Small RNA-mediated control of the Agrobacterium tumefaciens GABA binding protein

Molecular Microbiology

Volumn 80, Issue 2, 2011, Pages 492-506

  Wilms, Ina ^a   Voss, Björn ^c   Hess, Wolfgang R ^c   Leichert, Lars I ^b   Narberhaus, Franz ^a  

^a Lehrstuhl für Biologie der Mikroorganismen   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ABC REGULATOR 1; ABC TRANSPORTER; PERIPLASMIC BINDING PROTEIN; PROTEIN ATU2422; REGULATOR PROTEIN; RNA; SMALL RNA; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID UPTAKE; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL METABOLISM; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC REGULATION; HOST PATHOGEN INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RHIZOBIUM RADIOBACTER; RNA METABOLISM; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; DOWN-REGULATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RHIZOBIUM RADIOBACTER; RNA, SMALL INTERFERING; SEQUENCE ALIGNMENT;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); BRUCELLA; RHIZOBIACEAE;

EID: 79954421372     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07589.x     Document Type: Article

References (86)

1. Aiba, H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10: 134-139.
2. Aiba, H., Adhya, S., and de Crombrugghe, B. (1981) Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem 256: 11905-11910.
3. Altuvia, S., Weinstein-Fischer, D., Zhang, A., Postow, L., and Storz, G. (1997) A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90: 43-53.
4. Altuvia, S., Zhang, A., Argaman, L., Tiwari, A., and Storz, G. (1998) The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J 17: 6069-6075.
5. Anand, A., Uppalapati, S.R., Ryu, C.M., Allen, S.N., Kang, L., Tang, Y., and Mysore, K.S. (2008) Salicylic acid and systemic acquired resistance play a role in attenuating crown gall disease caused by Agrobacterium tumefaciens. Plant Physiol 146: 703-715.
6. Antal, M., Bordeau, V., Douchin, V., and Felden, B. (2005) A small bacterial RNA regulates a putative ABC transporter. J Biol Chem 280: 7901-7908.
7. Argaman, L., and Altuvia, S. (2000) fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisense-target RNA complex. J Mol Biol 300: 1101-1112.
8. Axmann, I.M., Kensche, P., Vogel, J., Kohl, S., Herzel, H., and Hess, W.R. (2005) Identification of cyanobacterial non-coding RNAs by comparative genome analysis. Genome Biol 6: R73.1-R73.16.
9. Babst, M., Hennecke, H., and Fischer, H.M. (1996) Two different mechanisms are involved in the heat-shock regulation of chaperonin gene expression in Bradyrhizobium japonicum. Mol Microbiol 19: 827-839.
10. Backofen, R., and Hess, W.R. (2010) Computational prediction of sRNAs and their targets in bacteria. RNA Biol 7: 33-42.
11. Balbontín, R., Fiorini, F., Figueroa-Bossi, N., Casadesús, J., and Bossi, L. (2010) Recognition of heptameric seed sequence underlies multi-target regulation by RybB small RNA in Salmonella enterica. Mol Microbiol 78: 380-394.
12. Bandow, J.E. (2010) Comparison of protein enrichment strategies for proteome analysis of plasma. Proteomics 10: 1416-1425.
13. Berghoff, B.A., Glaeser, J., Sharma, C.M., Vogel, J., and Klug, G. (2009) Photooxidative stress-induced and abundant small RNAs in Rhodobacter sphaeroides. Mol Microbiol 74: 1497-1512.
14. Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., etal. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21: 1353-1366.
15. Bouche, F., and Bouche, J.P. (1989) Genetic evidence that DicF, a second division inhibitor encoded by the Escherichia coli dicB operon, is probably RNA. Mol Microbiol 3: 991-994.
16. Bouvier, M., Sharma, C.M., Mika, F., Nierhaus, K.H., and Vogel, J. (2008) Small RNA binding to 5' mRNA coding region inhibits translational initiation. Mol Cell 32: 827-837.
17. Brantl, S., and Wagner, E.G. (1994) Antisense RNA-mediated transcriptional attenuation occurs faster than stable antisense/target RNA pairing: an in vitro study of plasmid pIP501. EMBO J 13: 3599-3607.
18. Brennan, R.G., and Link, T.M. (2007) Hfq structure, function and ligand binding. Curr Opin Microbiol 10: 125-133.
19. Cao, Y., Zhao, Y., Cha, L., Ying, X., Wang, L., Shao, N., and Li, W. (2009) sRNATarget: a web server for prediction of bacterial sRNA targets. Bioinformation 3: 364-366.
20. Carlier, A., Chevrot, R., Dessaux, Y., and Faure, D. (2004) The assimilation of gamma-butyrolactone in Agrobacterium tumefaciens C58 interferes with the accumulation of the N-acyl-homoserine lactone signal. Mol Plant Microbe Interact 17: 951-957.
21. Chai, Y., and Winans, S.C. (2005) A small antisense RNA downregulates expression of an essential replicase protein of an Agrobacterium tumefaciens Ti plasmid. Mol Microbiol 56: 1574-1585.
22. Chen, S., Zhang, A., Blyn, L.B., and Storz, G. (2004) MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol 186: 6689-6697.
23. Chevrot, R., Rosen, R., Haudecoeur, E., Cirou, A., Shelp, B.J., Ron, E., and Faure, D. (2006) GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 103: 7460-7464.
24. Davidson, A.L., and Chen, J. (2004) ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73: 241-268.
25. Gao, M., Barnett, M.J., Long, S.R., and Teplitski, M. (2010) Role of the Sinorhizobium meliloti global regulator Hfq in gene regulation and symbiosis. Mol Plant Microbe Interact 23: 355-365.
26. Grzendowski, M., Wolter, M., Riemenschneider, M.J., Knobbe, C.B., Schlegel, U., Meyer, H.E., etal. (2010) Differential proteome analysis of human gliomas stratified for loss of heterozygosity on chromosomal arms 1p and 19q. Neuro Oncol 12: 243-256.
27. Guillier, M., and Gottesman, S. (2008) The 5' end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 36: 6781-6794.
28. Hartz, D., McPheeters, D.S., Traut, R., and Gold, L. (1988) Extension inhibition analysis of translation initiation complexes. Methods Enzymol 164: 419-425.
29. Haudecoeur, E., and Faure, D. (2010) A fine control of quorum-sensing communication in Agrobacterium tumefaciens. Commun Integr Biol 3: 84-88.
30. Haudecoeur, E., Planamente, S., Cirou, A., Tannieres, M., Shelp, B.J., Morera, S., and Faure, D. (2009a) Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens. Proc Natl Acad Sci USA 106: 14587-14592.
31. Haudecoeur, E., Tannieres, M., Cirou, A., Raffoux, A., Dessaux, Y., and Faure, D. (2009b) Different regulation and roles of lactonases AiiB and AttM in Agrobacterium tumefaciens C58. Mol Plant Microbe Interact 22: 529-537.
32. Hosie, A.H., and Poole, P.S. (2001) Bacterial ABC transporters of amino acids. Res Microbiol 152: 259-270.
33. Hosie, A.H., Allaway, D., Galloway, C.S., Dunsby, H.A., and Poole, P.S. (2002) Rhizobium leguminosarum has a second general amino acid permease with unusually broad substrate specificity and high similarity to branched-chain amino acid transporters (Bra/LIV) of the ABC family. J Bacteriol 184: 4071-4080.
34. Huntzinger, E., Boisset, S., Saveanu, C., Benito, Y., Geissmann, T., Namane, A., etal. (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24: 824-835.
35. Jäger, D., Sharma, C.M., Thomsen, J., Ehlers, C., Vogel, J., and Schmitz, R.A. (2009) Deep sequencing analysis of the Methanosarcina mazei Go1 transcriptome in response to nitrogen availability. Proc Natl Acad Sci USA 106: 21878-21882.
36. Johansen, J., Eriksen, M., Kallipolitis, B., and Valentin-Hansen, P. (2008) Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and sigmaE-dependent CyaR-ompX regulatory case. J Mol Biol 383: 1-9.
37. Kawamoto, H., Koide, Y., Morita, T., and Aiba, H. (2006) Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol 61: 1013-1022.
38. Kazantsev, A.V., and Pace, N.R. (2006) Bacterial RNase P: a new view of an ancient enzyme. Nat Rev Microbiol 4: 729-740.
39. Khan, S.R., and Farrand, S.K. (2009) The BlcC (AttM) lactonase of Agrobacterium tumefaciens does not quench the quorum-sensing system that regulates Ti plasmid conjugative transfer. J Bacteriol 191: 1320-1329.
40. Lease, R.A., Cusick, M.E., and Belfort, M. (1998) Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci USA 95: 12456-12461.
41. Lenz, D.H., Mok, K.C., Lilley, B.N., Kulkarni, R.V., Wingreen, N.S., and Bassler, B.L. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
42. Liu, P., and Nester, E.W. (2006) Indoleacetic acid, a product of transferred DNA, inhibits vir gene expression and growth of Agrobacterium tumefaciens C58. Proc Natl Acad Sci USA 103: 4658-4662.
43. Majdalani, N., Cunning, C., Sledjeski, D., Elliott, T., and Gottesman, S. (1998) DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci USA 95: 12462-12467.
44. Majdalani, N., Hernandez, D., and Gottesman, S. (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46: 813-826.
45. Majdalani, N., Vanderpool, C.K., and Gottesman, S. (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40: 93-113.
46. Mandin, P., Repoila, F., Vergassola, M., Geissmann, T., and Cossart, P. (2007) Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res 35: 962-974.
47. Morera, S., Gueguen-Chaignon, V., Raffoux, A., and Faure, D. (2008) Cloning, purification, crystallization and preliminary X-ray analysis of a bacterial GABA receptor with a Venus flytrap fold. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 1153-1155.
48. Muto, A., Ushida, C., and Himeno, H. (1998) A bacterial RNA that functions as both a tRNA and an mRNA. Trends Biochem Sci 23: 25-29.
49. Narberhaus, F., and Vogel, J. (2009) Regulatory RNAs in prokaryotes: here, there and everywhere. Mol Microbiol 74: 261-269.
50. Padalon-Brauch, G., Hershberg, R., Elgrably-Weiss, M., Baruch, K., Rosenshine, I., Margalit, H., and Altuvia, S. (2008) Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36: 1913-1927.
51. Paulick, A., Koerdt, A., Lassak, J., Huntley, S., Wilms, I., Narberhaus, F., and Thormann, K.M. (2009) Two different stator systems drive a single polar flagellum in Shewanella oneidensis MR-1. Mol Microbiol 71: 836-850.
52. Planamente, S., Vigouroux, A., Mondy, S., Nicaise, M., Faure, D., and Morera, S. (2010) A Conserved Mechanism of GABA Binding and Antagonism Is Revealed by Structure-Function Analysis of the Periplasmic Binding Protein Atu2422 in Agrobacterium tumefaciens. J Biol Chem 285: 30294-30303.
53. Prell, J., Bourdes, A., Karunakaran, R., Lopez-Gomez, M., and Poole, P. (2009) Pathway of gamma-aminobutyrate metabolism in Rhizobium leguminosarum 3841 and its role in symbiosis. J Bacteriol 191: 2177-2186.
54. Rehmsmeier, M., Steffen, P., Hochsmann, M., and Giegerich, R. (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10: 1507-1517.
55. Reichenbach, B., Maes, A., Kalamorz, F., Hajnsdorf, E., and Görke, B. (2008) The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenylation in Escherichia coli. Nucleic Acids Res 36: 2570-2580.
56. Schägger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100kDa. Anal Biochem 166: 368-379.
57. Schlüter, J.P., Reinkensmeier, J., Daschkey, S., Evguenieva-Hackenberg, E., Janssen, S., Janicke, S., etal. (2010) A genome-wide survey of sRNAs in the symbiotic nitrogen-fixing alpha-proteobacterium Sinorhizobium meliloti. BMC Genomics 11: 245.1-245.35.
58. Sharma, C.M., and Vogel, J. (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12: 536-546.
59. Sharma, C.M., Darfeuille, F., Plantinga, T.H., and Vogel, J. (2007) A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev 21: 2804-2817.
60. Sharma, C.M., Hoffmann, S., Darfeuille, F., Reignier, J., Findeiss, S., Sittka, A., etal. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
61. Shelp, B.J., Bown, A.W., and Faure, D. (2006) Extracellular gamma-aminobutyrate mediates communication between plants and other organisms. Plant Physiol 142: 1350-1352.
62. Tjaden, B., Goodwin, S.S., Opdyke, J.A., Guillier, M., Fu, D.X., Gottesman, S., and Storz, G. (2006) Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 34: 2791-2802.
63. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., etal. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
64. Torres-Quesada, O., Oruezabal, R.I., Peregrina, A., Jofre, E., Lloret, J., Rivilla, R., etal. (2010) The Sinorhizobium meliloti RNA chaperone Hfq influences central carbon metabolism and the symbiotic interaction with alfalfa. BMC Microbiol 10: 71.
65. Tu, K.C., and Bassler, B.L. (2007) Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev 21: 221-233.
66. Udekwu, K.I., Darfeuille, F., Vogel, J., Reimegard, J., Holmqvist, E., and Wagner, E.G. (2005) Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 19: 2355-2366.
67. Ulve, V.M., Sevin, E.W., Cheron, A., and Barloy-Hubler, F. (2007) Identification of chromosomal alpha-proteobacterial small RNAs by comparative genome analysis and detection in Sinorhizobium meliloti strain 1021. BMC Genomics 8: 467.1-467.16.
68. Urban, J.H., and Vogel, J. (2008) Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6: e64.
69. Urbanowski, M.L., Stauffer, L.T., and Stauffer, G.V. (2000) The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol 37: 856-868.
70. del Val, C., Rivas, E., Torres-Quesada, O., Toro, N., and Jimenez-Zurdo, J.I. (2007) Identification of differentially expressed small non-coding RNAs in the legume endosymbiont Sinorhizobium meliloti by comparative genomics. Mol Microbiol 66: 1080-1091.
71. Valverde, C., Livny, J., Schlüter, J.P., Reinkensmeier, J., Becker, A., and Parisi, G. (2008) Prediction of Sinorhizobium meliloti sRNA genes and experimental detection in strain 2011. BMC Genomics 9: 416.1-416.24.
72. Vercruysse, M., Fauvart, M., Cloots, L., Engelen, K., Thijs, I.M., Marchal, K., and Michiels, J. (2010) Genome-wide detection of predicted non-coding RNAs in Rhizobium etli expressed during free-living and host-associated growth using a high-resolution tiling array. BMC Genomics 11: 53.
73. Vogel, J., and Wagner, E.G. (2007) Target identification of small noncoding RNAs in bacteria. Curr Opin Microbiol 10: 262-270.
74. Voss, B., Georg, J., Schon, V., Ude, S., and Hess, W.R. (2009a) Biocomputational prediction of non-coding RNAs in model cyanobacteria. BMC Genomics 10: 123.1-123.15.
75. Voss, B., Holscher, M., Baumgarth, B., Kalbfleisch, A., Kaya, C., Hess, W.R., etal. (2009b) Expression of small RNAs in Rhizobiales and protection of a small RNA and its degradation products by Hfq in Sinorhizobium meliloti. Biochem Biophys Res Commun 390: 331-336.
76. Waldminghaus, T., Fippinger, A., Alfsmann, J., and Narberhaus, F. (2005) RNA thermometers are common in alpha- and gamma-proteobacteria. Biol Chem 386: 1279-1286.
77. Wassarman, K.M., and Storz, G. (2000) 6S RNA regulates E. coli RNA polymerase activity. Cell 101: 613-623.
78. Waters, L.S., and Storz, G. (2009) Regulatory RNAs in bacteria. Cell 136: 615-628.
79. Weilbacher, T., Suzuki, K., Dubey, A.K., Wang, X., Gudapaty, S., Morozov, I., etal. (2003) A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48: 657-670.
80. White, C.E., and Winans, S.C. (2007) Cell-cell communication in the plant pathogen Agrobacterium tumefaciens. Philos Trans R Soc Lond B Biol Sci 362: 1135-1148.
81. Wood, D.W., Setubal, J.C., Kaul, R., Monks, D.E., Kitajima, J.P., Okura, V.K., etal. (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294: 2317-2323.
82. Yuan, Z.C., Edlind, M.P., Liu, P., Saenkham, P., Banta, L.M., Wise, A.A., etal. (2007) The plant signal salicylic acid shuts down expression of the vir regulon and activates quormone-quenching genes in Agrobacterium. Proc Natl Acad Sci USA 104: 11790-11795.
83. Yuan, Z.C., Haudecoeur, E., Faure, D., Kerr, K.F., and Nester, E.W. (2008) Comparative transcriptome analysis of Agrobacterium tumefaciens in response to plant signal salicylic acid, indole-3-acetic acid and gamma-amino butyric acid reveals signalling cross-talk and Agrobacterium-plant co-evolution. Cell Microbiol 10: 2339-2354.
84. Zhang, A., Wassarman, K.M., Ortega, J., Steven, A.C., and Storz, G. (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol Cell 9: 11-22.
85. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
86. Zupan, J., Muth, T.R., Draper, O., and Zambryski, P. (2000) The transfer of DNA from Agrobacterium tumefaciens into plants: a feast of fundamental insights. Plant J 23: 11-28.