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Volume 150, Issue 7

FixJ-regulated genes evolved through promoter duplication in Free

Abstract

The FixLJ two-component system of is a global regulator, turning on nitrogen-fixation genes in microaerobiosis. Up to now, and were the only genes known to be directly regulated by FixJ. We used a genomic SELEX approach in order to isolate new FixJ targets in the genome. This led to the identification of 22 FixJ binding sites, including the known sites in the and promoters. FixJ binding sites are unevenly distributed among the three replicons constituting the genome: a majority are carried either by pSymA or by a short chromosomal region of non-chromosomal origin. Thus FixJ binding sites appear to be preferentially associated with the pSymA replicon, which carries the gene. Functional analysis of FixJ targets led to the discovery of two new FixJ-regulated genes, and . This FixJ-dependent regulation appears to be mediated by a duplication of the whole promoter region, including the beginning of the gene. Similar duplications were previously reported for the promoter. By systematic comparison of all promoter regions we found 17 such duplications throughout the genome, indicating that promoter duplication is a common mechanism for the evolution of regulatory pathways in .

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2004-07-01
2024-04-24
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References

  1. Adams E., Frank L. 1980; Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49:1005–1061 [CrossRef]
     [Google Scholar]
  2. Bailey T. L., Elkan C. 1994; Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36
     [Google Scholar]
  3. Barnett M. J., Fisher R. F., Jones T. & 23 other authors; 2001; Nucleotide sequence and predicted functions of the entire Sinorhizobium meliloti pSymA megaplasmid. Proc Natl Acad Sci U S A 98:9883–9888 [CrossRef]
     [Google Scholar]
  4. Batut J., Daveran-Mingot M. L., David M., Jacobs J., Garnerone A. M., Kahn D. 1989; fixK, a gene homologous with fnr and crp from Escherichia coli, regulates nitrogen fixation genes both positively and negatively in Rhizobium meliloti. EMBO J 8:1279–1286
     [Google Scholar]
  5. Berg O. G., von Hippel P. H. 1988; Selection of DNA binding sites by regulatory proteins. Trends Biochem Sci 13:207–211 [CrossRef]
     [Google Scholar]
  6. Bergès H., Checroun C., Guiral S., Garnerone A. M., Boistard P., Batut J. 2001; A glutamine-amidotransferase-like protein modulates FixT anti-kinase activity in Sinorhizobium meliloti. BMC Microbiol 1:6 [CrossRef]
     [Google Scholar]
  7. Better M., Lewis B., Corbin D., Ditta G., Helinski D. R. 1983; Structural relationships among Rhizobium meliloti symbiotic promoters. Cell 35:479–485 [CrossRef]
     [Google Scholar]
  8. Better M., Ditta G., Helinski D. R. 1985; Deletion analysis of Rhizobium meliloti symbiotic promoters. EMBO J 4:2419–2424
     [Google Scholar]
  9. Boyer H. W., Roulland-Dussoix D. 1969; A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41:459–472 [CrossRef]
     [Google Scholar]
  10. Cabanes D., Boistard P., Batut J. 2000; Symbiotic induction of pyruvate dehydrogenase genes from Sinorhizobium meliloti. Mol Plant-Microbe Interact 13:483–493 [CrossRef]
     [Google Scholar]
  11. Capela D., Barloy-Hubler F., Gouzy J. & 25 other authors; 2001; Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci U S A 98:9877–9882 [CrossRef]
     [Google Scholar]
  12. David M., Daveran M. L., Batut J., Dedieu A., Domergue O., Ghai J., Hertig C., Boistard P., Kahn D. 1988; Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54:671–683 [CrossRef]
     [Google Scholar]
  13. D'Hooghe I., Michiels J., Vlassak K., Verreth C., Waelkens F., Vanderleyden J. 1995; Structural and functional analysis of the fixLJ genes of Rhizobium leguminosarum. biovar phaseoli CNPF512. Mol Gen Genet 249:117–126 [CrossRef]
     [Google Scholar]
  14. D'Hooghe I., Michiels J., Vanderleyden J. 1998; The Rhizobium etli FixL protein differs in structure from other known FixL proteins. Mol Gen Genet 257:576–580 [CrossRef]
     [Google Scholar]
  15. Ditta G., Virts E., Palomares A., Kim C. H. 1987; The nifA gene of Rhizobium meliloti is oxygen regulated. . J Bacteriol 169:3217–3223
     [Google Scholar]
  16. Earl C. D., Ronson C. W., Ausubel F. M. 1987; Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC. and fixX genes. J Bacteriol 169:1127–1136
     [Google Scholar]
  17. Ferrières L., Kahn D. 2002; Two distinct classes of FixJ binding sites defined by in vitro selection. FEBS Lett 517:185–189 [CrossRef]
     [Google Scholar]
  18. Figurski D. H., 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 U S A 76:1648–1652 [CrossRef]
     [Google Scholar]
  19. Finan T. M., Weidner S., Wong K. & 9 other authors; 2001; The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti. Proc Natl Acad Sci U S A 98:9889–9894 [CrossRef]
     [Google Scholar]
  20. Fischer H. M. 1994; Genetic regulation of nitrogen fixation in rhizobia. Microbiol Rev 58:352–386
     [Google Scholar]
  21. Foussard M., Garnerone A. M., Ni F., Boistard P., Batut J., Soupène E. 1997; Negative autoregulation of the Rhizobium meliloti fixK gene is indirect and requires a newly identified regulator, FixT. Mol Microbiol 25:27–37 [CrossRef]
     [Google Scholar]
  22. Galibert F., Finan T. M., Long S. R.53 other authors 2001; The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672 [CrossRef]
     [Google Scholar]
  23. Galinier A., Garnerone A. M., Reyrat J. M., Kahn D., Batut J., Boistard P. 1994; Phosphorylation of the Rhizobium meliloti FixJ protein induces its binding to a compound regulatory region at thefixK promoter. . J Biol Chem 269:23784–23789
     [Google Scholar]
  24. Gowers D. M., Halford S. E. 2003; Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling. EMBO J 22:1410–1418 [CrossRef]
     [Google Scholar]
  25. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
     [Google Scholar]
  26. Hirsch A. M., Bang M., Ausubel F. M. 1983; Ultrastructural analysis of ineffective alfalfa nodules formed by nif : : Tn5 mutants of Rhizobium meliloti. J Bacteriol 155:367–380
     [Google Scholar]
  27. Irreverre F., Morita K., Ishii S., Witkop B. 1962; Occurrence of cis- and trans-3-hydroxy-l-proline in acid hydrolyzate of telomycin. Biochem Biophys Res Commun 9:69–71 [CrossRef]
     [Google Scholar]
  28. Jefferson R. A. 1987; Assaying chimeric genes in plants : the GUS gene fusion system. Plant Mol Biol Report 5:387–405 [CrossRef]
     [Google Scholar]
  29. Jefferson R. A., Burgess S. M., Hirsh D. 1986; Beta-glucuronidase from Escherichia coli as a gene-fusion marker. Proc Natl Acad Sci U S A 83:8447–8451 [CrossRef]
     [Google Scholar]
  30. Jimenez-Zurdo J. I., Garcia-Rodriguez F. M., Toro N. 1997; The Rhizobium meliloti putA gene: its role in the establishment of the symbiotic interaction with alfalfa. Mol Microbiol 23:85–93 [CrossRef]
     [Google Scholar]
  31. Kahn D., Ditta G. 1991; Modular structure of FixJ: homology of the transcriptional activator domain with the −35 binding domain of sigma factors. Mol Microbiol 5:987–997 [CrossRef]
     [Google Scholar]
  32. Kaneko T., Nakamura Y., Sato S.21 other authors 2000; Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331–338 [CrossRef]
     [Google Scholar]
  33. Kaneko T., Nakamura Y., Sato S.14 other authors 2002; Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197 [CrossRef]
     [Google Scholar]
  34. King N. D., Hojnacki D., O'Brian M. R. 2000; The Bradyrhizobium japonicum proline biosynthesis gene proC is essential for symbiosis. Appl Environ Microbiol 66:5469–5471 [CrossRef]
     [Google Scholar]
  35. Martin M. O., Long S. R. 1984; Generalized transduction in Rhizobium meliloti. J Bacteriol 159:125–129
     [Google Scholar]
  36. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. 1982; Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 149:114–122
     [Google Scholar]
  37. Mori H., Shibasaki T., Uozaki Y., Ochiai K., Ozaki A. 1996; Detection of novel proline 3-hydroxylase activities in Streptomyces and Bacillus spp. by regio- and stereospecific hydroxylation of l-proline. Appl Environ Microbiol 62:1903–1907
     [Google Scholar]
  38. Mori H., Shibasaki T., Yano K., Ozaki A. 1997; Purification and cloning of a proline 3-hydroxylase, a novel enzyme which hydroxylates free l-proline to cis-3-hydroxy-l-proline. J Bacteriol 179:5677–5683
     [Google Scholar]
  39. Murphy P. J., Heycke N., Trenz S. P., Ratet P., de Bruijn F. J., Schell J. 1988; Synthesis of an opine-like compound, a rhizopine, in alfalfa nodules is symbiotically regulated. Proc Natl Acad Sci U S A 85:9133–9137 [CrossRef]
     [Google Scholar]
  40. Murphy P. J., Trenz S. P., Grzemski W., de Bruijn F. J., Schell J. 1993; The Rhizobium meliloti rhizopine mos locus is a mosaic structure facilitating its symbiotic regulation. J Bacteriol 175:5193–5204
     [Google Scholar]
  41. Nellen-Anthamatten D., Rossi P., Preisig O., Kullik I., Babst M., Fischer H. M., Hennecke H. 1998; Bradyrhizobium japonicum FixK2, a crucial distributor in the FixLJ-dependent regulatory cascade for control of genes inducible by low oxygen levels. J Bacteriol 180:5251–5255
     [Google Scholar]
  42. Osteras M., Stanley J., Finan T. M. 1995; Identification of Rhizobium-specific intergenic mosaic elements within an essential two-component regulatory system ofRhizobium species. . J Bacteriol 177:5485–5494
     [Google Scholar]
  43. Osteras M., Boncompagni E., Vincent N., Poggi M. C., Le Rudulier D. 1998; Presence of a gene encoding choline sulfatase in Sinorhizobium meliloti bet operon: choline-O-sulfate is metabolized into glycine betaine. Proc Natl Acad Sci U S A 95:11394–11399 [CrossRef]
     [Google Scholar]
  44. Prentki P., Krisch H. M. 1984; In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313 [CrossRef]
     [Google Scholar]
  45. Quandt J., Hynes M. F. 1993; Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127:15–21 [CrossRef]
     [Google Scholar]
  46. Rao J. P., Grzemski W., Murphy P. J. 1995; Rhizobium meliloti lacking mosA synthesizes the rhizopine scyllo-inosamine in place of 3-O-methyl-scyllo-inosamine. Microbiology 141:1683–1690 [CrossRef]
     [Google Scholar]
  47. Renalier M. H., Batut J., Ghai J. & 8 other authors; 1987; A new symbiotic cluster on the pSym megaplasmid of Rhizobium meliloti 2011 carries a functional fix gene repeat and a nod locus. J Bacteriol 169:2231–2238
     [Google Scholar]
  48. Sheehan J. C., Zachau H. G., Lawson W. B. 1958; The structure of etamycin. J Am Chem Soc 80:3349–3355 [CrossRef]
     [Google Scholar]
  49. Shoji J., Hinoo H., Katayama T., Nakagawa Y., Ikenishi Y., Iwatani K., Yoshida T. 1992; Structures of new peptide antibiotics, plusbacins A1-A4 and B1-B4. J Antibiot 45:824–831 [CrossRef]
     [Google Scholar]
  50. Singer B. S., Shtatland T., Brown D., Gold L. 1997; Libraries for genomic SELEX. Nucleic Acids Res 25:781–786 [CrossRef]
     [Google Scholar]
  51. Sullivan J. T., Trzebiatowski J. R., Cruickshank R. W.11 other authors 2002; Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. . J Bacteriol 184:3086–3095 [CrossRef]
     [Google Scholar]
  52. Trzebiatowski J. R., Ragatz D. M., de Bruijn F. J. 2001; Isolation and regulation of Sinorhizobium meliloti 1021 loci induced by oxygen limitation. Appl Environ Microbiol 67:3728–3731 [CrossRef]
     [Google Scholar]
  53. Turner G. L., Gibson A. H. 1980; Measurement of nitrogen fixation by indirect means. In Methods for Evaluating Biological Nitrogen Fixation pp. 111–138Edited by Bergersen F. J. Chichester: Wiley;
     [Google Scholar]
  54. Van den Eede G., Deblaere R., Goethals K., van Montagu M., Holsters M. 1992; Broad host range and promoter selection vectors for bacteria that interact with plants. Mol Plant-Microbe Interact 5:228–234 [CrossRef]
     [Google Scholar]
  55. von Hippel P. H., Berg O. G. 1989; Facilitated target location in biological systems. J Biol Chem 264:675–678
     [Google Scholar]
  56. Waelkens F., Foglia A., Morel J. B., Fourment J., Batut J., Boistard P. 1992; Molecular genetic analysis of the Rhizobium meliloti fixK promoter: identification of sequences involved in positive and negative regulation. Mol Microbiol 6:1447–1456 [CrossRef]
     [Google Scholar]
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FixJ-regulated genes evolved through promoter duplication in Sinorhizobium meliloti
Microbiology 150, 2335 (2004); https://doi.org/10.1099/mic.0.27081-0
/content/journal/micro/10.1099/mic.0.27081-0
/content/journal/micro/10.1099/mic.0.27081-0
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