Dual effect of Mesorhizobium loti T3SS functionality on the symbiotic process

FEMS Microbiology Letters

Volumn 330, Issue 2, 2012, Pages 148-156

  Sánchez, Cintia ^a   Mercante, Virginia ^a   Babuin, María F ^b   Lepek, Viviana C ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^b Camino Circunvalacion   (Argentina)

Author keywords

Competitiveness; Effector; Lotus; Nodulation; Pili; Rhizobium

Indexed keywords

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; CONTROLLED STUDY; LOTUS; LOTUS JAPONICUS; LOTUS TENUIS; MESORHIZOBIUM; MESORHIZOBIUM LOTI; MLR6316 GENE; MLR6331 GENE; NODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SYMBIOSIS; TYPE III SECRETION SYSTEM;

BACTERIAL SECRETION SYSTEMS; GENES, REPORTER; LOTUS; MESORHIZOBIUM; PLANT ROOT NODULATION; RECOMBINANT FUSION PROTEINS;

LOTUS CORNICULATUS VAR. JAPONICUS; LOTUS TENUIS; MESORHIZOBIUM LOTI; RHIZOBIUM;

EID: 84859445836     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2012.02545.x     Document Type: Article

References (42)

1. Alfano JR & Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42: 385-414.
2. Bartsev AV, Deakin WJ, Boukli NM, McAlvin CB, Stacey G, Malnoe P, Broughton WJ & Staehelin C (2004) NopL, an effector protein of Rhizobium sp. NGR234, thwarts activation of plant defense reactions. Plant Physiol 134: 871-879.
3. Boureau T, Slamer S, Perino C, Gaubert S, Patrit O, Degrave A, Fagard M, Chevreau E & Barny MA (2011) The HrpN effector of Erwinia amylovora, which is involved in type III translocation, contiributes directly or indirectly to callose elicitation on apple leaves. Mol Plant Microbe Interact 24: 577-584.
4. Boyd AP, Lambermont I & Cornelis GR (2000) Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J Bacteriol 182: 4811-4821.
5. Broughton WJ & Dilworth MJ (1971) Control of leghemoglobin synthesis in snake beans. Biochem J 125: 1075-1080.
6. Cornelis GR (2002) Yersinia type III secretion: send in the effectors. J Cell Biol 158: 401-408.
7. D'Antuono AL, Casabuono A, Couto A, Ugalde RA & Lepek VC (2005) Nodule development induced by Mesorhizobium loti mutant strains affected in polysaccharide synthesis. Mol Plant Microbe Interact 18: 446-457.
8. Dai WJ, Zeng Y, Xie ZP & Staehelin C (2008) Symbiosis-promoting and deleterious effects of NopT, a novel type 3 effector of Rhizobium sp. strain NGR234. J Bacteriol 190: 5101-5110.
9. de Lyra MCCP, López-Baena FJ, Madinabeitia N, Vinardell JM, Espuny MR, Cubo MT, Bellogín RA, Ruiz-Sainz JE & Ollero FJ (2006) Inactivation of the Sinorhizobium fredii HH103 rhcJ gene abolishes nodulation outer proteins (Nops) secretion and decreases the symbiotic capacity with soybean. Int Microbiol 9: 125-133.
10. Deng W, Li Y, Hardwidge PR, Frey WA, Pfuetzner RA, Lee S, Gruenheid S, Strynakda NCJ, Puente JL & Finlay BB (2005) Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect Immun 73: 2135-2146.
11. Douglas CJ, Staneloni RJ, Rubin RA & Nester EW (1985) Identification and genetic analysis of an Agrobacterium tumefaciens chromosomal virulence region. J Bacteriol 161: 850-860.
12. Galán JE (2001) Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17: 53-86.
13. Gosh P (2004) Process of protein transport by the type III secretion system. Microbiol Mol Biol Rev 68: 771-795.
14. Grant SR, Fisher EJ, Chang JH, Mole BM & Dangl L (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60: 425-429.
15. BAD Promoter. J Bacteriol 177: 4121-4130.
16. Hubber A, Vergunst AC, Sullivan JT, Hooykaas PJJ & Ronson CW (2004) Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol Microbiol 54: 561-574.
17. Kambara K, Ardissone S, Kobayashi H, Saad MM, Schumpp O, Broughton WJ & Deakin WJ (2009) Rhizobia utilize pathogen-like effector proteins during symbiosis. Mol Microbiol 71: 92-106.
18. Kaneko T, Nakamura Y, Sato S et al. (2000a) Complete genome structure of the nitrogen-fixing bacterium Mesorhizobium loti. DNA Res 7: 331-338.
19. Kaneko T, Nakamura Y, Sato S et al. (2000b) Complete genome structure of the nitrogen-fixing bacterium Mesorhizobium loti (Supplement). DNA Res 7: 381-406.
20. Krause A, Doerfel A & Göttfert M (2002) Mutational and transcriptional analysis of the type III secretion system of Bradyrhizobium japonicum. Mol Plant Microbe Interact 15: 1228-1235.
21. Lagares A, Caetano-Anollés G, Niehaus K, Lorenzen J, Ljunggren HD, Puhler A & Favelukes G (1992) A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa. J Bacteriol 174: 5941-5952.
22. Lee VT, Mazmanian SK & Schneewind O (2001) A program of Yersinia enterocolitica type III secretion reactions is activated by specific signals. J Bacteriol 183: 4970-4978.
23. López-Lara IM, van den Berg JDJ, Thomas-Oates JE, Glushka J, Lugtenberg BJJ & Spaink HP (1995) Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol Microbiol 15: 627-638.
24. Lorio JC, Kim WW & Krishnan HB (2004) NopB, a soybean cultivar-specificity protein from Sinorhizobium fredii USDA257, is a type III secreted protein. Mol Plant Microbe Interact 17: 1259-1268.
25. Marie C, Deakin WJ, Ojanen-Reuhs T, Diallo E, Reuhs B, Broughton WJ & Perret X (2004) TtsI, a key regulator of Rhizobium species NGR234 is required for type III-dependent protein secretion and synthesis of rhamnose-rich polysaccharides. Mol Plant Microbe Interact 17: 958-966.
26. McDermott TR & Graham PH (1990) Competitive ability and efficiency in nodule formation of strains of Bradyrhizobium japonicum. Appl Environ Microbiol 56: 3035-3039.
27. Oh HS, Park DH & Collmer A (2010) Components of the Pseudomonas syringae type III secretion system can suppress and may elicit plant innate immunity. Mol Plant Microbe Interact 23: 727-739.
28. Okazaki S, Okabe S, Higashi M, Shimoda Y, Sato S, Tabata S, Hashiguchi M, Akashi R, Göttfert M & Saeki K (2010) Identification and functional analysis of type III effector proteins in Mesorhizobium loti. Mol Plant Microbe Interact 23: 223-234.
29. Rodrigues JA, López-Baena FJ, Ollero FJ et al. (2007) NopM and NopD are rhizobial nodulation outer proteins: identification using LC-MALDI and LC-ESI with a monolithic capillary column. J Proteome Res 6: 1029-1037.
30. Rüssmann H, Kubori T, Sauer J & Galán JE (2002) Molecular and functional analysis of the type III secretion signal of the Salmonella enterica InvJ protein. Mol Microbiol 46: 769-779.
31. Saad MM, Staehelin C, Broughton WJ & Deakin WJ (2008) Protein-protein interactions within type III secretion system-dependent pili of Rhizobium sp. strain NGR234. J Bacteriol 190: 750-754.
32. Sánchez C, Iannino F, Deakin WJ, Ugalde RA & Lepek VC (2009) Characterization of the Mesorhizobium loti MAFF303099 type-three protein secretion system. Mol Plant Microbe Interact 22: 519-528.
33. Shimoda Y, Mitsui H, Kamimatsuse H et al. (2008a) Construction of signature-tagged mutant library in Mesorhizobium loti as a powerful tool for functional genomics. DNA Res 15: 297-308.
34. Shimoda Y, Shinpo S, Kohara S, Nakamura M, Tabata Y & Sato S (2008b) A large scale analysis of protein-protein interactions in the nitrogen-fixing bacterium Mesorhizobium loti. DNA Res 15: 13-23.
35. Simon R, Priefer U & Pühler (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Techology 1: 784-791.
36. Skorpil P, Saad MM, Boukli NM, Kobayashi H, Ares-Orpel F, Broughton WJ & Deakin WJ (2005) NopP, a phosphorylated effector of Rhizobium sp. strain NGR234, is a major determinant of nodulation of the tropical legumes Flemingia congesta and Tephrosia vogelii. Mol Microbiol 57: 1304-1317.
37. Spano S, Ugalde JE & Galán JE (2008) Delivery of a Salmonella Typhi exotoxin from a host intracellular compartment. Cell Host Microbe 3: 30-38.
38. Vincent JM (1970) A Manual for the Practical Study of Root Nodule Bacteria. Blackwell Scientific Publications, Oxford.
39. Vinuesa P, Neumann-Sllkow F, Pacios-Bras C, Spaink HP, Martínez-Romero E & Werner D (2002) Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness. Mol Plant Microbe Interact 16: 159-168.
40. 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.
41. Wassem R, Kobayashi H, Kambara K, Le Quéré A, Walker GC, Broughton WJ & Deakin WJ (2008) TtsI regulates symbiotic genes in Rhizobium species NGR234 by binding to tts boxes. Mol Microbiol 68: 736-748.
42. Yang Y, Zhao J, Morgan RL, Ma W & Jiang T (2010) Computational prediction of type III secreted proteins from gram-negative bacteria. BMC Bioinformatics 11(Suppl. 1): S47.