Characterization of SNP1, a cell wall-degrading trypsin, produced during infection by Stagonospora nodorum

Molecular Plant-Microbe Interactions

Volumn 13, Issue 5, 2000, Pages 538-550

  Carlile, A J ^a   Bindschedler, L V ^a   Bailey, A M ^b   Bowyer, P ^c   Clarkson, J M ^a   Cooper, R M ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

Cell wall proteins; Plant pathogen; Virulence

Indexed keywords

AMINO TERMINAL SEQUENCE; CELL WALL; CELL WALL DEGRADATION; DEGRADATION; DNA FRAGMENT; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME STRUCTURE; FUNGAL INFECTION; HYDROXYPROLINE; MOLECULAR WEIGHT; PH; SNP1 ENZYME; TRYPSIN; WHEAT;

EMBRYOPHYTA; PHAEOSPHAERIA NODORUM; SEPTORIA; STAGONOSPORA; STAGONOSPORA NODORUM; TRITICUM AESTIVUM;

EID: 0034000036     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2000.13.5.538     Document Type: Article

References (71)

1. Abraham, L. D., and Breuil, C. 1996. Isolation and characterisation of a subtilisin-like serine proteinase secreted by the sap-staining fungus Ophiostoma piceae. Enzyme Microb. Technol. 18:133-140.
2. Akashi, T., and Shibaoka, H. 1991. Involvement of transmembrane proteins in the association of cortical microtubules with the plasma membrane in tobacco BY-2 cells. J. Cell Sci. 98:169-174.
3. Ball, A. M., Ashby, A. M., Daniels, M. J., Ingram, D. S., and Johnstone, K. 1991. Evidence for the requirement of extracellular protease in the pathogenic interaction of Pyrenopeziza brassicae with oilseed rape. Physiol. Mol. Plant Pathol. 38:147-161.
4. Baker, C. S., and Mock, N. M. 1994. An improved method for monitoring cell death in cell suspension and leaf disc assays using Evans blue. Plant Cell Organ Cult. 39:7-12.
5. Bird, P. M., and Ride, J. P. 1981. The resistance of wheat to Septoria nodorum: fungal development in relation to host lignification. Physiol. Plant Pathol. 19:289-299.
6. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
7. 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.
8. Clarke, J. A., Lisker, N., Lamport, D. T. A., and Ellingboe, A. M. 1981. Hydroxyproline enhancement as a primary event in the successful development of Erysiphe graminis in wheat. Plant Physiol. 67:188-189.
9. Cooley, R. N., and Caten, C. E. 1993. Molecular analysis of the Septoria nodorum β-tubulin gene and characterisation of a benomyl-resistance mutation. Mol. Gen. Genet. 237:58-64.
10. Cooley, R. N., Shaw, R. K., Franklin, F. C. H., and Caten, C. E. 1988 Transformation of the phytopathogenic fungus Septoria nodorum to hygromycin B resistance. Curr. Genet. 13:383-389.
11. Cooper, R. M., Longman, D., Campbell, A., Henry, M., and Lees, P. E. 1988. Enzymic adaptation of cereal pathogens to the monocotyledonous primary wall. Physiol. Mol. Plant Pathol. 32:33-47.
12. Cornish-Bowden, A., and Eisenthal, R. 1974. Statistical considerations in the estimation of enzyme kinetic parameters by the direct linear plot and other methods. Biochem. J. 139:721.
13. D'Silva, I., Poirier, G. G., and Heath, M. M. 1998. Activation of cysteine proteases in cowpea plants during the hypersensitive response-a form of programmed cell death. Exp. Cell Res. 245:389-399.
14. Dahler, G. S., Barras, F., and Keen, N. T. 1990. Cloning of genes encoding extracellular metalloproteases from Erwinia chrysanthemi EC16. J. Bacteriol. 172:5803-5815.
15. Devereux, J., Haeberli, P., and Smithies, A. K. 1984. A comprehensive set of sequence analysis programs for VAX. Nucleic Acids Res. 12: 387-395.
16. Dow, J. M., Clarke, B. R., Milligan, D. E., Tang, J. L., and Daniels, M. J. 1990. Extracellular proteases from Xanthomonas campestris pv. campestris, the black rot pathogen. Appl. Environ. Microbiol. 56:2994-2998.
17. Dow, J. M., Davies, H. A., and Daniels, M. J. 1998. A metalloprotease from Xanthomonas campestris that specifically degrades proline/ hydroxyproline-rich glycoproteins of the plant extracellular matrix. Mol. Plant-Microbe Interact. 11:1085-1093.
18. Gebhard, W., Tschesche, H., and Frits, H. 1986. Biochemistry of aprotinin and aprotinin-like inhibitors. Pages 375-388 in: Proteinase Inhibitors. A. J. Barrett and G. Slavesen, eds. Elsevier Science, Amsterdam.
19. Hall, N., Keon, J. P. R., and Hargreaves, J. A. 1999. A homologue of a gene implicated in the virulence of human fungal disease is present in a plant fungal pathogen and is expressed during infection. Physiol. Mol. Plant Pathol. 55:69-73.
20. Heilbronn, J. Johnstone, D. J., Dunbar, B., and Lyon, G. D. 1995. Purification of a metalloprotease produced by Erwinia carotovora subsp. carotovora and the degradation of the potato lectin in vitro. Physiol. Mol. Plant Pathol. 47:285-292.
21. Hellmich, S., and Schauz, K. 1988. Production of extracellular alkaline and neutral proteases of Ustilago maydis. Exp. Mycol. 12:223-232.
22. Howard, S. P., and Buckley, J. T. 1985. Activation of the hole-forming toxin aerolysin by extracellular processing. J. Bacteriol. 163:336-340.
23. Joshi, B. N., Sainani, M. N., Bastawade, K. B., Gupta, V. S., and Ranjekar, P. K. 1998. Cysteine protease inhibitor from pearl millet: A new class of antifungal protein. Biochem. Biophys. Res. Commun. 246: 382-387.
24. Karjalainen, R., and Lounatmaa, K. 1986. Ultrastructure of penetration and colonisation of wheat leaves by Septoria nodorum. Physiol. Mol. Plant Pathol. 29:263-270.
25. Kieliszewski, M. J., Leykam, J. F., and Lamport, D. T. A. 1989. Trypsin cleaves lysylproline in a hydroxyproline-rich glycoprotein from Zea mays. Peptide Res. 2:246-248.
26. King, J. E., Cook, R. J., and Melville, S. C. 1983 A review of Septoria diseases of wheat and barley. Ann. Appl. Biol. 103:345-373.
27. Kivirikko, K. I., and Liesmaa, M. 1959. A colorimetric method for determination of hydroxyproline in tissue hydrolysates. Scand. J. Clin. Lab. Invest. 11:128-133.
28. Koiwa, H., Bressan, R. A., and Hasegawa, P. M. 1997. Regulation of protease inhibitors and plant defence. Trends Plant Sci. 2:379-384.
29. Kraut, J. 1977. Serine proteases: Structure and mechanisms of catalysis. Annu. Rev. Biochem. 46:331-358.
30. Laemmli, E. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
31. Lamport, D. T. A., and Miller, D. H. 1971. Hydroxyproline arabinosides in the plant kingdom. Plant Physiol. 48:454-456.
32. Lehtinen, U. 1993. Plant cell wall degrading enzymes of Septoria nodorum. Physiol. Mol. Plant Pathol. 43:121-134.
33. Lindstrom, J. T., and Belanger, F. C. 1994. Purification and characterisation of an endophytic fungal proteinase that is abundantly expressed in the infected host grass. Plant Physiol. 106:7-16.
34. Lorito, M., Broadway, R. M., Hayes, C. K., Woo, S. L., Noviello, C., Williams, D. L., and Harman, G. E. 1994. Proteinase inhibitors from plants as a novel class of fungicides. Mol. Plant-Microbe Interact. 7: 525-527.
35. Lusso, M., and Kuc, J. 1995. Increased activities of ribonuclease and protease after challenge in tobacco plants with induced systemic resistance. Physiol. Mol. Plant Pathol. 47:419-428.
36. Magro, P. 1984. Production of polysaccharide-degrading enzymes by Septoria nodorum in culture and during pathogenesis. Plant Sci. Lett. 37: 63-68.
37. Mauch, F., Mauch-Mani, B., and Boller, T. 1988. Antifungal hydrolases in pea tissue. II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase. Plant Physiol. 88:936-942.
38. Mazau, D., and Esquerré-Tugayé, M. T. 1986. Hydroxyproline-rich glycoprotein accumulation in the cell walls of plants infected by various pathogens. Physiol. Mol. Plant Pathol. 29:147-157.
39. Movahedi, S., and Heale, J. B. 1990a. Purification and characterisation of an aspartic proteinase secreted by Botrytis cinerea Pers ex. Pers in culture and in infected carrots. Physiol. Mol. Plant Pathol. 36:289-302.
40. Movahedi, S., and Heale, J. B. 1990b. The roles of aspartic proteinase and endo-pectin lyase enzymes in the primary stages of infection and pathogenesis of the various host tissues by different isolates of Botrytis cinerea Pers ex. Pers. Physiol. Mol. Plant Pathol. 36:303-324.
41. Murphy, J. M., and Walton, J. D. 1996. Three extracellular proteases from Cochliobolus carbonum: Cloning and targeted disruption of ALP1. Mol. Plant-Microbe Interact. 9:290-297.
42. Neurath, H. 1984. Evolution of proteolytic enzymes. Science 224:350-357.
43. Newton, A. C., and Caten, C. E. 1988. Auxotrophic mutants of Septoria nodorum isolated by direct screening and by selection for resistance to chlorate. Trans. Br. Mycol. Soc. 90:99-207.
44. Osbourn, A. E., Scott, P. R., and Caten, C. E. 1986. The effect of host passaging on the adaptation of Septoria nodorum to wheat or barley. Plant Pathol. 35:135-145.
45. Packman, L. C. 1993. Protein chemical methods for molecular biologists. Methods Mol. Cell. Biol. 4:189-198.
46. Powers, J. C., and Harper, E. A. 1986. Inhibitors of serine proteases. Pages 55-152 in: Proteinase Inhibitors. A. J. Barrett and G. Slavesen, eds. Elsevier Science, Amsterdam.
47. Punt, P. J., Oliver, R. P., Dingemanse, M. A., Pouwels, P. H., and van den Hondel, C. A. M. J. J. 1987. Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56:117-124.
48. Raeder, U., and Broda, P. 1985. Rapid preparation of DNA from filamentous fungi. Lett. Appl. Microbiol. 1:17-20.
49. Raucher, M., Mendgen, K., and Deising, H. 1995. Extracellular proteases of the rust fungus Uromyces viciae-fabae. Exp. Mycol. 19:26-34.
50. Raz, R., Crétin, C., Puigdomenech, D., and Martinez-Izquierd, J. A. 1991. The sequence of a hydroxyproline-rich glycoprotein gene from Sorghum vulgare. Plant Mol. Biol. 16:365-367.
51. Ries, S. M., and Albersheim, P. 1973. Purification of a protease secreted by Colletotrichum lindemuthianum. Phytopathology 63:625-629.
52. Robertson, B. 1984. An alkaline extracellular protease produced by Cladosporium cucumerinum and its possible importance in the development of scab disease of cucumber seedlings. Physiol. Plant Pathol. 24:83-92.
53. Rypniewski, W. R., Hastrup, S., Betzel, C., Dauter, M., Dauter, Z., Papendorf, G., Branner, S., and Wilson, K. S. 1993. The sequence and X-ray structure of the trypsin from Fusarium oxysporum. Protein Eng. 6:341-348.
54. Rypniewski, W. R., Perrakis, A., Vorgias, C. E., and Wilson, K. S. 1994. Evolutionary divergence and conservation of trypsin. Protein Eng. 7: 57-64.
55. Showalter, A. M. 1993. Structure and function of plant cell wall proteins. Plant Cell 2:1191-1200.
56. Sieber, T. 1989. Substrate utilization patterns of endophytic fungi of wheat seeds. J. Plant Dis. Prot. 96:627-632.
57. Smith, J. J., Muldoon, E. P., Willard, J. J., and Lamport, D. T. A. 1986. Tomato extensin precursors p1 and p2 are highly periodic structures. Phytochemistry 25:1021-1030.
58. Smithson, S. L., Paterson, I. C., Bailey, A. M., Screen, S. E., Hunt, B. A., Cobb, B. D., Cooper, R. M., Charnley, A. K., and Clarkson, J. M. 1995. Cloning and characterisation of a gene encoding a cuticle-degrading protease from the insect pathogenic fungus Metarhizium anisopliae. Gene 166:161-165.
59. Spellig, T., Bottin, A., and Kahmann, R. 1996. Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252:503-509.
60. Sreedhar, L., Kobayashi, D. Y., Bunting, T. E., Hillman, B. I., and Belanger, F. C. 1999 Fungal protease expression in the interaction of the plant pathogen Magnaporthe poae with its host. Gene 235:121-129.
61. Steitz, T. A., and Shulman, R. G. 1982. Crystallographic and NMR studies of the serine proteases. Annu. Rev. Biochem. Biophys. 11: 419-444.
62. Stevens, C., Titarenko, E., Hargreaves, J. A., and Gurr, S. J. 1996. Defence-related gene activation during an incompatible interaction between Stagonospora (Septoria) nodorum and barley (Hordeum vulgare L.) coleoptile cells. Plant Mol. Biol. 31:741-749.
63. St. Leger, R. J., Joshi, L., Bidochka, M. J., Rizzo, N. W., and Roberts, D. W. 1996. Biochemical characterisation and ultrastructural localisation of two extracellular trypsins produced by Metarhizium anisopliae in infected insect cuticles. Appl. Environ. Microbiol. 62:1257-1264.
64. Tseng, T. C., and Mount, M. S. 1974. Toxicity of endopolygalacturonate trans-eliminase, phosphatidase and protease to potato and cucumber tissue. Phytopathology 64:229-236.
65. Vallélian-Bindschedler, L, Mösinger, E., Métraux, J.-P., and Schweizer, P. 1998. Structure, expression and localisation of a germin-like protein in barley (Hordeum vulgare L.) that is insoluble in stressed leaves. Plant Mol. Biol. 37:297-308.
66. van den Ackerveken, G. F. J. M., Vossen, P., and De Wit, P. J. G. M. 1993. The AVR9 race-specific elicitor of Cladosporium fulvum is processed by endogenous and plant proteases. Plant Physiol. 103:91-96.
67. von Heijne, G. 1986. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14:4683-4690.
68. Walton, J. D. 1994. Deconstructing the cell wall. Plant Physiol. 104: 1113-1118.
69. Weber, G. F. 1922. II. Septoria diseases of wheat. Phytopathology 12: 537-585.
70. Willis, J. W., Engwall, J. K., Leach, J. E., and Chatterjee, A. K. 1987. Extracellular protease of Erwinia carotovora subsp. carotovora: Characteristics and involvement in soft-rot pathogenesis. (Abstr.) Phytopathology 77:1736.
71. Zinkernagel, V., Reiss, F., and Wendland, M. 1988. Infection structures of Septoria nodorum in leaves of susceptible wheat cultivars. J. Plant Dis. Prot. 95:169-175.