Transcriptome analysis of Sinorhizobium melilotiduring symbiosis

Genome Biology

Volumn 4, Issue 2, 2003, Pages

  Ampe, Frederic ^a   Kiss, Ernö ^a   Sabourdy, Frédérique ^a   Batut, Jacques ^a  

^a CNRS   (France)

Author keywords

Additional Data File; Infection Thread; Luteolin; Oxygen Limitation; Symbiotic Bacterium

Indexed keywords

ALFALFA; ARTICLE; CLUSTER ANALYSIS; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METHODOLOGY; MICROBIOLOGY; NITROGEN FIXATION; PLANT ROOT; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, PLANT; MEDICAGO SATIVA; NITROGEN FIXATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT ROOTS; SINORHIZOBIUM MELILOTI; SYMBIOSIS; TRANSCRIPTION, GENETIC;

EID: 0037270254     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2003-4-2-r15     Document Type: Article

References (62)

1. Denarié J, Debellé F, Promé JC: Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem. 1996, 65: 503-535. 10.1146/annurev.biochem.65.1.503. DOI: 10.1146/annurev.bi.65.070196.002443
2. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J: Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell. 2000, 12: 1647-1666. 10.1105/tpc.12.9.1647. DOI: 10.1105/tpc.12.9.1647
3. Pellock BJ, Cheng HP, Walker GC: Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides. J Bacteriol. 2000, 182: 4310-4318. 10.1128/JB.182.15.4310-4318.2000. DOI: 10.1128/JB.182.15.4310-4318.2000
4. Santos R, Herouart D, Puppo A, Touati D: Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Mol Microbiol. 2000, 38: 750-759. 10.1046/j.1365-2958.2000.02178.x. DOI: 10.1046/j.1365-2958.2000.02178.x
5. Vasse J, de Billy F, Camut S, Truchet G: Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol. 1990, 172: 4295-4306.
6. Brewin NJ: Tissue and cell invasion by Rhizobium: the structure and development of infection threads and symbiosomes. In The Rhizobiaceae. Edited by: Spaink HP, Kondorosi A, Hooykaas PJJ. 1998, Dordrecht: Kluwer Academic Publishers, 417-429. DOI: 10.1007/978-94-011-5060-6_22
7. Ferguson GP, Roop RM, Walker GC: Deficiency of a Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of the cell envelope. J Bacteriol. 2002, 184: 5625-5632. 10.1128/JB.184.20.5625-5632.2002. DOI: 10.1128/JB.184.20.5625-5632.2002
8. Glazebrook J, Ichige A, Walker GC: A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev. 1993, 7: 1485-1497. DOI: 10.1101/gad.7.8.1485
9. Watson RJ, Chan YK, Wheatcroft R, Yang AF, Han SH: Rhizobium meliloti genes required for C4-dicarboxylate transport and symbiotic nitrogen fixation are located on a megaplasmid. J Bacteriol. 1988, 170: 927-934.
10. Kaminski PA, Batut J, Boistard P: A survey of nitrogen fixation by rhizobia. In The Rhizobiaceae. Edited by: Spaink HP, Kondorosi A, Hooykaas PJJ. 1998, Dordrecht: Kluwer Academic Publishers, 431-460. DOI: 10.1007/978-94-011-5060-6_23
11. Soupène E, Foussard M, Boistard P, Truchet G, Batut J: Oxygen as a key developmental regulator of Rhizobium meliloti N2-fixation gene expression within the alfalfa root nodule. Proc Natl Acad Sci USA. 1995, 92: 3759-3763. DOI: 10.1073/pnas.92.9.3759
12. Perret X, Freiberg C, Rosenthal A, Broughton WJ, Fellay R: High-resolution transcriptional analysis of the symbiotic plasmid of Rhizobium sp. NGR234. Mol Microbiol. 1999, 32: 415-425. 10.1046/j.1365-2958.1999.01361.x. DOI: 10.1046/j.1365-2958.1999.01361.x
13. Galibert F, Finan TM, Long SR, Puhler A, Abola P, Ampe F, Barloy-Hubler F, Barnett MJ, Becker A, Boistard P, et al: The composite genome of the legume symbiont Sinorhizobium meliloti. Science. 2001, 293: 668-672. DOI: 10.1126/science.1060966
14. Infection macroarray. [http://sequence.toulouse.inra.fr/rhime/Expression/Infection/Infection_macro-array_2002.htm]
15. Bénaben V, Duc G, Lefebvre V, Huguet T: TE7, an inefficient mutant of Medicago truncatula Gaertn. cv Jemalong. Plant Physiol. 1995, 107: 53-62.
16. Cabanes D, Boistard P, Batut J: Symbiotic induction of pyruvate dehydrogenase genes from Sinorhizobium meliloti. Mol Plant-Microbe Interact. 2000, 13: 483-493. DOI: 10.1094/MPMI.2000.13.5.483
17. Oke V, Long SR: Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol Microbiol. 1999, 32: 837-849. 10.1046/j.1365-2958.1999.01402.x. DOI: 10.1046/j.1365-2958.1999.01402.x
18. Davey ME, de Bruijn FJ: A homologue of the tryptophan-rich sensory protein TspO and FixL regulate a novel nutrient deprivation-induced Sinorhizobium meliloti locus. Appl Environ Microbiol. 2000, 66: 5353-5359. 10.1128/AEM.66.12.5353-5359.2000. DOI: 10.1128/AEM.66.12.5353-5359.2000
19. Schlaman HR, Horvath B, Vijgenboom E, Okker RJ, Lugtenberg BJ: Suppression of nodulation gene expression in bacteroids of Rhizobium leguminosarum biovar viciae. J Bacteriol. 1991, 173: 4277-4287.
20. Timmers AC, Auriac MC, de Billy F, Truchet G: Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development. 1998, 125: 339-349.
21. Chen H, Higgins J, Oresnik IJ, Hynes MF, Natera S, Djordjevic MA, Weinman JJ, Rolfe BG: Proteome analysis demonstrates complex replicon and luteolin interactions in pSymA-cured derivatives of Sinorhizobium meliloti strain 2011. Electrophoresis. 2000, 21: 3833-3842. 10.1002/1522-2683(200011)21:17<3833::AID-ELPS3833>3.0.CO;2-I. DOI: 10.1002/1522-2683(200011)21:17<3833::AID-ELPS3833>3.0.CO;2-I
22. Wexler M, Yeoman KH, Stevens JB, de Luca NG, Sawers G, Johnston AW: The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron. Mol Microbiol. 2001, 41: 801-816. 10.1046/j.1365-2958.2001.02556.x. DOI: 10.1046/j.1365-2958.2001.02556.x
23. Minnick MF, Mitchell SJ, McAllister SJ: Cell entry and the pathogenesis of Bartonella infections. Trends Microbiol. 1996, 4: 343-347. 10.1016/0966-842X(96)10055-X. DOI: 10.1016/0966-842X(96)10055-X
24. Capela D, Barloy-Hubler F, Gouzy J, Bothe G, Ampe F, Batut J, Boistard P, Becker A, Boutry M, Cadieu E, et al: Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti. Proc Natl Acad Sci USA. 2001, 98: 9877-9882. 10.1073/pnas.161294398. DOI: 10.1073/pnas.161294398
25. Katz ME, Wright CL, Gartside TS, Cheetham BF, Doidge CV, Moses EK, Rood JI: Genetic organization of the duplicated vap region of the Dichelobacter nodosus genome. J Bacteriol. 1994, 176: 2663-2669.
26. Sigaud S, Becquet V, Frendo P, Puppo A, Herouart D: Differential regulation of two divergent Sinorhizobium meliloti genes for HPII-like catalases during free-living growth and protective role of both catalases during symbiosis. J Bacteriol. 1999, 181: 2634-2639.
27. Cheng HP, Walker GC: Succinoglycan production by Rhizobium meliloti is regulated through the ExoS-ChvI two-component regulatory system. J Bacteriol. 1998, 180: 20-26.
28. Natera SH, Guerreiro N, Djordjevic MA: Proteome analysis of differentially displayed proteins as a tool for the investigation of symbiosis. Mol Plant Microbe Interact. 2000, 13: 995-1009. DOI: 10.1094/MPMI.2000.13.9.995
29. Gage DJ, Bobo T, Long SR: Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). J Bacteriol. 1996, 178: 7159-7166.
30. Quail MA, Guest JR: Purification characterization and mode of action of PdhR, the transcriptional repressor of the pdhR-aceEF-lpd operon of Escherichia coli. Mol Microbiol. 1995, 15: 519-529. DOI: 10.1111/j.1365-2958.1995.tb02265.x
31. Ogawa J, Long SR: The Rhizobium meliloti groELc locus is required for regulation of early nod genes by the transcription activator NodD. Genes Dev. 1995, 9: 714-729. DOI: 10.1101/gad.9.6.714
32. Ercolano E, Mirabella R, Merrick M, Chiurazzi M: The Rhizobium leguminosarum glnB gene is down-regulated during symbiosis. Mol Gen Genet. 2001, 264: 555-564. 10.1007/s004380000333. DOI: 10.1007/s004380000333
33. Djordjevic MA, Natera SH, Chen HC, Weiller G, Menzel C, van Noorden G, Weinman J, Taylor S, Guo J, Rolfe BG: Proteome analysis of Sinorhizobium meliloti. In Nitrogen Fixation, Global Perspective 2002. Edited by: Finan TM, O'Brian MR, Layzell DB, Vessey JK, Newton W. 2002, Oxford: CABI, 50-54.
34. Hentschel U, Steinert M, Hacker J: Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol. 2000, 8: 226-231. 10.1016/S0966-842X(00)01758-3. DOI: 10.1016/S0966-842X(00)01758-3
35. LeVier K, Phillips RW, Grippe VK, Roop RM, Walker GC: Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science. 2000, 287: 2492-2493. 10.1126/science.287.5462.2492. DOI: 10.1126/science.287.5462.2492
36. Barnett MJ, Fisher RF, Jones T, Komp C, Abola AP, Barloy-Hubler F, Bowser L, Capela D, Galibert F, Gouzy J, et al: Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci USA. 2001, 98: 9883-9888. 10.1073/pnas.161294798. DOI: 10.1073/pnas.161294798
37. Chen L, Chen Y, Wodd DW, Nester EW: A new type IV secretion system promotes conjugal transfer in Agrobacterium tumefaciens. J Bacteriol. 2002, 184: 4838-4845. 10.1128/JB.184.17.4838-4845.2002. DOI: 10.1128/JB.184.17.4838-4845.2002
38. Ratledge C, Dover LG: Iron metabolism in pathogenic bacteria. Annu Rev Microbiol. 2000, 54: 881-941. 10.1146/annurev.micro.54.1.881. DOI: 10.1146/annurev.micro.54.1.881
39. Santos R, Herouart D, Sigaud S, Touati D, Puppo A: Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol Plant Microbe Interact. 2001, 14: 86-89. DOI: 10.1094/MPMI.2001.14.1.86
40. Hérouart D, Sigaud S, Moreau S, Frendo P, Touati D, Puppo A: Cloning and characterization of the katA gene of Rhizobium meliloti encoding a hydrogen peroxide-inducible catalase. J Bacteriol. 1996, 178: 6802-6809.
41. Imlay KR, Imlay JA: Cloning and analysis of sodC encoding the copper-zinc superoxide dismutase of Escherichia coli. J Bacteriol. 1996, 178: 2564-2571.
42. Won SH, Lee BH, Lee HS, Jo J: An Ochrobactrum anthropi gene conferring paraquat resistance to the heterologous host Escherichia coli. Biochem Biophys Res Commun. 2001, 285: 885-890. 10.1006/bbrc.2001.5268. DOI: 10.1006/bbrc.2001.5268
43. Nienaber A, Hennecke H, Fischer HM: Discovery of a haem uptake system in the soil bacterium Bradyrhizobium japonicum. Mol Microbiol. 2001, 41: 787-800. 10.1046/j.1365-2958.2001.02555.x. DOI: 10.1046/j.1365-2958.2001.02555.x
44. Lynch D, O'Brien J, Welch T, Clarke P, Cuiv PO, Crosa JH, O'Connell M: Genetic organization of the region encoding regulation biosynthesis and transport of rhizobactin 1021, a siderophore produced by Sinorhizobium meliloti. J Bacteriol. 2001, 183: 2576-2585. 10.1128/JB.183.8.2576-2585.2001. DOI: 10.1128/JB.183.8.2576-2585.2001
45. Johnston AW, Yeoman KH, Wexler M: Metals and the rhizobiallegume symbiosis - uptake utilization and signalling. Adv Microb Physiol. 2001, 45: 113-156. DOI: 10.1016/S0065-2911(01)45003-X
46. Bearden SW, Staggs TM, Perry RD: An ABC transporter system of Yersinia pestis allows utilization of chelated iron by Escherichia coli SAB11. J Bacteriol. 1998, 180: 1135-1147.
47. Zhou D, Hardt WD, Galan JE: Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect Immun. 1999, 67: 1974-1981.
48. Ehrhardt DW, Wais R, Long SR: Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell. 1996, 85: 673-681. DOI: 10.1016/S0092-8674(00)81234-9
49. McCue LA, McDonough KA, Lawrence CE: Functional classification of cNMP-binding proteins and nucleotide cyclases with implications for novel regulatory pathways in Mycobacterium tuberculosis. Genome Res. 2000, 10: 204-219. 10.1101/gr.10.2.204. DOI: 10.1101/gr.10.2.204
50. Archdeacon J, Talty J, Boesten B, Danchin A, O'Gara F: Cloning of the second adenylate cyclase gene (cya2) from Rhizobium meliloti F34: sequence similarity to eukaryotic cyclases. FEMS Microbiol Lett. 1995, 128: 177-184. 10.1016/0378-1097(95)00109-I. DOI: 10.1111/j.1574-6968.1995.tb07519.x
51. Sharypova LA, Yurgel SN, Keller M, Simarov BV, Puhler A, Becker A: The eff-482 locus of Sinorhizobium meliloti CXM1-105 that influences symbiotic effectiveness consists of three genes encoding an endoglycanase, a transcriptional regulator and an adenylate cyclase. Mol Gen Genet. 1999, 261: 1032-1044. 10.1007/s004380051052. DOI: 10.1007/s004380051052
52. Mock M, Ullmann A: Calmodulin-activated bacterial adenylate cyclases as virulence factors. Trends Microbiol. 1993, 1: 187-192. 10.1016/0966-842X(93)90089-A. DOI: 10.1016/0966-842X(93)90089-A
53. Ladant D, Ullmann A: Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol. 1999, 7: 172-176. 10.1016/S0966-842X(99)01468-7. DOI: 10.1016/S0966-842X(99)01468-7
54. Sinorhizobium meliloti Genome Project. [http://sequence.toulouse.inra.fr/meliloti.html]
55. Vincent JM: A Manual for the Practical Study of Root Nodule Bacteria. 1970
56. Maillet F, Debellé F, Dénarié J: Role of the nodD and syrM genes in the activation of the regulatory gene nodD3 and of the common and host-specific nod genes of Rhizobium meliloti. Mol Microbiol. 1990, 4: 1975-1984. DOI: 10.1111/j.1365-2958.1990.tb02047.x
57. Gallusci P, Dedieu A, Journet EP, Huguet T, Barker DG: Synchronous expression of leghaemoglobin genes in Medicago truncatula during nitrogen-fixing root nodule development and response to exogenously supplied nitrate. Plant Mol Biol. 1991, 17: 335-349. DOI: 10.1007/BF00040629
58. Arfin SM, Long AD, Ito ET, Tolleri L, Riehle MM, Paegle ES, Hatfield GW: Global gene expression profiling in Escherichia coli K12. The effects of integration host factor. J Biol Chem. 2000, 275: 29672-29684. 10.1074/jbc.M002247200. DOI: 10.1074/jbc.M002247200
59. Jackson AD, Larkins BA: Influence of ionic strength pH and chelation of divalent metals on isolation of polyribosomes from tobacco leaves. Plant Physiol. 1976, 57: 5-10. DOI: 10.1104/pp.57.1.5
60. Tao H, Bausch C, Richmond C, Blattner FR, Conway T: Functional genomics: expression analysis of Escherichia coli growing on minimal and rich media. J Bacteriol. 1999, 181: 6425-6440.
61. Génopôle Toulouse. [http://genopole.toulouse.inra.fr]
62. Alizadeh AA, Eisen MB, Davis RE, Lossos IS, Rosenwald A, Boldrick JC, Sabet H, Tran T, Yu X, et al: Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000, 403: 503-511. 10.1038/35000501. DOI: 10.1038/35000501