys-Leu motif. Eur. J. Cell Biol. 71:248-258.
58. Tudzynski, P. Genetics of Claviceps purpurea. In: Medicinal & Aromatic Plants - Industrial Profiles, vol. Claviceps. R. Hardman, V. Kren, and L. Cvak, eds. Harwood Academic Publishers, Chur, Switzerland. In press.
59. Tudzynski, P., Tenberge, K. B., and Oeser, B. 1995. Claviceps purpurea. Pages 161-187 in: Pathogenesis and Host Specificity in Plant Diseases: Histopathological, Biochemical, Genetic and Molecular Bases, vol. II, Eukaryotes. K. Kohmoto, U. S. Singh, and R. P. Singh, eds. Elsevier Science, Pergamon Press, Oxford.
60. Tudzynski, P., and Tudzynski, B. 1996. Genetics of phytopathogenic fungi. Prog. Bot. 57:235-252.
61. von Ossowski, I., Hausner, G., and Loewen, P. C. 1993. Molecular evolutionary analysis based on the amino acid sequence of catalase. J. Mol. Evol. 37:71-76.
62. Walton, J. D. 1994. Deconstructing the cell wall. Plant Physiol. 104: 1113-1118.
63. Witteveen, C. F. B., Veenhuis, M., and Visser, J. 1992. Localization of glucose oxidase and catalase activities in Aspergillus niger. Appl. Environ. Microbiol. 58:1190-1194.
64. 2-generating glucose oxidase in transgenic potato plants. Plant Cell 7:1357-1368.
65. 2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J. 8:139-145.