A polygalacturonase-inhibiting protein with a role in pea defence against the cyst nematode Heterodera goettingiana

Molecular Plant Pathology

Volumn 12, Issue 3, 2011, Pages 275-287

  Veronico, Pasqua ^a   Melillo, M Teresa ^a   Saponaro, Concetta ^a   Leonetti, Paola ^a   Picardi, Ernesto ^b   Jones, John T ^c  

^a INSTITUTE FOR SUSTAINABLE PLANT PROTECTION   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; COMPLEMENTARY DNA; CYCLOPENTANE DERIVATIVE; JASMONIC ACID METHYL ESTER; MESSENGER RNA; OXYLIPIN; PGIP PROTEIN, PLANT; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL; ARTICLE; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; NEMATODE; PARASITOLOGY; PEA; PHYLOGENY; PHYSIOLOGY; PLANT GENOME; PLANT ROOT; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

ACETIC ACIDS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANIMALS; CYCLOPENTANES; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MOLECULAR SEQUENCE DATA; OXYLIPINS; PEAS; PHYLOGENY; PLANT PROTEINS; PLANT ROOTS; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ALIGNMENT; TYLENCHOIDEA;

HETERODERA GOETTINGIANA; PISUM SATIVUM;

EID: 79952050928     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2010.00671.x     Document Type: Article

References (47)

1. Agüero, C.B., Uratsu, S.L., Greve, C., Powell, A., Labavitch, J.M., Meredith, C.P. and Dandejar, A.M. (2005) Evaluation of tolerance to Pierce's disease and Botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Mol. Plant Pathol. 6, 43-51.
2. Baum, T.J., Hussey, R.S. and Davis, E.L. (2007) Root-knot and cyst nematode parasitism genes: the molecular basis of plant parasitism. Genet. Eng. (NY), 28, 17-43.
3. Bendtsen, J.D., Nielsen, H., von Heijne, G. and Brunak, S. (2004) Improved prediction of signal peptides: signalP 3.0. J. Mol. Biol. 340, 783-795.
4. Bleve-Zacheo, T., Melillo, M.T. and Zacheo, G. (1990) Syncytia development in germplasm pea accessions infected with Heterodera goettingiana. Nematol. Med. 18, 93-102.
5. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G. and Thompson, J.D. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 31, 3497-3500.
6. D'Ovidio, R., Raiola, A., Capodicasa, C., Devoto, A., Pontiggia, D., Roberti, S., Galletti, R., Conti, E., O'Sullivan, D. and De Lorenzo, G. (2004a) Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol. 135, 2424-2435.
7. D'Ovidio, R., Mattei, B., Roberti, S. and Bellincampi, D. (2004b) Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Biochem. Biophys. Acta, 1696, 237-244.
8. De Lorenzo, G. and Ferrari, S. (2002) Polygalacturonase-inhibiting proteins in defense against pathogenic fungi. Curr. Opin. Plant Biol. 5, 295-299.
9. De Lorenzo, G., D'Ovidio, R. and Cervone, F. (2001) The role of polygalacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. Annu. Rev. Phytopathol. 39, 313-335.
10. Dellaporta, S., Wood, J. and Hicks, J. (1983) A plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 1, 19-21.
11. Di Matteo, A., Federici, L., Mattei, B., Salvi, G., Johnson, K.A., Savino, C., De Lorenzo, G., Tsernoglou, D. and Cervone, F. (2003) The crystal structure of PGIP (polygalacturonase-inhibiting protein), a leucine-rich repeat protein involved in plant defense. Proc. Natl. Acad. Sci. USA, 100, 10124-10128.
12. Ferrari, S., Vairo, D., Ausubel, F.M., Cervone, F. and De Lorenzo, G. (2003) Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated co-ordinately by different signal transduction pathways in response to fungal infection. Plant Cell, 15, 93-106.
13. Ferrari, S., Galletti, R., Vairo, D., Cervone, F. and De Lorenzo, G. (2006) Antisense expression of the Arabidopsis thaliana AtPGIP1 gene reduces polygalacturonase-inhibiting protein accumulation and enhances susceptibility to Botrytis cinerea. Mol. Plant-Microbe Interact. 19, 931-936.
14. Gao, X., Starr, J., Göbel, C., Engelberth, J., Feussner, I., Tumlinson, J. and Kolomiets, M. (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defence genes, and resistance to root-knot nematodes. Mol. Plant-Microbe Interact. 21, 98-109.
15. Girard, C. and Jouanin, L. (1999) Molecular cloning of cDNAs encoding a range of digestive enzymes from aphytophagous beetle, Phaedon cochleariae. Insect Biochem. Mol. Biol. 29, 1129-1142.
16. Goellner, M., Wang, X. and Davis, E.L. (2001) Endo-1, 4-glucanase expression in compatible plant-nematode interactions. Plant Cell, 13, 2241-2255.
17. Guindon, S., Delsuc, F., Dufayard, J.F. and Gascuel, O. (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol. Biol. 537, 113-137.
18. ten Have, A., Tenberge, K.B., Benen, J.A.E., Tudzynski, P., Visser, J. and van Kan, J.A.L. (2002) The contribution of the cell wall degrading enzymes to pathogenesis of fungal plant pathogens. In: The Mycota XI, Agricultural Applications (Kempken, F., ed.), pp. 341-358. Berlin: Springer-Verlag.
19. Huang, Q. and Allen, C. (2000) Polygalacturonases are required for rapid colonization and full virulence of Ralstonia solanacearum on tomato plants. Physiol. Mol. Plant Pathol. 57, 77-83.
20. Hugouvieux-Cotte-Pattat, N., Condemine, G., Nasser, W. and Reverchon, S. (1996) Regulation of pectinolysis in Erwinia chrysanthemi. Annu. Rev. Microbiol. 50, 213-257.
21. Jackson, D.P. (1991) In situ hybridization in plants. In: Molecular Plant Pathology: A practical Approach (Bowles, D.J., Gurr, S.J. and McPherson, M., eds), pp. 157-181. Oxford: Oxford University Press.
22. Janni, M., Sella, L., Favaron, F., Blechl, A.E., De Lorenzo, G. and D'Ovidio, R. (2008) The expression of a bean PGIP in transgenic wheat confers increased resistance to the fungal pathogen Bipolaris sokoriniana. Mol. Plant-Microbe Interact. 21, 171-177.
23. Jaubert, S., Laffaire, J.B., Abad, P. and Rosso, M.N. (2002) A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett. 522, 109-112.
24. Jones, D.A. and Jones, J.D.G. (1997) The roles of leucine rich repeats in plant defences. Adv. Bot. Res. 24, 90-167.
25. Jones, D.T., Taylor, W.R. and Thornton, J.M. (1992) The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282.
26. Jones, M.G.K. (1981) Host cell responses to endoparasitic nematode attack: structure and function of giant cells and syncytia. Ann. Appl. Biol. 97, 353-372.
27. Joubert, D.A., Slaughter, A.R., Kemp, G., Becker, J., Krooshof, G.H., Bergmann, C., Benen, J., Pretorius, I.S. and Vivier, M.A. (2006) The grapevine polygalacturonase-inhibiting protein (VvPGIP1) reduces Botrytis cinerea susceptibility in transgenic tobacco and differentially inhibits fungal polygalacturonases. Transgenic Res. 15, 687-702.
28. Joubert, D.A., Kars, I., Wagemakers, L., Bergmann, C., Kemp, G., Vivier, M.A. and van Kan, J.A.L. (2007) A polygalacturonase-inhibiting protein from grapevine reduces the symptoms of the endopolygalacturonase BcPG2 from Botrytis cinerea in Nicotiana benthamiana leaves without any evidence for in vitro interaction. Mol. Plant-Microbe Interact. 4, 392-402.
29. Kumar, S., Dudley, J., Nei, M. and Tamura, K. (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinformatics, 9, 299-306.
30. Lanave, C., Preparata, G., Saccone, C. and Serio, G. (1984) A new method for calculating evolutionary substitution rates. J. Mol. Evol. 20, 86-93.
31. Leckie, F., Mattei, B., Capodicasa, C., Hemmings, A., Nuss, L., Aracri, B., De Lorenzo, G. and 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. 18, 2352-2363.
32. Leone, A., Melillo, M.T. and Bleve-Zacheo, T. (2001) Lipoxygenase in pea roots subjected to biotic stress. Plant Sci. 161, 703-717.
33. Li, R., Rimmer, R., Yu, M., Sharpe, A.G., Seguin-Swartz, G., Lydiate, D. and Hegedus, D.D. (2003) Two Brassica napus polygacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses. Planta, 217, 299-308.
34. Mahalingam, R., Wang, G. and Knap, H.T. (1999) Polygalacturonase and polygalacturonase inhibitor protein: gene isolation and transcription in Glycine max-Heterodera glycines interactions. Mol. Plant-Microbe Interact. 12, 490-498.
35. Martin, G.B., Bogdanove, A.J. and Sessa, G. (2003) Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54, 23-61.
36. Mattei, B., Bernalda, M.S., Federici, L., Roepstorff, P., Cervone, F. and Boffi, A. (2001) Secondary structure and post-translational modifications of the leucine-reach repeat protein PGIP (polygalacturonase-inhibiting protein) from Phaseolus vulgaris. Biochemistry, 40, 569-576.
37. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 2002-2007.
38. Powell, A.L.T., van Kan, J., ten Have, A., Visser, J., Greve, L.C., Bennett, A.B. and Labavitch, J.M. (2000) Transgenic expression of pear PGIP in tomato limits fungal colonization. Mol. Plant-Microbe Interact. 13, 942-950.
39. Prior, A.E., Jones, J.T., Blok, V.C., Beauchamp, J., McDermott, L., Cooper, A. and Kennedy, M.W. (2001) A surface-associated retinol- and fatty acid-binding protein (GpLBP20) from the potato cyst nematode Globodera pallida-lipid binding activities, structural analysis and expression pattern. Biochem. J. 356, 387-394.
40. Ridley, B.L., O' Neill, M.A. and Mohnen, D. (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry, 57, 929-967.
41. Sambrook, J., Fristch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
42. Veronico, P., Giannino, D., Melillo, M.T., Leone, A., Reyes, A., Kennedy, M.W. and Bleve-Zacheo, T. (2006) A novel lipoxygenase in pea roots. Its function in wounding and biotic stress. Plant Physiol. 141, 1045-1055.
43. Vos, M., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J. and Kuiper, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407-4414.
44. Walton, J.D. (1994) Deconstructing the cell wall. Plant Physiol. 104, 1113-1118.
45. Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 100, 681-697.
46. Wilkins, M.R., Gasteiger, E., Bairoch, A., Sanchez, J.C., Williams, K.L., Appel, R.D. and Hochstrasser, D.F. (1999) Protein identification and analysis tools in ExPASy server. In: Methods in Molecular Biology, 2-D Proteome Analysis Protocols, Vol. 112. (Link, A.J., ed.), pp. 531-552. Totowa, NJ: Humana Press Inc.
47. Zhao, S. and Fernald, R.D. (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 12, 1047-1064.