Characterization of the complex locus of bean encoding polygalacturonase- inhibiting proteins reveals subfunctionalization for defense against fungi and insects

Plant Physiology

Volumn 135, Issue 4, 2004, Pages 2424-2435

  D'Ovidio, Renato ^a   Raiola, Alessandro ^b,e   Capodicasa, Cristina ^a   Devoto, Alessandra ^b,f   Pontiggia, Daniela ^b   Roberti, Serena ^a   Galletti, Roberta ^b   Conti, Eric ^c   O'Sullivan, Donal ^d   De Lorenzo, Giulia ^b  

^a UNIVERSITY OF TUSCIA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF PERUGIA   (Italy)

^d NATIONAL INSTITUTE OF AGRICULTURAL BOTANY   (United Kingdom)

^e UNIVERSITY OF PADOVA   (Italy)

^f UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; DISEASE CONTROL; FUNGI; GENES; PATHOLOGY; PLANTS (BOTANY);

ELICITORS; GENOTYPE; PATHOGENIC FUNGI;

PROTEINS;

AMINO ACIDS; DISEASES; FUNGI; GENES; PATHOLOGY; PLANTS; PROTEINS;

ADELPHOCORIS; ADELPHOCORIS LINEOLATUS; EUKARYOTA; FUNGI; FUSARIUM; FUSARIUM MONILIFORME; GIBBERELLA FUJIKUROI; HEXAPODA; INSECTA; LYGUS; LYGUS RUGULIPENNIS; PHASEOLUS (ANGIOSPERM); PHASEOLUS VULGARIS;

EID: 4444320185     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.104.044644     Document Type: Article

References (57)

1. Baulcombe D, Chapman S, Santa Cruz S (1995) Jellyfish green fluorescent protein as a reporter for virus infections. Plant J 7: 1045-1053
2. Baumgarten A, Cannon S, Spangler R, May G (2003) Genome-level evolution of resistance genes in Arabidopsis thaliana. Genetics 165: 309-319
3. Becraft PW (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18: 163-192
4. Bellincampi D, Camardella L, Delcour JA, Desseaux V, D'Ovidio R, Durand A, Elliot G, Gebruers K, Giovane A, Juge N, et al (2004) Potential physiological role of plant glycosidase inhibitors. Biochim Biophys Acta 1696: 265-274
5. Bellincampi D, Cardarelli M, Zaghi D, Serino G, Salvi G, Gatz C, Cervone F, Altamura MM, Costantino P, De Lorenzo G (1996) Oligogalacturonides prevent rhizogenesis in rol B transformed tobacco explants by inhibiting auxin-induced expression of the rol B gene. Plant Cell 8: 477-487
6. Bergelson J, Kreitman M, Stahl EA, Tian D (2001) Evolutionary dynamics of plant R-genes. Science 292: 2281-2285
7. Bergmann C, Ito Y, Singer D, Albersheim P, Darvill 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
8. Boyd DW Jr, Cohen AC, Alverson DR (2002) Digestive enzymes and stylet morphology of Deraeocoris nebulosus (hemiptera: Miridae), a predacious plant bug. Ann Entomol Soc Am 95: 395-401
9. Brenner S (2000) Biochemistry strikes back. Trends Biochem Sci 25: 584
10. Caprari C, Bergmann C, Migheli Q, Salvi G, Albersheim P, Darvill A, Cervone F, De Lorenzo G (1993) Fusarium moniliforme secretes four endopolygalacturonases derived from a single gene product. Physiol Mol Plant Pathol 43: 453-462
11. Caprari C, Mattei B, Basile ML, Salvi G, Crescenzi V, De Lorenzo G, Cervone F (1996) Mutagenesis of endopolygalacturonase from Fusarium moniliforme: histidine residue 234 is critical for enzymatic and macerating activities and not for binding to polygalacturonase-inhibiting protein (PGIP). Mol Plant Microbe Interact 9: 617-624
12. Cervone F, De Lorenzo G, Degrà L, Salvi G (1987) Elicitation of necrosis in Vigna unguiculata Walp. by homogeneous Aspergillus niger endo-polygalacturonase and by α-D-galacturonate oligomers. Plant Physiol 85: 626-630
13. Comeron JM (1999) K-estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15: 763-764
14. Daroda L, Hahn K, Pashkoulov D, Benvenuto E (2001) Molecular characterization and in planta detection of Fusarium moniliforme endopolygalacturonase isoforms. Physiol Mol Plant Pathol 59: 317-325
15. De Lorenzo G, D'Ovidio R, Cervone F (2001) The role of polygacturonase-inhibiting proteins (PGIPs) in defense against pathogenic fungi. Annu Rev Phytopathol 39: 313-335
16. De Lorenzo G, Ferrari S (2002) Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi. Curr Opin Plant Biol 5: 295-299
17. Desiderio A, Aracri B, Leckie F, Mattei B, Salvi G, Tigelaar H, Van Roekel JS, Baulcombe DC, Melchers LS, De Lorenzo G, et al (1997) Polygalacturonase-inhibiting proteins (PGIPs) with different specificities are expressed in Phaseolus vulgaris. Mol Plant Microbe Interact 10: 852-860
18. Devereux J, Haeberlei P, Smithies O (1984) A comprehensive set of sequence analysis programs for the Vax. Nucleic Acids Res 12: 387-395
19. Devoto A, Leckie F, Lupotto E, Cervone F, De Lorenzo G (1998) The promoter of a gene encoding PGIP (polygalacturonase-inhibiting protein) of Phaseolus vulgaris L. is activated by wounding but not by elicitors or pathogen infection. Planta 205: 165-174
20. Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, De Lorenzo G, Tsernoglou D, 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
21. Doostdar H, McCollum TG, Mayer RT (1997) Purification and characterization of an endo-polygalacturonase from the gut of West Indies sugarcane rootstalk borer weevil (Diaprepes abbreviatus L.) larvae. Comp Biochem Physiol 118B: 861-867
22. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5: 199-206
23. Federici L, Caprari C, Mattei B, Savino C, Di Matteo A, De Lorenzo G, Cervone F, Tsernoglou D (2001) Structural requirements of endo-polygalacturonase for the interaction with PGIP (polygalacturonase-inhibiting protein). Proc Natl Acad Sci USA 98: 13425-13430
24. Ferrari S, Vairo D, Ausubel FM, Cervone F, De Lorenzo G (2003) Tandemly duplicated Arabidopsis genes that encode polygalacturonase-inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Plant Cell 15: 93-106
25. Freyre R, Skroch PW, Geffroy V, Adam-Blondon A-F, Shirmohamadali A, Johonson WC, Llaca V, Nodari RO, Pereira PA, Tsai S-M, et al (1998) Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP map. Theor Appl Genet 97: 847-856
26. Gassmann W, Dahlbeck D, Chesnokova O, Minsavage GV, Jones JB, Staskawicz BJ (2000) Molecular evolution of virulence in natural field strains of Xanthomonas campestris pv. vesicatoria. J Bacteriol 182: 7053-7059
27. Girard C, Jouanin L (1999) Molecular cloning of cDNAs encoding a range of digestive enzymes from a phytophagous beetle, Phaedon cochleariae. Insect Biochem Mol Biol 29: 1129-1142
28. Gomez-Gomez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13: 1155-1163
29. Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39: 285-312
30. Idnurm A, Hewlett BJ (2001) Pathogenicity genes of phytopathogenic fungi. Mol Plant Pathol 2: 241-255
31. Jaubert S, Laffaire JB, Abad P, Rosso MN (2002) A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Lett 522: 109-112
32. Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7: 511-518
33. Leckie F, Mattei B, Capodicasa C, Hemmings A, 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/β-strand;-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J 18: 2352-2363
34. Lehmann P (2002) Structure and evolution of plant disease resistance genes. J Appl Genet 43: 403-414
35. Li R, Rimmer R, Yu M, Sharpe AG, Seguin-Swartz G, Lydiate D, Hegedus DD (2003) Two Brassica napus polygalacturonase inhibitory protein genes are expressed at different levels in response to biotic and abiotic stresses. Planta 217: 299-308
36. Li W-H (1997) Molecular Evolution. Sinauer, Sunderland, MA
37. Lynch M, O'Hely M, Walsh B, Force A (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159: 1789-1804
38. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54: 23-61
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. Meyer A (2003) Molecular evolution: duplication, duplication. Nature 421: 31-32
41. Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW (1998) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 10: 1833-1846
42. Ndimba BK, Chivasa S, Hamilton A, Simon WJ, Slabas AR (2003) Proteomic analysis of changes in the extracellular matrix of Arabidopsis cell suspension cultures induced by fungal elicitors. Proteomics 3: 1047-1059
43. Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148: 929-936
44. Oeser B, Heidrich PM, Muller U, Tudzynski P, Tenberge KB (2002) Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet Biol 36: 176-186
45. Poinssot B, Vandelle E, Bentejac M, Adrian M, Levis C, Brygoo Y, Garin J, Sicilia F, Coutos-Thevenot P, Pugin A (2003) The endopolygalacturonase 1 from Botrytis cinerea activates grapevine defense reactions unrelated to its enzymatic activity. Mol Plant Microbe Interact 16: 553-564
46. 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
47. Rombauts S, Dehais P, Van Montagu M, Rouze P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27: 295-296
48. Salvi G, Giarrizzo F, De Lorenzo G, Cervone F (1990) A polygalacturonase-inhibiting protein in the flowers of Phaseolus vulgaris L. J Plant Physiol 136: 513-518
49. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning, A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
50. Stotz HU, Bishop JG, Bergmann CW, Koch M, Albersheim P, Darvill AG, Labavitch JM (2000) Identification of target amino acids that effect interactions of fungal polygalacturonases and their plant inhibitors. Physiol Mol Plant Pathol 56: 117-130
51. Szekeres M (2003) Brassinosteroid and systemin: two hormones perceived by the same receptor. Trends Plant Sci 8: 102-104
52. Talhinhas P, Screenivasaprasad S, Neves-Martins J, Oliveira H (2002) Genetic and morphological characterization of Colletotrichum acutatum causing anthracnose of lupins. Phytopathology 92: 986-995
53. Toubart P, Desiderio A, Salvi G, Cervone F, Daroda L, De Lorenzo G, Bergmann C, Darvill AG, Albersheim P (1992) Cloning and characterization of the gene encoding the endopolygalacturonase-inhibiting protein (PGIP) of Phaseolus vulgaris L. Plant J 2: 367-373
54. 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
55. Wheeler AGJ (2001) Biology of the Plant Bugs (Hemiptera: Miridae). Cornell University Press, Ithaca, NY
56. Yang HA, Sweetingham MW (1998) The taxonomy of Colletotrichum isolates associated with lupin anthracnose. Aust J Agric Res 49: 1213-1223
57. Zhang J, Kumar S, Nei M (1997) Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol Biol Evol 14: 1335-1338