NopL, an Effector Protein of Rhizobium sp. NGR234, Thwarts Activation of Plant Defense Reactions

Plant Physiology

Volumn 134, Issue 2, 2004, Pages 871-879

  Bartsev, Alexander V ^a,d   Deakin, William J ^a   Boukli, Nawal M ^a,e   McAlvin, Crystal B ^b   Stacey, Gary ^b,f   Malnoë, Pia ^c   Broughton, William J ^a   Staehelin, Christian ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF TENNESSEE   (United States)

^c Federal Agronomy Research Station   (Switzerland)

^d INSTITUT DES SCIENCES DU VÉGÉTAL   (France)

^e Universidad Central del Caribe School of Medicine   (Puerto Rico)

^f UNIVERSITY OF MISSOURI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ENZYMES; GENES; NITROGEN FIXATION; TOBACCO;

SECRETION SYSTEMS;

PLANTS (BOTANY);

BACTERIA (MICROORGANISMS); EUKARYOTA; LOTUS; LOTUS CORNICULATUS VAR. JAPONICUS; LOTUS JAPONICUS; NICOTIANA; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; POTATO VIRUS Y; RHIZOBIUM; RHIZOBIUM SP.; SOLANUM TUBEROSUM;

EID: 1342308488     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.103.031740     Document Type: Article

References (60)

1. Ausubel FM, Brent R, Kingston RE, More DD, Seidman JG, Smith JA, Struhl K (1990) Current Protocols in Molecular Biology, Vol. 1 (Supplement 9). John Wiley & Sons, New York
2. Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377
3. Bartsev AV, Boukli NM, Deakin WJ, Staehelin C, Broughton WJ (2003) Purification and phosphorylation of the effector protein NopL from Rhizobium sp. NGR234. FEBS Lett 554: 271-274
4. Beffa RS, Neuhaus J-M, Meins F (1993) Physiological compensation in antisense transformants: specific induction of an "ersatz" glucan endo-1, 3-β-glucosidase in plants infected with necrotizing viruses. Proc Natl Acad Sci USA 90: 8792-8796
5. Boller T, Gehri A, Mauch F, Vögeli U (1983) Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157: 22-31
6. Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125: 1075-1080
7. Broughton WJ, Jabbouri S, Perret X (2000) Keys to symbiotic harmony. J Bacteriol 182: 5641-5652
8. Broughton WJ, Wong CH, Lewin A, Samrey U, Myint H, Meyer zA, H, Dowling DN, Simon R (1986) Identification of Rhizobium plasmid sequences involved in recognition of Psophocarpus, Vigna, and other legumes. J Cell Biol 102: 1173-1182
9. Casper-Lindley C, Dahlbeck D, Clark ET, Staskawicz BJ (2002) Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc Natl Acad Sci USA 99: 8336-8341
10. Collinge DB, Slusarenko AJ (1987) Plant gene expression in response to pathogens. Plant Mol Biol 9: 389-410
11. Cornelis GR (2002) The Yersinia Ysc-Yop virulence apparatus. Intern J Med Microbiol 291: 455-462
12. Cornelis GR, van Gijsegem F (2000) Assembly and function of type III secretory systems. Annu Rev Microbiol 54: 735-774
13. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833
14. Ecker JR, Davis RW (1987) Plant defense genes are regulated by ethylene. Proc Natl Acad Sci USA 84: 5202-5206
15. Felix G, Meins F (1985) Purification, immunoassay and characterization of an abundant, cytokinin-regulated polypeptide in cultured tobacco tissues: evidence the protein is a β-1,3-glucanase. Planta 164: 423-428
16. Figurski DH, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 76: 1648-1652
17. Fodor J, Hideg E, Kecskes A, Kiraly Z (2001) In vivo detection of tobacco mosaic virus-induced local and systemic oxidative burst by electron paramagnetic resonance spectroscopy. Plant Cell Physiol 42: 775-779
18. Freiberg C, Fellay R, Bairoch A, Broughton WJ, Rosenthal A, Perret X (1997) Molecular basis of symbiosis between Rhizobium and legumes. Nature 387: 394-401
19. Goormachtig S, Lievens S, Van de Velde W, van Montagu M, Holsters M (1998) Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. Plant Cell 10: 905-915
20. Gopalan S, Bauer DW, Alfano JR, Loniello AO, He SY, Collmer A (1996) Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8: 1095-1105
21. Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25: 989-994
22. Handberg K, Stougaard J (1992) Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J 2: 487-496
23. Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers S-G, Fraley R-T (1985) A simple and general method for transferring genes into plants. Science 227: 1229-1231
24. Jakab G, Droz E, Brigneti G, Baulcombe D, Malnoe P (1997) Infectious in vivo and in vitro transcripts from a full-length cDNA clone of PVY-N605, a Swiss necrotic isolate of potato virus Y. J Gen Virol 78: 3141-3145
25. Juris SJ, Rudolph AE, Huddler D, Orth K, Dixon JE (2000) A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Proc Natl Acad Sci USA 97: 9431-9436
26. Kang MK, Park KS, Choi D (1998) Coordinated expression of defense-related genes by TMV infection or salicylic acid treatment in tobacco. Mol Cells 8: 388-392
27. Kjemtrup S, Nimchuk Z, Dangl JL (2000) Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr Opin Microbiol 3: 73-78
28. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685
29. Lahaye T, Bonas U (2001) Molecular secrets of bacterial type III effector proteins. Trends Plant Sci 6: 479-485
30. Leister RT, Ausubel FM, Katagiri F (1996) Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc Natl Acad Sci USA 93: 15497-15502
31. Leubner-Metzger G, Meins F (2001) Antisense transformation reveals novel roles for class I β-1,3-glucanase in tobacco seed after-ripening and photodormancy. J Exp Bot 52: 1753-1759
32. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389
33. Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108: 743-754
34. Marie C, Broughton WJ, Deakin WJ (2001) Rhizobium type III secretion systems: legume charmers or alarmers? Curr Opin Plant Biol 4: 336-342
35. Marie C, Deakin WJ, Viprey V, Kopciñska J, Golinowski W, Krishnan HB, Perret X, Broughton WJ (2003) Characterisation of Nops, Nodulation Outer Proteins, secreted via the type III secretion system of NGR234. Mol Plant-Microbe Interact 16: 743-751
36. Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue: inhibition of fungal growth by combinations of chitinase and β-1, 3-glucanase. Plant Physiol 88: 936-942
37. Mithöfer A, Bhagwat AA, Feger M, Ebel J (1996) Suppression of fungal β-glucan-induced plant defence in soybean (Glycine max L.) by cyclic 1, 3-1, 6-β-glucans from the symbiont Bradyrhizobium japonicum. Planta 199: 270-275
38. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473-490
39. Murphy AM, Gilliland A, Wong C-E, West J, Singh DP, Carr JP (2001) Signal transduction in resistance to plant viruses. Eur J Plant Pathol 107: 121-128
40. Orth K, Palmer LE, Bao ZQ, Stewart S, Rudolph AE, Bliska JB, Dixon JE (1999) Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285: 1920-1923
41. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597
42. Perret X, Broughton WJ, Brenner S (1991) Canonical ordered cosmid library of the symbiotic plasmid of Rhizobium species NGR234. Proc Natl Acad Sci USA 88: 1923-1927
43. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201
44. Plano GV, Day JB, Ferracci F (2001) Type in export: new uses for an old pathway. Mol Microbiol 40: 284-293
45. Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher RA, Lange J, Wiemken A, Kim D, Cook DR, Boller T (2000) Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Mol Plant-Microbe Interact 13: 763-777
46. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, Ed 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
47. Shao F, Merritt PM, Bao Z, Innes RW, Dixon JE (2002) A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109: 575-588
48. Shinshi H, Mohnen D, Meins F (1987) Regulation of a plant pathogenesis-related enzyme: inhibition of chitinase and chitinase messenger RNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc Natl Acad Sci USA 84: 89-93
49. -) soybean nodules. Planta 187: 295-300
50. Staskawicz BJ, Mudgett MB, Dangl JL, Galan JE (2001) Common and contrasting themes of plant and animal diseases. Science 292: 2285-2289
51. Stepanova AN, Ecker JR (2000) Ethylene signaling: from mutants to molecules. Curr Opin Plant Biol 3: 353-360
52. Stiller J, Martirani L, Tuppale S, Chian RJ, Chiurazzi M, Gresshoff PM (1997) High frequency transformation and regeneration of transgenic plants in the model legume Lotus japonicus. J Exp Bot 48: 1357-1365
53. Szurek B, Rossier O, Hause G, Bonas U (2002) Type III-dependent translocation of the Xanthomonas AvrBs3 protein into the plant cell. Mol Microbiol 46: 13-23
54. Töpfer R, Matzeit V, Gronenborn B, Schell J, Steinbiss H-H (1987) A set of plant expression vectors for transcriptional and translational fusions. Nucleic Acids Res 15: 5890
55. van den Ackerveken G, Marois E, Bonas U (1996) Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87: 1307-1316
56. van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103: 753-765
57. Vasse J, de Billy F, Truchet G (1993) Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J 4: 555-566
58. Viprey V, Del Greco A, Golinowski W, Broughton WJ, Perret X (1998) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol 28: 1381-1389
59. Vögeli-Lange R, Frûndt C, Hart CM, Nagy F, Meins F (1994) Developmental, hormonal, and pathogenesis-related regulation of the tobacco class I β-1, 3-glucanase B promoter. Plant Mol Biol 25: 299-311
60. Voller A, Bartlett A, Bidwell DE, Clark MF, Adams AN (1976) The detection of viruses by enzyme-linked immunosorbent assay (ELISA). J Gen Virol 33: 165-167