Genetic analysis of a pH-regulated operon from Rhizobium tropici CIAT899 involved in acid tolerance and nodulation competitiveness

Molecular Plant-Microbe Interactions

Volumn 16, Issue 2, 2003, Pages 159-168

  Vinuesa, Pablo ^a,c   Neumann Silkow, Frauke ^a   Pacios Bras, Cristina ^b   Spaink, Herman P ^b   Martínez Romero, Esperanza ^c   Werner, Dietrich ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b LEIDEN UNIVERSITY   (Netherlands)

^c INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

GusA; Lipolytic enzymes; Symbiosis

Indexed keywords

EUKARYOTA; FIRMICUTES; GAMMAPROTEOBACTERIA; INSERTION SEQUENCES; PHASEOLUS VULGARIS; PROTEOBACTERIA; RHIZOBIUM; RHIZOBIUM TROPICI;

EID: 0037306656     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2003.16.2.159     Document Type: Article

References (63)

1. Aarons, S. R., and Graham, P. H. 1991. Response of Rhizobium leguminosarum bv. phaseoli to acidity. Plant and Soil 134:145-151.
2. Aranda-Rickert, A., Soria, M. A., and Correa, O. S. 2000. The adaptive acid response in Mesorhizobium sp. World J. Microbiol. Biotechnol. 16:475-480.
3. Arpigny, J. L., and Jaeger, K.-E. 1999. Bacterial lipolytic enzymes: Classification and properties. Biochem. J. 343:177-183.
4. Brady, L., Brzozowski, A. M., Derewenda, Z. S., Dodson, E., Doson, G., Tolley, S., Turkenburg, J. P., Christiansen, L., Huge-Jensen, B., Norskov, L., Thim, L., and Menge, U. 1990. A serine protease triad forms the catalytic centre of a triacylglycerol lipase. Nature 343:767-770.
5. Brumlik, M. J., and Buckley, J. T. 1996. Identification of the catalytic triad of the lipase/acyltransferase from Aeromonas hydrophila. J. Bacteriol. 178:2060-2064.
6. Cermola, M., Fedorova, E., Tate, R., Riccio, A., Favre, R., and Patriarca, E. J. 2000. Nodule invasion and symbiosome differentiation during Rhizobium etli-Phaseolus vulgaris symbiosis. Mol. Plant-Microbe Interact. 13:733-741.
7. Chen, H., Richardson, A. E., and Rolfe, B. G. 1993. Studies of the physiological and genetic basis of acid tolerance in Rhizobium leguminosarum biovar trifolii. Appl. Environ. Microbiol. 6:1798-1804.
8. Figurski, D. H., and Helinski, D. R. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. 76:1648-1652.
9. Foster, J. W. 1999. When protons attack: Microbial strategies of acid adaptation. Curr. Opin. Microbiol. 2:170-174.
10. Fujiwara, A., Takamura, H., Majumder, P., Yoshida, H., and Kojima, M. 1998. Functional analysis of the protein encoded by the chromosomal virulence gene (acvB) of Agrobacterium tumefaciens. Ann. Phytopathol. Soc. Jpn. 64:191-193.
11. Galibert, F., Finan, T. M., Long, S. R., Puhler, A., Abola, P., Ampe, F., Barloy-Hubler, F., Barnett, M. J., Becker, A., Boistard, P., Bothe, G., Boutry, M., Bowser, L., Buhrmester, J., Cadieu, E., Capela, D., Chain, P., Cowie, A., Davis, R. W., Dreano, S., Federspiel, N. A., Fisher, R. F., Gloux, S., Godrie, T., Goffeau, A., Golding, B., Gouzy, J., Gurjal, M., Hernandez-Lucas, I., Hong, A., Huizar, L., Hyman, R. W., Jones, T., Kahn, D., Kahn, M. L., Kalman, S., Keating, D. H., Kiss, E., Komp, C., Lelaure, V., Masuy, D., Palm, C., Peck, M. C., Pohl, T. M., Portetelle, D., Purnelle, B., Ramsperger, U., Surzycki, R., Thebault, P., Vandenbol, M., Vorholter, F. J., Weidner, S., Wells, D. H., Wong, K., Yeh, K. C., and Batut, J. 2001. The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668-672.
12. García-Olmedo, F., Molina, A., Alamillo, J. M., and Rodríguez-Palenzuela, P. 1998. Plant defense peptides. Biopolymers 47:479-491.
13. Glenn, A. R., Reeve, W. G., Tiwari, R. P., and Dilworth, M. J. 1999. Acid tolerance in root nodule bacteria. Pages 112-130 in: Bacterial Responses to pH. R. I. Booth, ed. Wiley, Chichester, U.K.
14. Goss, T. J., O'Hara, G. W., Dilworth, M. J., and Glenn, A. R. 1990. Cloning, characterization, and complementation of lesions causing acid sensitivity in Tn5-induced mutants of Rhizobium meliloti WSM419. J. Bacteriol. 172:5173-5179.
15. Graham, P. H., Viteri, S. E., Mackie, F., Vargas, A. A. T., and Palacios, A. 1982. Variation in acid soil tolerance among strains of Rhizobium phaseoli. Field Crop Res. 5:121-128.
16. Graham, P. H., Draeger, K. J., Ferrey, M. L., Conroy, M. J., Hammer, B. E., Martínez, E., Aarons, S. R., and Quinto, C. 1994. Acid pH tolerance in strains of Rhizobium and Bradyrhizobium, and initial studies on the basis for acid tolerance of Rhizobium tropici UMR1899. Can. J. Microbiol. 40:189-207.
17. Howieson, J. G., and Ewing, M. A. 1986. Acid tolerance in the Rhizobium meliloti-Medicago symbiosis. Aust. J. Agric. Res. 37:153-155.
18. Jaeger, K.-E., Dijkstra, B. W., and Reetz, M. T. 1999. Bacterial biocatalysts: Molecular biology, three-dimensional structures, and biotechnological applications of lipases. Ann. Rev. Microbiol. 53:315-351.
19. Kalogeraki, V. S., and Winans, S. C. 1995. The octopine-type Ti plasmid pTiA6 of Agrobacterium tumefaciens contains a gene homologous to the chromosomal virulence gene acvB. J. Bacteriol. 177:892-897.
20. Kang, H. W., Wirawan, I. G. P., and Kojima, M. 1994. Cellular localization and functional analysis of the protein encoded by chromosomal virulence gene (acvB) of Agrobacterium tumefaciens. Biosci. Biotech. Biochem. 58:2024-2032.
21. Kingsley, M. T., and Bohlool, B. B. 1992. Extracellular polysaccharide is not responsible for aluminum tolerance of Rhizobium leguminosarum bv. phaseoli CIAT899. Appl. Environ. Microbiol. 58:1095-1101.
22. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M. II, and Peterson, K. M. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic resistance cassettes. Gene 166:175-176.
23. LeVier, K., Phillips, R. W., Grippe, V. K., Roop, R. M. II, and Walker, G. C. 2000. Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492-2493.
24. Majumder, P., Takagi, K., Shioiri, H., Nozue, M., and Kojima, M. 1999. Functional analysis of two chromosomal virulence genes chvA and acvB of Agrobacterium tumefaciens using avirulent mutants with transposon 5 insertion in the respective gene. Ann. Phytopathol. Soc. Jpn. 65:254-263.
25. Marschner, H. 1995. Mineral Nutrition of Higher Plants. Academic Press, London.
26. Martínez-Romero, E., Segovia, L., Mercante, F. M., Franco, A. A., Graham, P., and Pardo, M. A. 1991. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. Syst. Bacteriol. 41:417-426.
27. Matsumoto, S., Machida, Y., and Tabeke, I. 1986. A rapid method for assaying tumorigenicity of Agrobacterium tumefaciens. Plant Mol. Biol. Rep. 4:42-47.
28. Mellor, R. B. 1989. Bacteroids in the Rhizobium-legume symbiosis inhabit a plant internal lytic compartment: Implications for other microbial endosymbioses. J. Exp. Bot. 40:831-839.
29. Nogales, J., Campos, R., BenAbdelkhalek, H., Olivares, J., Lluch, C., and Sanjuan, J. 2002. Rhizobium tropici genes involved in free-living salt tolerance are required for the establishment of efficient nitrogen-fixing symbiosis with Phaseolus vulgaris. Mol. Plant-Microbe Interact. 15:225-232.
30. O'Hara, G. W., and Glenn, A. R. 1994. The adaptive acid tolerance response in root nodule bacteria and Escherichia coli. Arch. Microbiol. 161:286-292.
31. O'Hara, G. W., Goss, T. J., Dilworth, M. J., and Glenn, A. R. 1989. Maintenance of intracellular pH and acid tolerance in Rhizobium meliloti. Appl. Environ. Microbiol. 55:1870-1876.
32. Oke, V., and Long, S. R. 1999a. Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol. Microbiol. 32:837-849.
33. Oke, V., and Long, S. R. 1999b. Bacteroid formation in the Rhizobium-legume symbiosis. Curr. Opin. Microbiol. 2:641-646.
34. Pan, S. Q., Jin, S., Boulton, M. I., Hawes, M., Gordon, P. M., and Nester, E. W. 1995. An Agrobacterium virulence factor encoded by a Ti plasmid gene or a chromosomal gene is required for T-DNA transfer into plants. Mol. Microbiol. 17:59-269.
35. Parniske, M. 2000. Intracellular accommodation of microbes by plants: A common developmental program for symbiosis and disease? Curr. Opin. Plant Biol. 3:320-328.
36. Peick, B., Graumann, P., Schmid, R., Marahhiel, M., and Werner, D. 1999. Differential pH-induced proteins in Rhizobium tropici CIAT899 and Rhizobium etli CIAT611. Soil Biol. Biochem. 31:189-194.
37. Peschel, A., Jack, R. W., Otto, M., Collins, L. V., Staubitz, P., Nicholson, G., Kalbacher, H., Nieuwenhuizen, W. F., Jung, G., Tarkowski, A., van Kessel, K. P., and van Strijp, J. A. 2001. Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with 1-lysine. J. Exp. Med. 193:1067-1076.
38. Pillai, S. D., Josephson, K. L., Bailey, R. L., and Pepper, I. L. 1992. Specific detection of rhizobia in root nodules and soil using the polymerase chain reaction. Soil Biol. Biochem. 24:885-891.
39. Priefer, U. B., Aurag, J., Boesten, B., Bouhmouch, I., Defez, R., Filali-Maltouf, A., Miklis, M., Moawad, H., Mouhsine, B., Prell, J., Schluter, A., and Senatore, B. 2001. Characterisation of Phaseolus symbionts isolated from Mediterranean soils and analysis of genetic factors related to pH tolerance. J. Biotechnol. 91:223-236.
40. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Reviews 57:50-108.
41. Rainey, P. B. 1999. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1:243-257.
42. Reese, M. G., Harris, N. L., and Eeckman, F. H. 1995. Large scale sequencing specific neural networks for promoter and splice site recognition. Pages 737-738 in: Biocomputing: Proceedings of the 1996 Pacific Symposium. L. Hunter and T. Klein, eds. World Scientific Publishing Co., Singapore.
43. Riccillo, P., Muglia, C., de Bruijn, F. J., Roe, A., Booth, I. R., and Aguilar, M. 2000. Glutathione is involved in environmental stress response in Rhizobium tropici, including acid tolerance. J. Bacteriol. 182:1748-1753.
44. Roth, L. E., Jeon, K. W., and Stacey, G. 1988. Homology in endosymbiotic systems: The term 'symbiosome.' Pages 220-225 in: Molecular Genetics of Plant-Microbe Interactions. R. Palacios and D. P. S. Verma, eds. American Phytopathological Society Press, St. Paul, MN, U.S.A.
45. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
46. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, G., Thierbach, G., and Pühler, A. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: Selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73.
47. Simon, R., Priefer, U., and 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.
48. Somasegaran, P., and Hoben, H. J. 1994. Handbook for rhizobia: Methods in legume-Rhizobium technology, Springer-Verlag, Heidelberg, Germany.
49. Steele, H., Vinuesa, P., Strümpeler, M., Schmid, R., and Werner, D. 2000. 2D SDS-PAGE analysis of proteins involved in acid tolerance in Rhizobium tropici CIAT899. Pages 481-482 in: Nitrogen Fixation: From Molecules to Crop Productivity. F. O. Pedrosa, M. Hungria, M. G. Yates, and W. E. Newton, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
50. Streit, W., Kosch, K., and Werner, D. 1992. Nodulation competitiveness of Rhizobium leguminosarum bv. phaseoli and Rhizobium tropici strains measured by glucuronidase (gusA) gene fusion. Biol. Fertil. Soils 14:140-144.
51. Tatusov, R. L., Natale, D. A., Garkavtsev, I. V., Tatusova, T. A., Shankavaram, U. T., Rao, B. S., Kiryutin, B., Galperin, M. Y., Fedorova, N. D., and Koonin, E. V. 2001. The COG database: New developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res. 29:22-8.
52. Udvardi, M. K., and Day, D. A. 1997. Metabolite transport across symbiotic membranes of legume nodules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:493-523.
53. Vargas, C., Martinez, J. L., Megias, M., and Quinto, C. 1990. Identification and cloning of nodulation genes and host specificity determinants of the broad host-range Rhizobium leguminosarum biovar phaseoli strain CIAT899. Mol. Microbiol. 11:1899-1910.
54. Vinuesa, P., Reuhs, B. L., Breton, C., and Werner, D. 1999. Identification of a plasmid-borne locus in Rhizobium etli KIM5s involved in lipopolysaccharide O-chain biosynthesis and nodulation of Phaseolus vulgaris. J. Bacteriol. 181:5606-5614.
55. Vlassak, K., Vanderleyden, J., and Franco, A. 1996. Competition and persistence of Rhizobium tropici and Rhizobium etli in tropical soil during successive bean (Phaseolus vulgaris L.) cultures. Biol. Fertil. Soils 21:61-68.
56. Werner, D., Wilcockson, J., and Zimmermann, E. 1975. Adsorption and selection of rhizobia by ion exchange papers. Arch. Microbiol. 105:27-32.
57. Wilson, K. 1990. Preparation of genomic DNA from bacteria. Pages 241-245 in: Current Protocols in Molecular Biology. F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl, eds. Greene Publishing Associates and John Wiley & Sons, New York.
58. Wilson, K. J., Sessisch, A., C., C. J., Giller, K. E., Akkermans, A. D. L., and Jefferson, R. A. 1995. β-glucuronidase (GUS) transposons for ecological and genetic studies of rhizobia and other gram-negative bacteria. Microbiology. 141:1691-1705.
59. Wirawan, G. P., Kang, H. W., and Kojima, M. 1993. Isolation and characterization of a new chromosomal virulence gene of Agrobacterium tumefaciens. J. Bacteriol. 175:3208-3212.
60. Wood, D. W., Setubal, J. C., Kaul, R., Monks, D. E., Kitajima, J. P., Okura, V. K., Zhou, Y., Chen, L., Wood, G. E., Almeida, N. F., Jr., Woo, L., Chen, Y., Paulsen, I. T., Eisen, J. A., Karp, P. D., Bovee, D., Sr., Chapman, P., Clendenning, J., Deatherage, G., Gillet, W., Grant, C., Kutyavin, T., Levy, R., Li, M. J., McClelland, E., Palmieri, A., Raymond, C., Rouse, G., Saenphimmachak, C., Wu, Z., Romero, P., Gordon, D., Zhang, S., Yoo, H., Tao, Y., Biddle, P., Jung, M., Krespan, W., Perry, M., Gordon-Kamm, B., Liao, L., Kim, S., Hendrick, C., Zhao, Z. Y., Dolan, M., Chumley, F., Tingey, S. V., Tomb, J. F., Gordon, M. P., Olson, M. V., and Nester, E. W. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317-2323.
61. Zahran, H. H. 1999. Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in arid climate. Microbiol. Mol. Biol. Rev. 63:968-989.
62. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389-395.
63. Zhu, J., Oger, P. M., Schrammeijer, B., Hooykaas, P. J., Farrand, S. K., and Winans, S. C. 2000. The bases of crown gall tumorigenesis. J. Bacteriol. 182:3885-3895.