Endo- and exopolygalacturonases of Ralstonia solanacearum are inhibited by polygalacturonase-inhibiting protein (PGIP) activity in tomato stem extracts

Plant Physiology and Biochemistry

Volumn 49, Issue 4, 2011, Pages 377-387

  Schacht, Tanja ^a   Unger, Christoph ^b   Pich, Andreas ^c   Wydra, Kerstin ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b UNIVERSITY OF ROSTOCK   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Polygalacturonase inhibiting protein; Polygalacturonases; R. solanacearum

Indexed keywords

BACTERIAL PROTEIN; PECTIN; POLYGALACTURONASE; POLYGALACTURONIC ACID; VEGETABLE PROTEIN;

ARTICLE; CELL WALL; CHEMISTRY; DRUG ANTAGONISM; ENZYMOLOGY; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; PLANT STEM; RALSTONIA SOLANACEARUM; TOMATO;

BACTERIAL PROTEINS; CELL WALL; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MUTATION; PECTINS; PLANT DISEASES; PLANT IMMUNITY; PLANT PROTEINS; PLANT STEMS; POLYGALACTURONASE; RALSTONIA SOLANACEARUM;

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; RALSTONIA SOLANACEARUM;

EID: 79953043376     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2011.02.001     Document Type: Article

References (64)

1. Abu-Goukh A.A., Strand L.L., Labavitch J.M. Development-regulated changes in decay susceptibility and polygalacturonase inhibitor content of 'Barlett' pear fruit. Physiol. Plant Pathol. 1983, 23:101-109.
2. Alghisi P., Favaron F. Pectin-degrading enzymes and plant-parasite interactions. Eur. J. Plant Pathol. 1995, 101:365-375.
3. Allen C., Gay J., Simon-Buela L. A regulatory locus, pehSR, controls polygalacturonase production and other virulence functions in Ralstonia solanacearum. Mol. Plant-Microbe Interact. 1997, 10:1054-1064.
4. Allen C., Huang Y., Sequeira L. Cloning of genes affecting polygalacturonase production in Pseudomonas solanacearum. Mol. Plant-Microbe Interact. 1991, 4:147-154.
5. Allen C., Simon L., Atkinson M., Sequeira S. Analysis of polygalacturonase as a component of bacterial wilt disease. Bacterial Wilt 1993, 238-244. ACAIR Press, Canberra, Australia. G.L. Hartman, A.C. Hayward (Eds.).
6. Bellincampi D., Camardella L., Delcour J.A., Desseaux V., D'Ovidio R., Durand A., Elliot G., Gebruers K., Giovane A., Juge N., SØrensen J.F., Svensson B., Vairo D. Potential physiological role of plant glycosidase inhibitors. Biochim. Biophys. Acta Protein Proteom. 2004, 1696:265-274.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Brumbley S.M., Carney B.F., Denny T.P. Phenotype conversion in Pseudomonas solanacearum due to spontaneous inactivation of PhcA, a putative LysR transcriptional regulator. J. Bacteriol. 1993, 175:5477-5487.
9. Brumbley S.M., Denny T.P. Cloning of wild-type Pseudomonas solanacearum phcA, a gene that when mutated alters expression of multiple traits that contribute to virulence. J. Bacteriol. 1990, 172:5677-5685.
10. Buddenhagen I., Kelman A. Biological and physiological aspects of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Plant Pathol. 1964, 2:203-230.
11. Buza N.L., Krinitsyna A.A., Protsenko M.A., Vartapetyan V.V. Role of the polygalacturonidase inhibitor protein in the ripening of apples and their resistance to Monilia fructigena, a causative agent of fruit rot. Appl. Biochem. Microbiol. 2004, 40:89-92.
12. Cervone F., Castoria R., Leckie F., De Lorenzo G. Perception of fungal elicitors and signal transduction. Signal Transduction in Plants 1997, 153-177. Birkhäuser Verlag, Basel, Switzerland. P. Aducci (Ed.).
13. Cervone F., De Lorenzo G., Pressey R., Darvill A.G., Albersheim P. Can Phaseolus PGIP inhibit pectic enzymes from microbes and plants?. Phytochemistry 1990, 29:447-449.
14. D'Ovidio R., Raiola A., Capodicasa C., Devoto A., Pontiggia D., Roberti S., Galletti R., Conti E., O'Sullivan D., De Lorenzo G. Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol. 2004, 135:2424-2435.
15. De Lorenzo G., D'Ovidio R., Cervone F. The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. Annu. Rev. Phytopathol. 2001, 39:313-335.
16. De Lorenzo G., Cervone F., Bellincampi D., Caprari C., Clark A.J., Desiderio A., Devoto A., Forrest R., Leckie F., Nuss L., Salvi G. Polygalacturonase, PGIP and oligogalacturonides in cell-cell communication. Biochem. Soc. Trans. 1994, 22:394-397.
17. De Lorenzo G., Ferrari S. Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Curr. Opin. Plant Biol. 2002, 5:295-299.
18. Denny T.P. Plant pathogenic Ralstonia species. Plant Associated Bacteria 2006, 573-644. Springer, Dordrecht, The Netherlands. S.S. Gnanamanickam (Ed.).
19. Denny T.P., Brumbley S.M., Carney B.F., Cloug S.J., Schell M.A. Phenotype conversion of Pseudomonas solanacearum: its molecular basis and potential function. Bacterial Wilt: The Disease and Its Causative Agent, Pseudomonas solanacearum 1994, 137-143. CAB International, Wallingford, UK. C.A. Hayward, G.L. Hartmann (Eds.).
20. Denny T.P., Makini F.W., Brumbley S.M. Characterization of Pseudomonas solanacearum Tn5 mutants deficient in extracellular polysaccharide. Mol. Plant-Microbe Interact. 1988, 1:215-223.
21. Di Pietro A., Roncero M.I.G. Endopolygalacturonase from Fusarium oxysporum f. sp. lycopersici: purification, characterization, and production during infection of tomato plants. Phytopathology 1996, 86:1324-1330.
22. Dingle J., Reid W.W., Solomons G.L. The enzymatic degradation of pectin and other polysaccharides. II. Application of the 'cup-plate' assay to the estimation of enzymes. J. Sci. Food Agric. 1953, 4:149-155.
23. Diogo R.V.C., Wydra K. Silicon-induced basal resistance in tomato against Ralstonia solanacearum is related to modification of pectic cell wall polysaccharide structure. Physiol. Mol. Plant Pathol. 2007, 70:120-129.
24. Federici L., Di Matteo A., Fernandez-Recio J., Tsernoglou D., Cervone F. Polygalacturonase inhibiting proteins: players in plant innate immunity?. Trends Plant Sci. 2006, 11:65-70.
25. Fisch W.W. Polygalacturonase-inhibiting protein activity in cantaloupe fruit as a function of fruit maturation and tissue origin. Eur. J. Plant Pathol. 2005, 111:67-76.
26. Flavier A.B., Clough S.J., Schell M.A., Denny T.P. Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol. Microbiol. 1997, 26:251-259.
27. García Maceira F.I., Di Pietro A., Roncero I.G. Purification and characterization of a novel exopolygalacturonase from Fusarium oxysporum f. sp. lycopersici. FEMS Microbiol. Lett. 1997, 154:37-43.
28. Genin S., Boucher C. Ralstonia solanacearum: secrets of a major pathogen unveiled by analysis of its genome. Mol. Plant Pathol. 2002, 3:111-118.
29. González E.T., Allen C. Characterization of a Ralstonia solanacearum operon required for polygalacturonate degradation and uptake of galacturonic acid. Mol. Plant-Microbe Interact. 2003, 16:536-544.
30. Hayward A.C. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 1991, 29:65-87.
31. Hikichi Y., Yoshimochi T., Tsujimoto S., Shinohara R., Nakaho K., Kanda A., Kiba A., Ohnishi K. Global regulation of pathogenicity mechanism of Ralstonia solanacearum. Plant Biotech. 2007, 24:149-154.
32. Huang J., Schell M. Molecular characterization of the eps gene cluster of Pseudomonas solanacearum and its transcriptional regulation at a single promoter. Mol. Microbiol. 1995, 16:977-989.
33. Huang Q., Allen C. An exo-poly-α-D-galacturonosidase, PehB, is required for wild-type virulence of Ralstonia solanacearum. J. Bacteriol. 1997, 179:7369-7378.
34. Huang Q., Allen C. Polygalacturonases are required for rapid colonization and full virulence of Ralstonia solanacearum on tomato plants. Physiol. Mol. Plant Pathol. 2000, 57:77-83.
35. Husain A., Kelman A. Relation of slime production to mechanism of wilting and pathogenicity of Pseudomonas solanacearum. Phytopathology 1958, 48:155-165.
36. Husain A., Kelman A. The role of pectic and cellulolytic enzymes in pathogenesis by Pseudomonas solanacearum. Phytopathology 1958, 48:377-386.
37. Jeger M.J., Viljanen-Rollinson S.L.H. The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars. Theor. Appl. Genet. 2001, 102:32-40.
38. Jeong E.-L., Timmis J.N. Novel insertion sequence elements associated with genetic heterogeneity and phenotype conversion in Ralstonia solanacearum. J. Bacteriol. 2000, 182:4673-4676.
39. Johnston D.J., Ramanathan V., Williamson B. A protein from immature raspberry fruits which inhibits endopolygalacturonases from Botrytis cinerea and other micro-organisms. J. Exp. Bot. 1993, 44:971-976.
40. Kelemu S., Collmer A. Erwinia chrysanthemi EC16 produces a second set of plant inducible pectate lyase isozymes. Appl. Environ. Microbiol. 1993, 59:1756-1761.
41. Kelman A. The relationship of pathogenicity of Pseudomnas solanacearum to colony appearance in a tetrazolium medium. Phytopathology 1954, 44:693-695.
42. Kelman A., Hruschka J. The role of motility and aerotaxis in the selective increase of avirulent bacteria in still broth cultures of Pseudomonas solanacearum. J. Gen. Microbiol. 1973, 76:177-188.
43. Kemp G., Bergmann C.W., Clay R., Van der Westhuizen A.J., Pretorius Z.A. Isolation of a polygalacturonase-inhibiting protein (PGIP) from wheat. Mol. Plant-Microbe Interact. 2003, 16:955-961.
44. Kemp G., Stanton L., Bergmann C.W., Clay R.P., Albersheim P., Darvill A. Polygalacturonase-inhibiting protein can function as activators of polygalacturonase. Mol. Plant-Microbe Interact. 2004, 17:888-894.
45. Laemmli U.K. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
46. Lafitte C., Barthe J.P., Montillet J.L., Touzé A. Glycoprotein inhibitors of Colletotrichum lindemuthianum endopolygalacturonase in near isogenic lines of Phaseolus vulgaris resistant and susceptible to anthracnose. Physiol. Plant Pathol. 1984, 25:39-53.
47. Leckie F., Mattei B., Capodicasa C., Hemmings A., Nuss L., Aracri B., De Lorenzo G., Cervone F. The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed β-strand/β-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J. 1999, 18:2352-2363.
48. Lojkowska E., Masclaux C., Boccara M., Robert-Baudouy J., Hugouvieux-Cotte Pattat N. Characterization of the pelL gene encoding a novel pectate lyase of Erwinia chrysanthemi 3937. Mol. Microbiol. 1995, 16:1183-1195.
49. Mattei B., Bernalda M.S., Federici L., Roepstorff P., Cervone F., Boffi A. Secondary structure and post-translational modifications of leucine-rich repeat protein PGIP (polygalacturonase-inhibiting protein) from Phaseolus vulgaris. Biochemistry 2001, 40:569-576.
50. Nelson N. A photometric adaptation of the Somogyi method for the determination of glucose. J. Biol. Chem. 1944, 153:375-380.
51. Poussier S., Thoquet P., Trigalet-Demery D., Barthet S., Meyer D., Arlat M., Trigalet A. Host plant-dependent phenotypic reversion of Ralstonia solanacearum from non-pathogenic to pathogenic forms via alterations in the phcA gene. Mol. Microbiol. 2003, 49:991-1003.
52. R: A Language and Environment for Statistical Computing 2004, vol. 69. R Development Core Team, R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org.
53. Roberts D.P., Denny T.P., Schell M.A. Cloning of the egl gene of Pseudomonas solanacearum and analysis of its role in phytopathogenicity. J. Bacteriol. 1988, 170:1445-1451.
54. Ryan C.A. Oligosaccharide signalling in plants. Annu. Rev. Cell Biol. 1987, 3:295-317.
55. Salvi G., Giarrizzo F., De Lorenzo G., Cervone F. A polygalacturonase-inhibiting protein in the flowers of Phaseolus vulgaris L. J. Plant Physiol. 1990, 136:513-518.
56. Schell M.A. To be or not to be: how Pseudomonas solanacearum decides whether or not to express virulence genes. Eur. J. Plant Pathol. 1996, 102:459-469.
57. Schell M.A. Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annu. Rev. Phytopathol. 2000, 38:263-292.
58. Schell M.A., Roberts D.P., Denny T.P. Analysis of the Pseudomonas solanacearum polygalacturonase encoded by pglA and its involvement in phytopathogenicity. J. Bacteriol. 1988, 170:4501-4508.
59. Somogyi M. A new reagent for the determination of sugars. J. Biol. Chem. 1945, 160:61-68.
60. Tans-Kersten J., Brown D., Allen C. Swimming motility, a virulence trait of Ralstonia solanacearum, is regulated by FlhDC and the plant host environment. Mol. Plant-Microbe Interact. 2004, 17:686-695.
61. Tans-Kersten J., Guan Y., Allen C. Ralstonia solanacearum pectin methylesterase is required for growth on methylated pectin but not for bacterial wilt virulence. Appl. Environ. Microbiol. 1998, 64:4918-4923.
62. Valls M., Genin S., Boucher C. Integrated regulation of the type III secretion system and other virulence determinants in Ralstonia solanacearum. PloS Pathog. 2006, 2:798-807. http://www.plospathogens.org.
63. Vasse J., Frey P., Trigalet A. Microscopic studies of intercellular infection and protoxylem invasion of tomato roots of Pseudomonas solanacearum. Mol. Plant-Microbe Interact 1995, 8:241-251.
64. Vidhyasekaran P. Bacterial Disease Resistance in Plants 2002, Haworth Press Inc., Binghampton, NY.