An outer membrane autotransporter, AoaA, of Azorhizobium caulinodans is required for sustaining high N2-fixing activity of stem nodules

FEMS Microbiology Letters

Volumn 285, Issue 1, 2008, Pages 16-24

  Suzuki, Tadahiro ^a   Aono, Toshihiro ^a   Liu, Chi Te ^a   Suzuki, Shino ^a   Iki, Taichiro ^a   Yokota, Keisuke ^a   Oyaizu, Hiroshi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Autotransporter; Azorhizobium caulinodans; Exopolysaccharide; Pathogen response; Sesbania rostrata; Type V secretion system

Indexed keywords

CARRIER PROTEIN; EXOPOLYSACCHARIDE; NITROGEN; OUTER MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; AZORHIZOBIUM CAULINODANS; DNA SEQUENCE; GENE EXPRESSION; GENE SEQUENCE; NITROGEN FIXATION; NODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PLANT STEM; PRIORITY JOURNAL; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SESBANIA; SYMBIOSIS; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; AZORHIZOBIUM CAULINODANS; BACTERIAL OUTER MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NITROGEN FIXATION; PLANT PROTEINS; PLANT STEMS; PROTEIN TRANSPORT; SESBANIA;

AZORHIZOBIUM CAULINODANS; SESBANIA ROSTRATA;

EID: 47349118252     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2008.01215.x     Document Type: Article

References (53)

1. Aono T, Kanada N, Ijima A Oyaizu H (2001) The response of the phosphate uptake system and the organic acid exudation system to phosphate starvation in Sesbania rostrata. Plant Cell Physiol 42:1253 1264.
2. Bachem CW, van der Hoeven RS, de Bruijn SM, Vreugdenhil D, Zabeau M Visser RG (1996) Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. Plant J 9:745 753.
3. Bendtsen JD, Nielsen H, von Heijne G Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783 795.
4. Benedetti CE Arruda P (2002) Altering the expression of the chlorophyllase gene ATHCOR1 in transgenic Arabidopsis caused changes in the chlorophyll-to-chlorophyllide ratio. Plant Physiol 128:1255 1263.
5. Benedetti CE, Costa CL, Turcinelli SR Arruda P (1998) Differential expression of a novel gene in response to coronatine, methyl jasmonate, and wounding in the Coi1 mutant of Arabidopsis. Plant Physiol 116:1037 1042.
6. Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188 198.
7. Bölin I, Norlander L Wolf-Watz H (1982) Temperature-inducible outer membrane protein of Yersinia pseudotuberculosis and Yersinia enterocolitica is associated with the virulence plasmid. Infect Immun 37:506 512.
8. Chittoor JM, Leach JE White FF (1997) Differential induction of a peroxidase gene family during infection of rice by Xanthomonas oryzae pv. oryzae. Mol Plant-Microbe Interact 10:861 871.
9. Comanducci M, Bambini S, Brunelli B et al 2002) NadA, a novel vaccine candidate of Neisseria meningitidis. J Exp Med 195:1445 1454.
10. Cook D, Dreyer D, Bonnet D, Howell M, Nony E VandenBosch K (1995) Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7:43 55.
11. Corich V, Goormachtig S, Lievens S, Van Montagu M Holsters M (1998) Patterns of ENOD40 gene expression in stem-borne nodules of Sesbania rostrata. Plant Mol Biol 37:67 76.
12. Cotter PA, Yuk MH, Mattoo S, Akerley BJ, Boschwitz J, Relman DA Miller JF (1998) Filamentous hemagglutinin of Bordetella bronchiseptica is required for efficient establishment of tracheal colonization. Infect Immun 66:5921 5929.
13. Curtis MD, Rae AL, Rusu AG, Harrison SJ Manners JM (1997) A peroxidase gene promoter induced by phytopathogens and methyl jasmonate in transgenic plants. Mol Plant-Microbe Interact 10:326 338.
14. Dangl JL Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826 833.
15. Den Herder J, Lievens S, Rombauts S, Holsters M Goormachtig S (2007) A symbiotic plant peroxidase involved in bacterial invasion of the tropical legume Sesbania rostrata. Plant Physiol 144:717 727.
16. Desvaux M, Parham NJ Henderson IR (2004a) Type V protein secretio: simplicity gone awry? Curr Issues Mol Biol 6:111 124.
17. Desvaux M, Parham NJ Henderson IR (2004b) The autotransporter secretion system. Res Microbiol 155:53 60.
18. Dharmapuri S Sonti RV (1999) A transposon insertion in the gumG homologue of Xanthomonas oryzae pv. oryzae causes loss of extracellular polysaccharide production and virulence. FEMS Microbiol Lett 179:53 59.
19. Dreyfus B, Garcia JL Gillis M (1988) Characterization of Azorhizobium cauhodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated Sesbania rostrata. Int J Syst Bacteriol 38:1988.
20. Eulgem T, Rushton PJ, Robatzek S Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199 206.
21. Gu K, Yang B, Tian D et al 2005) R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122 1125.
22. Hammond-Kosack KE Jones JD (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575 607.
23. Harrison SJ, Curtis MD, McIntyre CL, Maclean DJ Manners JM (1995) Differential expression of peroxidase isogenes during the early stages of infection of the tropical forage legume Stylosanthes humilis by Colletotrichum gloeosporioides. Mol Plant-Microbe Interact 8:398 406.
24. Henderson IR, Navarro-Garcia F Nataro JP (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6:370 378.
25. Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC Ala'Aldeen D (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68:692 744.
26. Hoiczyk E, Roggenkamp A, Reichenbecher M, Lupas A Heesemann J (2000) Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J 19:5989 5999.
27. Inatsuka CS, Julio SM Cotter PA (2005) Bordetella filamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity. Proc Natl Acad Sci USA 102:18578 18583.
28. Ishibashi Y Nishikawa A (2002) Bordetella pertussis infection of human respiratory epithelial cells up-regulates intercellular adhesion molecule-1 expression: role of filamentous hemagglutinin and pertussis toxin. Microb Pathog 33:115 125.
29. Ishibashi Y Nishikawa A (2003) Role of nuclear factor-kappa B in the regulation of intercellular adhesion molecule 1 after infection of human bronchial epithelial cells by Bordetella pertussis. Microb Pathog 35:169 177.
30. Ishibashi Y, Claus S Relman DA (1994) Bordetella pertussis filamentous hemagglutinin interacts with a leukocyte signal transduction complex and stimulates bacterial adherence to monocyte CR3 (CD11b/CD18). J Exp Med 180:1225 1233.
31. Jacob-Dubuisson F, Locht C Antoine R (2001) Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol Microbiol 40:306 313.
32. Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA Walker GC (2008) Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci USA 105:704 709.
33. Kajava AV Steven AC (2006) The turn of the screw: variations of the abundant beta-solenoid motif in passenger domains of Type V secretory proteins. J Struct Biol 155:306 315.
34. Kariola T, Brader G, Li J Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17:282 294.
35. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM Peterson KM (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175 176.
36. Levy M, Edelbaum O Sela I (2004) Tobacco mosaic virus regulates the expression of its own resistance gene N. Plant Physiol 135:2392 2397.
37. Liu G, Sheng X, Greenshields DL, Ogieglo A, Kaminskyj S, Selvaraj G Wei Y (2005) Profiling of wheat class III peroxidase genes derived from powdery mildew-attacked epidermis reveals distinct sequence-associated expression patterns. Mol Plant-Microbe Interact 18:730 741.
38. McGuirk P, Johnson PA, Ryan EJ Mills KH (2000) Filamentous hemagglutinin and pertussis toxin from Bordetella pertussis modulate immune responses to unrelated antigens. J Infect Dis 182:1286 1289.
39. Passardi F, Cosio C, Penel C Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255 265.
40. Radwan O, Mouzeyar S, Nicolas P Bouzidi MF (2005) Induction of a sunflower CC-NBS-LRR resistance gene analogue during incompatible interaction with Plasmopara halstedii. J Exp Bot 56:567 575.
41. Rajeshwari R Sonti RV (2000) Stationary-phase variation due to transposition of novel insertion elements in Xanthomonas oryzae pv. oryzae. J Bacteriol 182:4797 4802.
42. Ray SK, Rajeshwari R, Sharma Y Sonti RV (2002) A high-molecular-weight outer membrane protein of Xanthomonas oryzae pv. oryzae exhibits similarity to non-fimbrial adhesins of animal pathogenic bacteria and is required for optimum virulence. Mol Microbiol 46:637 647.
43. Relman D, Domenighini M, Tuomanen E, Rappuoli R Falkow S (1989) Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci USA 86:2637 2641.
44. Relman D, Tuomanen E, Falkow S, Golenbock DT, Saukkonen K Wright SD (1990) Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61:1375 1382.
45. Simon R, Priefer A Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio-Technology 1:784 791.
46. Staehelin C, Forsberg LS, D'Haeze W et al 2006) Exo-oligosaccharides of Rhizobium sp. strain NGR234 are required for symbiosis with various legumes. J Bacteriol 188:6168 6178.
47. Suzuki S, Aono T, Lee KB, Suzuki T, Liu CT, Miwa H, Wakao S, Iki T Oyaizu H (2007) Rhizobial factors required for stem nodule maturation and maintenance in Sesbania rostrata-Azorhizobium caulinodans ORS571 symbiosis. Appl Environ Microbiol 73:6650 6659.
48. Tang JL, Feng JX, Li QQ, Wen HX, Zhou DL, Wilson TJ, Dow JM, Ma QS Daniels MJ (1996) Cloning and characterization of the rpfC gene of Xanthomonas oryzae pv. Oryzae: involvement in exopolysaccharide production and virulence to rice. Mol Plant-Microbe Interact 9:664 666.
49. Thompson JD, Higgins DG Gibson TJ (1994) Clustal-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673 4680.
50. Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T Takamiya K (1999) Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci USA 96:15362 15367.
51. Ulker B Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491 498.
52. Wells TJ, Tree JJ, Ulett GC Schembri MA (2007) Autotransporter proteins: novel targets at the bacterial cell surface. FEMS Microbiol Lett 274:163 172.
53. Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N Sasaki T (1998) Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95:1663 1668.