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Annual Review of Microbiology

Volume 70, 2016

Riboswitch-Mediated Gene Regulation: Novel RNA Architectures Dictate Gene Expression Responses

Abstract

Riboswitches are RNA elements that act on the mRNA with which they are cotranscribed to modulate expression of that mRNA. These elements are widely found in bacteria, where they have a broad impact on gene expression. The defining feature of riboswitches is that they directly recognize a physiological signal, and the resulting shift in RNA structure affects gene regulation. The majority of riboswitches respond to cellular metabolites, often in a feedback loop to repress synthesis of the enzymes used to produce the metabolite. Related elements respond to the aminoacylation status of a specific tRNA or to a physical parameter, such as temperature or pH. Recent studies have identified new classes of riboswitches and have revealed new insights into the molecular mechanisms of signal recognition and gene regulation. Application of structural and biophysical approaches has complemented previous genetic and biochemical studies, yielding new information about how different riboswitches operate.

Keyword(s): RNA structure, RNA-mediated regulation, transcription attenuation, translational regulation
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2016-09-08
2024-04-25
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Literature Cited

  1. Ames TD, Rodionov DA, Weinberg Z, Breaker RR. 1.  2010. A eubacterial riboswitch class that senses the coenzyme tetrahydrofolate. Chem. Biol. 17:681–85 [Google Scholar]
  2. Ames TD, Breaker RR. 2.  2011. Bacterial aptamers that selectively bind glutamine. RNA Biol. 8:82–89 [Google Scholar]
  3. Baker JL, Sudarsan N, Weinberg Z, Roth A, Stockbridge RB, Breaker RR. 3.  2012. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 335:233–35 [Google Scholar]
  4. Böhme K, Steinmann R, Kortmann J, Seekircher S, Heroven AK. 4.  et al. 2012. Concerted actions of a thermo-labile regulator and a unique intergenic RNA thermosensor control Yersinia virulence. PLOS Pathog. 8:e1002518 [Google Scholar]
  5. Breaker RR. 5.  2011. Prospects for riboswitch discovery and analysis. Mol. Cell 43:867–79 [Google Scholar]
  6. Cheah MT, Wachter A, Sudarsan N, Breaker RR. 6.  2007. Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 44:497–500 [Google Scholar]
  7. Chinnappan R, Dube A, Lemay JF, Lafontaine DA. 7.  2013. Fluorescence monitoring of riboswitch transcription regulation using a dual molecular beacon assay. Nucleic Acids Res. 41:e106 [Google Scholar]
  8. Collins JA, Irnov I, Baker S, Winkler WC. 8.  2007. Mechanism of mRNA destabilization by the glmS ribozyme. Genes Dev. 21:3356–68 [Google Scholar]
  9. Corbino KA, Barrick JE, Lim J, Welz R, Tucker BJ. 9.  et al. 2005. Evidence for a second class of S-adenosylmethionine riboswitches and other regulatory RNA motifs in alpha-proteobacteria. Genome Biol. 6:R70 [Google Scholar]
  10. Cromie MJ, Shi Y, Latifi T, Groisman EA. 10.  2006. An RNA sensor for intracellular Mg2+. Cell 125:71–84 [Google Scholar]
  11. Dann CE. Wakeman CA, Sieling CL, Baker SC, Irnov I, Winkler WC. 11.  III, 2007. Structure and mechanism of a metal-sensing regulatory RNA. Cell 130:878–92 [Google Scholar]
  12. Dixon N, Robinson CJ, Geerlings T, Duncan JN, Drummond SP, Micklefield J. 12.  2012. Orthogonal riboswitches for tuneable coexpression in bacteria. Angew. Chem. Int. Ed. 51:3620–24 [Google Scholar]
  13. Fuchs RT, Grundy FJ, Henkin TM. 13.  2006. The SMK box is a new SAM-binding RNA for translational regulation of SAM synthetase. Nat. Struct. Mol. Biol. 13:226–33 [Google Scholar]
  14. Fuchs RT, Grundy FJ, Henkin TM. 14.  2007. S-adenosylmethionine directly inhibits binding of 30S ribosomal subunits to the SMK box translational riboswitch RNA. PNAS 104:4876–80 [Google Scholar]
  15. Furukawa K, Ramesh A, Zhou Z, Weinberg Z, Vallery T. 15.  et al. 2015. Bacterial riboswitches cooperatively bind Ni2+ or Co2+ ions and control expression of heavy metal transporters. Mol. Cell 57:1088–98 [Google Scholar]
  16. Gilbert SD, Rambo RP, Van Tyne D, Batey RT. 16.  2008. Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat. Struct. Mol. Biol. 15:177–82 [Google Scholar]
  17. Gottesman S, Storz G. 17.  2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb. Perspect. Biol. 3:12a003798 [Google Scholar]
  18. Grigg JC, Chen Y, Grundy FJ, Henkin TM, Pollack L, Ke A. 18.  2013. T box RNA decodes both the information content and geometry of tRNA to affect gene expression. PNAS 110:7240–45 [Google Scholar]
  19. Groher F, Suess B. 19.  2014. Synthetic riboswitches—A tool comes of age. Biochim. Biophys. Acta 1839:964–73 [Google Scholar]
  20. Grundy FJ, Henkin TM. 20.  1993. tRNA as a positive regulator of transcription antitermination in B. subtilis. Cell 74:475–82 [Google Scholar]
  21. Grundy FJ, Henkin TM. 21.  1998. The S box regulon: a new global transcription termination control system for methionine and cysteine biosynthesis genes in gram-positive bacteria. Mol. Microbiol. 30:737–49 [Google Scholar]
  22. Grundy FJ, Hodil SE, Rollins SM, Henkin TM. 22.  1997. Specificity of tRNA-mRNA interactions in Bacillus subtilis tyrS antitermination. J. Bacteriol. 179:2587–94 [Google Scholar]
  23. Grundy FJ, Lehman SC, Henkin TM. 23.  2003. The L box regulon: lysine sensing by leader RNAs of bacterial lysine biosynthesis genes. PNAS 100:12057–62 [Google Scholar]
  24. Grundy FJ, Winkler WC, Henkin TM. 24.  2002. tRNA-mediated transcription antitermination in vitro: codon-anticodon pairing independent of the ribosome. PNAS 99:11121–26 [Google Scholar]
  25. Gutiérrez-Preciado A, Henkin TM, Grundy FJ, Yanofsky C, Merino E. 25.  2009. Biochemical features and functional implications of the RNA-based T-box regulatory mechanism. Microbiol. Mol. Biol. Rev. 73:36–61 [Google Scholar]
  26. Henkin TM. 26.  2014. The T box riboswitch: a novel regulatory RNA that utilizes tRNA as its ligand. Biochim. Biophys. Acta 1839:959–63 [Google Scholar]
  27. Hollands K, Sevostiyanova A, Groisman EA. 27.  2014. Unusually long-lived pause required for regulation of a Rho-dependent transcription terminator. PNAS 111:1999–2007 [Google Scholar]
  28. Huang L, Serganov A, Patel DJ. 28.  2010. Structural insights into ligand recognition by a sensing domain of the cooperative glycine riboswitch. Mol. Cell 40:774–86 [Google Scholar]
  29. Kim JN, Roth A, Breaker RR. 29.  2007. Guanine riboswitch variants from Mesoplasma florum selectively recognize 2′-deoxyguanosine. PNAS 104:16092–97 [Google Scholar]
  30. Krajewski SS, Narberhaus F. 30.  2014. Temperature-driven differential gene expression by RNA thermosensors. Biochim. Biophys. Acta 1839:978–88 [Google Scholar]
  31. Kubodera T, Watanabe M, Yoshiuchi K, Yamashita N, Nishimura A. 31.  et al. 2003. Thiamine-regulated gene expression of Aspergillus oryzae thiA requires splicing of the intron containing a riboswitch-like domain in the 5′-UTR. FEBS Lett. 555:516–20 [Google Scholar]
  32. Lemay J-F, Desnoyers G, Blouin S, Heppell B, Bastet L. 32.  et al. 2011. Comparative study between transcriptionally- and translationally-acting adenine riboswitches reveals key differences in riboswitch regulatory mechanisms. PLOS Genet. 7:e1001278 [Google Scholar]
  33. Liu L-C, Grundy FJ, Henkin TM. 33.  2015. Non-conserved residues in Clostridium acetobutylicum tRNAAla contribute to tRNA tuning for efficient antitermination of the alaS T box riboswitch. Life 5:1567–82 [Google Scholar]
  34. Loh E, Kugelberg E, Tracy A, Zhang Q, Gollan B. 34.  et al. 2013. Temperature triggers immune evasion by Neisseria meningitidis. Nature 502:237–40 [Google Scholar]
  35. Lu C, Smith AM, Fuchs RT, Ding F, Rajashankar K. 35.  et al. 2008. Crystal structures of the SAM-III/SMK riboswitch reveal the SAM-dependent translation inhibition mechanism. Nat. Struct. Mol. Biol. 15:1076–83 [Google Scholar]
  36. Lu C, Smith AM, Ding F, Chowdhury A, Henkin TM, Ke A. 36.  2011. Variable sequences outside the SAM-binding core critically influence the conformational dynamics of the SAM-III/SMK box riboswitch. J. Mol. Biol. 409:786–99 [Google Scholar]
  37. Mandal M, Breaker RR. 37.  2004. Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat. Struct. Mol. Biol. 11:29–35 [Google Scholar]
  38. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR. 38.  2003. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113:577–86 [Google Scholar]
  39. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM. 39.  et al. 2004. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 306:275–79 [Google Scholar]
  40. McDaniel BAM, Grundy FJ, Artsimovitch I, Henkin TM. 40.  2003. Transcription termination control of the S box system: direct measurement of S-adenosylmethionine by the leader RNA. PNAS 100:3083–88 [Google Scholar]
  41. Mironov AS, Gusarov I, Rafikov R, Lopez LE, Shatalin K. 41.  et al. 2002. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 111:747–56 [Google Scholar]
  42. Nahvi A, Sudarsan N, Ebert MS, Zou X, Brown KL, Breaker RR. 42.  2002. Genetic control by a metabolite binding mRNA. Chem. Biol. 9:1043–49 [Google Scholar]
  43. Nechooshtan G, Elgrably-Weiss M, Sheaffer A, Westhof E, Altuvia S. 43.  2009. A pH-responsive riboregulator. Genes Dev. 23:2650–62 [Google Scholar]
  44. Nelson JW, Sudarsan N, Furukawa K, Weinberg Z, Wang JX, Breaker RR. 44.  2013. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat. Chem. Biol. 9:834–39 [Google Scholar]
  45. Peselis A, Serganov A. 45.  2014. Themes and variations in riboswitch structure and function. Biochim. Biophys. Acta 1839:908–18 [Google Scholar]
  46. Price IR, Grigg JC, Ke A. 46.  2014. Common themes and differences in SAM recognition among SAM riboswitches. Biochim. Biophys. Acta 1839:931–38 [Google Scholar]
  47. Putzer H, Gendron N, Grunberg-Manago M. 47.  1992. Co-ordinate expression of the two threonyl-tRNA synthetase genes in Bacillus subtilis: control by transcriptional antitermination involving a conserved regulatory sequence. EMBO J. 11:3117–27 [Google Scholar]
  48. Regulski EE, Moy RH, Weinberg Z, Barrick JE, Yao Z. 48.  et al. 2008. A widespread riboswitch candidate that controls bacterial genes involved in molybdenum cofactor and tungsten cofactor metabolism. Mol. Microbiol. 68:918–32 [Google Scholar]
  49. Roth A, Winkler WC, Regulski EE, Lee BWK, Lim J. 49.  et al. 2007. A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain. Nat. Struct. Mol. Biol. 14:308–17 [Google Scholar]
  50. Savinov A, Perez CF, Block SM. 50.  2014. Single-molecule studies of riboswitch folding. Biochim. Biophys. Acta 1839:1030–45 [Google Scholar]
  51. Serganov A, Yuan YR, Pikovskaya O, Polonskaia A, Malinina L. 51.  et al. 2004. Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem. Biol. 11:1729–41 [Google Scholar]
  52. Serganov A, Polonskaia A, Phan AT, Breaker RR, Patel DJ. 52.  2006. Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 441:1167–71 [Google Scholar]
  53. Serganov A, Nudler E. 53.  2013. A decade of riboswitches. Cell 152:17–24 [Google Scholar]
  54. Sherwood AV, Grundy FJ, Henkin TM. 54.  2015. T box riboswitches in Actinobacteria: translational regulation via novel tRNA interactions. PNAS 112:1113–18 [Google Scholar]
  55. Shi Y, Zhao G, Kong W. 55.  2014. Genetic analysis of riboswitch-mediated transcriptional regulation responding to Mn2+ in Salmonella. J. Biol. Chem. 289:11353–66 [Google Scholar]
  56. Shivers RP, Sonenshein AL. 56.  2005. Bacillus subtilis ilvB operon: an intersection of global regulons. Mol. Microbiol. 56:1549–59 [Google Scholar]
  57. Smith AM, Fuchs RT, Grundy FJ, Henkin TM. 57.  2010. Riboswitch RNAs: regulation of gene expression by direct monitoring of a physiological signal. RNA Biol. 7:104–10 [Google Scholar]
  58. Smith AM, Fuchs RT, Grundy FJ, Henkin TM. 58.  2010. The SAM-responsive SMK box is a reversible riboswitch. Mol. Microbiol. 78:1393–402 [Google Scholar]
  59. Storz G, Vogel J, Wassarman KM. 59.  2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell 43:880–91 [Google Scholar]
  60. Sudarsan N, Hammond MC, Block KF, Welz R, Barrick JE. 60.  et al. 2006. Tandem riboswitch architectures exhibit complex gene control functions. Science 314:300–4 [Google Scholar]
  61. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN. 61.  et al. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411–13 [Google Scholar]
  62. Sun EI, Rodionov DA. 62.  2014. Computational analysis of riboswitch-based regulation. Biochim. Biophys. Acta 1839:900–7 [Google Scholar]
  63. Tomsic J, McDaniel BA, Grundy FJ, Henkin TM. 63.  2008. Natural variability in S-adenosylmethionine (SAM)-dependent riboswitches: S-box elements in Bacillus subtilis exhibit differential sensitivity to SAM in vivo and in vitro. J. Bacteriol. 37:123–31 [Google Scholar]
  64. Wachter A, Tunc-Ozdemir M, Grove BC, Green PJ, Shintani DK, Breaker RR. 64.  2007. Riboswitch control of gene expression in plants by splicing and alternative 3′ end processing of mRNAs. Plant Cell 19:3437–50 [Google Scholar]
  65. Wang JX, Lee ER, Morales DR, Lim J, Breaker RR. 65.  2015. Riboswitches that sense S-adenosylhomocysteine and activate genes involved in coenzyme recycling. Mol. Cell 29:691–702 [Google Scholar]
  66. Watson PY, Fedor MJ. 66.  2012. The ydaO motif is an ATP-sensing riboswitch in Bacillus subtilis. Nat. Chem. Biol. 8:963–65 [Google Scholar]
  67. Wickiser JK, Winkler WC, Breaker RR, Crothers DM. 67.  2005. The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch. Mol. Cell 18:49–60 [Google Scholar]
  68. Wickiser JK, Cheah MT, Breaker RR, Crothers DM. 68.  2005. The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 44:13404–14 [Google Scholar]
  69. Wilson RC, Smith AM, Fuchs RT, Kleckner IR, Henkin TM, Foster MP. 69.  2011. Tuning riboswitch regulation through conformational selection. J. Mol. Biol. 405:926–38 [Google Scholar]
  70. Wilson-Mitchell SN, Grundy FJ, Henkin TM. 70.  2012. Analysis of lysine recognition and specificity of the Bacillus subtilis L box riboswitch. Nucleic Acids Res. 40:5706–17 [Google Scholar]
  71. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. 71.  2004. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281–86 [Google Scholar]
  72. Yousef MR, Grundy FJ, Henkin TM. 72.  2005. Structural transitions induced by the interaction between tRNAGly and the Bacillus subtilis glyQS T box leader RNA. J. Mol. Biol. 349:273–87 [Google Scholar]
  73. Zhang J, Ferré-D'Amaré AR. 73.  2013. Co-crystal structure of a T-box riboswitch stem I domain in complex with its cognate tRNA. Nature 500:363–66 [Google Scholar]
  74. Zhang J, Ferré-D'Amaré AR. 74.  2014. Direct evaluation of tRNA aminoacylation status by the T-box riboswitch using tRNA-mRNA stacking and steric readout. Mol. Cell 55:148–55 [Google Scholar]
  75. Zhang J, Jones CP, Ferré-D'Amaré AR. 75.  2014. Global analysis of riboswitches by small-angle X-ray scattering and calorimetry. Biochim. Biophys. Acta 1839:1020–29 [Google Scholar]
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Riboswitch-Mediated Gene Regulation: Novel RNA Architectures Dictate Gene Expression Responses
Annual Review of Microbiology 70, 361 (2016); https://doi.org/10.1146/annurev-micro-091014-104306
/content/journals/10.1146/annurev-micro-091014-104306
/content/journals/10.1146/annurev-micro-091014-104306
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