Two Brassica napus polygalacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses

Planta

Volumn 217, Issue 2, 2003, Pages 299-308

  Li, Rugang ^a   Rimmer, Roger ^a   Yu, Min ^a   Sharpe, Andrew G ^a   Séguin Swartz, Ginette ^a   Lydiate, Derek ^a   Hegedus, Dwayne D ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Brassica; Defense response; Polygalacturonase inhibitory protein; Sclerotinia; Stress; Wounding

Indexed keywords

FUNGI; GENES; PROTEINS;

FUNGAL PATHOGENS;

PLANTS (BOTANY);

ALTICINI; BRASSICA; BRASSICA NAPUS; COLEOPTERA; EMBRYOPHYTA; EUKARYOTA; FUNGI; SCLEROTINIA; SCLEROTINIA SCLEROTIORUM; SIPHONAPTERA (FLEAS);

EID: 0038082135     PISSN: 00320935     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00425-003-0988-5     Document Type: Article

References (65)

1. Becraft PW (1998) Receptor kinases in plant development. Trends Plant Sci 3:384-388
2. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz, BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265:1856-1860
3. Bergmann CW, ItoY, Singer D, Albersheim P, Darwill AG, Benhamou N, Nuss L, Salvi G, Cervone F, De Lorenzo G (1994) Polygalacturonase-inhibiting protein accumulates in Phaseolus vulgaris L. in response to wounding, elicitors and fungal infection. Plant J 5:625-634
4. Cervone F, De Lorenzo G, Pressey R, Darvill AG, Albersheim P (1990) Can Phaseolus PGIP inhibit pectic enzymes from microbes and plants? Phytochemistry 29:447-449
5. Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661-677
6. Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575-585
7. Cook BJ, Clay RP, Bergmann CW, Albersheim P, Darvill AG (1999) Fungal polygalacturonases exhibit different substrate degradation patterns and differ in their susceptibilities to polygalacturonase-inhibiting proteins. Mol Plant Microbe Interact 12:703-711
8. Darvill A, Bergmann C, Cervone F, De Lorenzo G, Ham KS, Spiro MD, York WS, Albersheim P (1994) Oligosaccharins involved in plant growth and host-pathogen interactions. Biochem Soc Symp 60:89-94
9. de Bruxelles GL, Roberts MR (2001) Signals regulating multiple responses to wounding and herbivores. Crit Rev Plant Sci 20:487-521
10. De Lorenzo G, Cervone F (1997) Polygalacturonase-inhibiting proteins (PGIP): their role in specificity and defense against pathogenic fungi. In: Stacey G, Keen NT (eds) Plant-microbe interactions, Chapman & Hall, New York, vol 3, pp 76-93
11. De Lorenzo G, Ito Y, D'Ovidio R, Cervone F, Albersheim P, Darvill AG (1990) Host-pathogen interactions. X X X VII. Abilities of the polygalacturonase-inhibiting proteins from four cultivars of Phaseolus vulgaris to inhibit the polygalacturonases from three races of Colletotrichum lindemuthianum. Physiol Mol Plant Pathol 36:421-435
12. De Lorenzo G, Cervone F, Bellicampi D, Caprari C, Clark AJ, Desiderio A, Devoto A, Forrest R, Leckie F, Nuss L, Salvi G (1994) Polygalacturonase, PGIP and oligogalacturonides in cell-cell communication. Biochem Soc Trans 22:396-399
13. De Lorenzo G, D'Ovidio R, Cervone F (2001) The role of polygalacturonase-inhibiting proteins (PGIP) in defense against pathogenic fungi. Annu Rev Phytopathol 39:313-335
14. Dempsey DA, Shah J, Klessig D (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547-575
15. Desiderio A, Aracri B, Leckie F, Mattei B, Salvi G, Tigelaar H, Vanroekel JSC, Baulcombe DC, Melchers LS, Delorenzo G, Cervone F (1997) Polygalacturonase-inhibiting proteins (PGIP) with different specificities are expressed in Phaseolus vulgaris. Mol Plant Microbe Interact 10:852-860
16. Devoto A, Clark AJ, Nuss L, Cervone F, De Lorenzo G (1997) Developmental and pathogen-induced accumulation of transcripts of polygalacturonase-inhibiting protein in Phaseolus vulgaris L. Planta 202:284-292
17. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG (1996) The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84:451-459
18. Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741-1746
19. Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316-323
20. Favaron F, D'Ovidio R, Porceddu E, Alghisi P (1994) Purification and molecular characterization of a soybean polygalacturonase inhibiting protein. Planta 195:80-87
21. Frediani M, Cremonini R, Salvi G, Caprari C, Desiderio A (1993) Cytological localization of the pgip genes in the embryo suspensor cells of Phaseolus vulgaris L. Theor Appl Genet 87:369-373
22. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis - 2001 status. Curr Opin Plant Biol 4:301-308
23. Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269:843-846
24. Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117:337-343
25. Hanfrey C, Fife M, Buchanan-Wollaston V (1996) Leaf senescence in Brassica napus: expression of genes encoding pathogenesis-related proteins. Plant Mol Biol 30:597-609
26. Johnston DJ, Ramanathan V, Williamson B (1993) A protein from immature raspberry fruits which inhibits endopolygalacturonases from Botrytis cinerea and other micro-organisms. J Exp Bot 44:971-976
27. Jones DA, Jones JDG (1997) The role of leucine-rich repeat proteins in plant defence. Adv Bot Res 24:89-166
28. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789-793
29. Keen NT (1992) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447-463
30. Kobe B, Deisenhofer J (1993) Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats. Nature 366:751-756
31. Kobe B, Deisenhofer JZ (1994) The leucine-rich repeat: a versatile binding motif. Trends Biochem Sci 19:415-21
32. Komjanc M., Festi S, Rizzotti L, Cattivelli L, Cervone F, De Lorenzo G (1999) A leucine-rich repeat receptor-like protein kinase (LRPKm1) gene is induced in Malus x domestica by Venturia inaequalis infection and salicylic acid treatment. Plant Mol Biol 40:945-957
33. Kreegipuu A, Blom N, Brunak S (1999) PhosphoBase, a database of phosphorylation sites: release 2.0. Nucleic Acids Res 27:237-239
34. Leckie F, Mattei B, Capodicasa C, Hemmings S, Nuss L, Aracri B, De Lorenzo G, Cervone F (1999) 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 9:2352-2363
35. Leech A, Mattei B, Federici L, De Lorenzo G, Hemmings AM (2000) Preliminary X-ray crystallographic analysis of a plant defence protein, the polygalacturonase-inhibiting protein from Phaseolus vulgaris. Acta Crystallogr D Biol Crystallogr 56:98-100
36. Li JM, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929-938
37. Li R, Rimmer R, Sharpe A, Séguin-Swartz G, Hegedus D (2002) Polygalacturonases of Sclerotinia sclerotiorum: expression during saprophytic and parasitic modes of growth. Phytopathology 92:S47
38. Machinandiarena MF, OLivieri FP, Daleo GR, Oliva CR (2001) Isolation and characterization of a polygalacturonase-inhibiting protein from potato leaves: accumulation in response to salicylic acid, wounding and infection. Plant Physiol Biochem 39:129-136
39. Mattei B, Bernalda MS, Federici L, Roepstorff P, Cervone F, Boffi A (2001) Secondary structure and post-translational modifications of the leucine-rich repeat protein PGIP (polygalacturonase-inhibiting protein) from Phaseolus vulgaris. Biochemistry 40:569-576
40. Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994) The Arabidopsis thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089-1099
41. Nielson H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of cleavage sites. Protein Eng 10:1-6
42. Pieterse CMJ, van Loon LC (1999) Salicylic acid-independent plant defense pathways. Trends Plant Sci 4:52-58
43. Powell AL, van Kan J, ten Have A, Visser J, Greve LC, Bennett AB, Labavitch JM (2000) Transgenic expression of pear PGIP in tomato limits fungal colonization. Mol Plant Microbe Interact 13:942-950
44. Powell ALT, Stotz HU, Labavitch JM, Bennett AB (1994) Glycoprotein inhibitors of fungal polygalacturonases. Adv Mol Genet Plant Microbe Interact 3:399-402
45. Pressey R (1996) Polygalacturonase inhibitors in bean pods. Phytochemistry 42:1267-1270
46. Ramonell KM, Somerville S (2002) The genomics parade of defense responses: to infinity and beyond. Curr Opin Plant Biol 5:1-4
47. Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707-719
48. Ronald PC (1997) The molecular basis of disease resistance in rice. Plant Mol Biol 35:179-186
49. Rojo E, Titarenko E, Leon J, Berger S, Vancanneyt G, Sanchez-Serrano JJ (1998) Reversible protein phosphorylation regulates jasmonic acid-dependent and -independent wound signal transduction pathways in Arabidopsis thaliana. Plant J 13:153-165
50. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809-1819
51. Sander L, Child R, Ulvskov P, Albrechtsen M, Borkhardt B (2001) Analysis of a dehiscence zone endo-polygalacturonase in oilseed rape (Brassica napus) and Arabidopsis thaliana: evidence for roles in cell separation in dehiscence and abscission zones, and in stylar tissue during pollen tube growth. Plant Mol Biol 46:469-479
52. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655-11660
53. Shieh MT, Brown RL, Whitehead MP, Cary JW, Cotty PJ, Cleveland TE, Dean RA (1997) Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Appl Environ Microbiol 63:3548-52
54. Simpson CG, MacRae E, Gardner RC (1995) Cloning of a polygalacturonase-inhibiting protein from kiwi fruit (Actinidia deliciosa). Plant Physiol 108:1748
55. Song WY, Wang GL, Chen LL et al (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804-1806
56. Stotz HU, Powell AL, Damon SE, Greve LC, Bennett AB, Labavitch JM (1993) Molecular characterization of a polygalacturonase inhibitor from Pyrus communis L. cv Bartlett. Plant Physiol 102:133-138
57. Stotz HU, Contos JJA, Powell ALT, Bennett AB, Labavitch JM (1994) Structure and expression of an inhibitor of fungal polygalacturonases from tomato. Plant Mol Biol 25:607-617
58. Taipalensuu J, Andreasson E, Eriksson S, Rask L (1997) Regulation of the wound-induced myrosinase-associated protein transcript in Brassica napus plants. Eur J Biochem 247:963-971
59. ten Have A, Breuil WO, Wubben JP, Visser J, van Kan JA (2001) Botrytis cinerea endopolygalacturonase genes are differentially expressed in various plant tissues. Fungal Genet Biol 33:97-105
60. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JD (1997) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209-2224
61. Toubart P, Desiderio A, Salvi G, Cervone F, Daroda L, De Lorenzo G (1992) Cloning and characterization of the gene encoding the endopolygalacturonase-inhibiting protein (PGIP) of Phaseolus vulgaris L. Plant J 2:367-373
62. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-1 receptor. Cell 78:1101-1115
63. Walker JC (1993) Receptor-like protein kinase genes of Arabidopsis thaliana. Plant J 3:451-456
64. Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998) A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10:1439-1452
65. Yao C, Conway WS, Ren R, Smith D, Ross GS, Sams CE (1999) Gene encoding polygalacturonase inhibitor in apple fruit is developmentally regulated and activated by wounding and fungal infection. Plant Mol Biol 39:1231-1241