The role of mRNA structure in bacterial translational regulation

The characteristics of bacterial messenger RNAs (mRNAs) that influence translation efficiency provide many convenient handles for regulation of gene expression, especially when coupled with the processes of transcription termination and mRNA degradation. An mRNA's structure, especially near the site of initiation, has profound consequences for how readily it is translated. This property allows bacterial gene expression to be altered by changes to mRNA structure induced by temperature, or interactions with a wide variety of cellular components including small molecules, other RNAs (such as sRNAs and tRNAs), and RNA‐binding proteins. This review discusses the links between mRNA structure and translation efficiency, and how mRNA structure is manipulated by conditions and signals within the cell to regulate gene expression. The range of RNA regulators discussed follows a continuum from very complex tertiary structures such as riboswitch aptamers and ribosomal protein‐binding sites to thermosensors and mRNA:sRNA interactions that involve only base‐pairing interactions. Furthermore, the high degrees of diversity observed for both mRNA structures and the mechanisms by which inhibition of translation occur have significant consequences for understanding the evolution of bacterial translational regulation. WIREs RNA 2017, 8:e1370. doi: 10.1002/wrna.1370

[1]  T. Henkin,et al.  Interaction between the acceptor end of tRNA and the T box stimulates antitermination in the Bacillus subtilis tyrS gene: a new role for the discriminator base , 1994, Journal of bacteriology.

[2]  M. Rosenberg,et al.  rho Is Not Essential for Viability or Virulence inStaphylococcus aureus , 2001, Antimicrobial Agents and Chemotherapy.

[3]  Sriram Kosuri,et al.  Causes and Effects of N-Terminal Codon Bias in Bacterial Genes , 2013, Science.

[4]  G. Storz,et al.  An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin , 2007, Molecular microbiology.

[5]  Jeffrey E. Barrick,et al.  Coenzyme B12 riboswitches are widespread genetic control elements in prokaryotes. , 2004, Nucleic acids research.

[6]  T. A. Krulwich,et al.  Identification of a putative Bacillus subtilis rho gene , 1993, Journal of bacteriology.

[7]  M. Sørensen,et al.  Absolute in vivo translation rates of individual codons in Escherichia coli. The two glutamic acid codons GAA and GAG are translated with a threefold difference in rate. , 1991, Journal of molecular biology.

[8]  I. Boni,et al.  Regulation of the rplY gene encoding 5S rRNA binding protein L25 in Escherichia coli and related bacteria , 2015, RNA.

[9]  Vitaly Epshtein,et al.  Riboswitch control of Rho-dependent transcription termination , 2012, Proceedings of the National Academy of Sciences.

[10]  E. Wagner,et al.  RNA antitoxins. , 2007, Current opinion in microbiology.

[11]  M. Grunberg‐Manago,et al.  Translational autocontrol of the Escherichia coli ribosomal protein S15. , 1990, Journal of molecular biology.

[12]  C. Condon,et al.  The phylogenetic distribution of bacterial ribonucleases. , 2002, Nucleic acids research.

[13]  R. Batey,et al.  Structure of the SAM-II riboswitch bound to S-adenosylmethionine , 2008, Nature Structural &Molecular Biology.

[14]  F. Repoila,et al.  Fresh layers of RNA-mediated regulation in Gram-positive bacteria. , 2016, Current opinion in microbiology.

[15]  J. Vogel,et al.  An antisense RNA inhibits translation by competing with standby ribosomes. , 2007, Molecular cell.

[16]  T. Hwa,et al.  Quantitative Characteristics of Gene Regulation by Small RNA , 2007, PLoS Biology.

[17]  M. Cusick,et al.  Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Michael I. Jordan,et al.  Toward a protein profile of Escherichia coli: Comparison to its transcription profile , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Satoru Miyano,et al.  Prediction of Transcriptional Terminators in Bacillus subtilis and Related Species , 2005, PLoS Comput. Biol..

[20]  G Humphreys,et al.  Codon usage can affect efficiency of translation of genes in Escherichia coli. , 1984, Nucleic acids research.

[21]  Rob Knight,et al.  Structural basis for diversity in the SAM clan of riboswitches , 2014, Proceedings of the National Academy of Sciences.

[22]  J. Bujnicki,et al.  Loss of Conserved Noncoding RNAs in Genomes of Bacterial Endosymbionts , 2016, Genome biology and evolution.

[23]  G. Storz,et al.  Small Toxic Proteins and the Antisense RNAs That Repress Them , 2008, Microbiology and Molecular Biology Reviews.

[24]  E. Nudler,et al.  RNA polymerase and the ribosome: the close relationship. , 2013, Current opinion in microbiology.

[25]  H. Schwalbe,et al.  Translation on demand by a simple RNA-based thermosensor , 2010, Nucleic acids research.

[26]  Jeffrey E. Barrick,et al.  The distributions, mechanisms, and structures of metabolite-binding riboswitches , 2007, Genome Biology.

[27]  J. Cole,et al.  Changes in the half-life of ribosomal protein messenger RNA caused by translational repression. , 1986, Journal of molecular biology.

[28]  A. Serganov,et al.  Do mRNA and rRNA binding sites of E.coli ribosomal protein S15 share common structural determinants? , 2002, Journal of molecular biology.

[29]  Torsten Waldminghaus,et al.  Genome-wide bioinformatic prediction and experimental evaluation of potential RNA thermometers , 2007, Molecular Genetics and Genomics.

[30]  W. Winkler,et al.  Multiple posttranscriptional regulatory mechanisms partner to control ethanolamine utilization in Enterococcus faecalis , 2009, Proceedings of the National Academy of Sciences.

[31]  S. Even,et al.  Ribosomal protein L20 controls expression of the Bacillus subtilis infC operon via a transcription attenuation mechanism , 2007, Nucleic acids research.

[32]  G. W. Hatfield,et al.  Codon Pair Utilization Biases Influence Translational Elongation Step Times (*) , 1995, The Journal of Biological Chemistry.

[33]  H. Margalit,et al.  Accessibility and Evolutionary Conservation Mark Bacterial Small-RNA Target-Binding Regions , 2011, Journal of bacteriology.

[34]  N. Amrani,et al.  Translational regulation of gene expression , 2004, Genome Biology.

[35]  Christopher A. Voigt,et al.  Automated design of synthetic ribosome binding sites to control protein expression , 2016 .

[36]  G. Dougan,et al.  Cooperation Between Translating Ribosomes and RNA Polymerase in Transcription Elongation , 2010, Science.

[37]  Arkady B. Khodursky,et al.  Global analysis of mRNA decay and abundance in Escherichia coli at single-gene resolution using two-color fluorescent DNA microarrays , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[38]  R. Batey,et al.  B12 cofactors directly stabilize an mRNA regulatory switch , 2012, Nature.

[39]  M. Meyer,et al.  Most RNAs regulating ribosomal protein biosynthesis in Escherichia coli are narrowly distributed to Gammaproteobacteria , 2013, Nucleic acids research.

[40]  Andrey A Mironov,et al.  Regulation of the vitamin B12 metabolism and transport in bacteria by a conserved RNA structural element. , 2003, RNA.

[41]  G. Krishnamoorthy,et al.  Site-specific fluorescence dynamics in an RNA ‘thermometer’ reveals the role of ribosome binding in its temperature-sensitive switch function , 2014, Nucleic acids research.

[42]  F. Narberhaus,et al.  Molecular basis for temperature sensing by an RNA thermometer , 2006, The EMBO journal.

[43]  É. Massé,et al.  Dual-acting riboswitch control of translation initiation and mRNA decay , 2012, Proceedings of the National Academy of Sciences.

[44]  M. Nomura,et al.  Feedback regulation of ribosomal protein gene expression in Escherichia coli. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[45]  M. Springer,et al.  Double molecular mimicry in Escherichia coli: binding of ribosomal protein L20 to its two sites in mRNA is similar to its binding to 23S rRNA , 2005, Molecular microbiology.

[46]  S. Cohen,et al.  A+U content rather than a particular nucleotide order determines the specificity of RNase E cleavage. , 1994, The Journal of biological chemistry.

[47]  S. Gottesman,et al.  Competition among Hfq‐binding small RNAs in Escherichia coli , 2011, Molecular microbiology.

[48]  Jos Vanderleyden,et al.  RNA-binding proteins involved in post-transcriptional regulation in bacteria , 2015, Front. Microbiol..

[49]  S. Altuvia,et al.  Alternative mRNA structures of the cIII gene of bacteriophage lambda determine the rate of its translation initiation. , 1989, Journal of molecular biology.

[50]  G. Storz,et al.  Modulating the outer membrane with small RNAs. , 2006, Genes & development.

[51]  E. Wagner,et al.  Small RNAs in bacteria and archaea: who they are, what they do, and how they do it. , 2015, Advances in genetics.

[52]  H. Salis,et al.  Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites , 2013, Nucleic acids research.

[53]  J. Friesen,et al.  RNA secondary structure and translation inhibition: analysis of mutants in the rplJ leader. , 1984, The EMBO journal.

[54]  J. Steitz,et al.  How ribosomes select initiator regions in mRNA: base pair formation between the 3' terminus of 16S rRNA and the mRNA during initiation of protein synthesis in Escherichia coli. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Saman Halgamuge,et al.  Analysis of SD sequences in completed microbial genomes: non-SD-led genes are as common as SD-led genes. , 2006, Gene.

[56]  R. Kadner,et al.  Adenosylcobalamin inhibits ribosome binding to btuB RNA. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  M. Meyer,et al.  RNA structures regulating ribosomal protein biosynthesis in bacilli , 2013, RNA biology.

[58]  T. Henkin,et al.  S-adenosylmethionine directly inhibits binding of 30S ribosomal subunits to the SMK box translational riboswitch RNA , 2007, Proceedings of the National Academy of Sciences.

[59]  N. Majdalani,et al.  The RpoS-mediated general stress response in Escherichia coli. , 2011, Annual review of microbiology.

[60]  K. Jensen,et al.  The RNA chain elongation rate in Escherichia coli depends on the growth rate , 1994, Journal of bacteriology.

[61]  É. Massé,et al.  Noncanonical repression of translation initiation through small RNA recruitment of the RNA chaperone Hfq. , 2012, Genes & development.

[62]  S. Tishchenko,et al.  Ribosomal protein L1 recognizes the same specific structural motif in its target sites on the autoregulatory mRNA and 23S rRNA , 2005, Nucleic acids research.

[63]  Shigeyuki Yokoyama,et al.  A snapshot of the 30S ribosomal subunit capturing mRNA via the Shine-Dalgarno interaction. , 2007, Structure.

[64]  J. Belasco,et al.  Lost in translation: the influence of ribosomes on bacterial mRNA decay. , 2005, Genes & development.

[65]  M. Nomura,et al.  Regulation of ribosomal protein synthesis in Escherichia coli by selective mRNA inactivation. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Y. Pilpel,et al.  An Evolutionarily Conserved Mechanism for Controlling the Efficiency of Protein Translation , 2010, Cell.

[67]  Ali Nahvi,et al.  Genetic control by a metabolite binding mRNA. , 2002, Chemistry & biology.

[68]  P. Romby,et al.  Base Pairing Interaction between 5′- and 3′-UTRs Controls icaR mRNA Translation in Staphylococcus aureus , 2013, PLoS genetics.

[69]  N. Brot,et al.  Autogenous control of Escherichia coli ribosomal protein L10 synthesis in vitro. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[70]  M. Saier,et al.  Comparative genomics of metabolic capacities of regulons controlled by cis-regulatory RNA motifs in bacteria , 2013, BMC Genomics.

[71]  G. Soberón-Chávez,et al.  RNA structures are involved in the thermoregulation of bacterial virulence-associated traits. , 2015, Trends in microbiology.

[72]  Grant S. Jones,et al.  Posttranscriptional Self-Regulation by the Lyme Disease Bacterium's BpuR DNA/RNA-Binding Protein , 2013, Journal of bacteriology.

[73]  T. Ikemura.  Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. , 1981, Journal of molecular biology.

[74]  Ignacio Tinoco,et al.  Ribosomal protein S1 unwinds double-stranded RNA in multiple steps , 2012, Proceedings of the National Academy of Sciences.

[75]  P. Cossart,et al.  Unexpected versatility in bacterial riboswitches. , 2015, Trends in genetics : TIG.

[76]  E. Papoutsakis,et al.  Synthetic tolerance: three noncoding small RNAs, DsrA, ArcZ and RprA, acting supra-additively against acid stress , 2013, Nucleic acids research.

[77]  G. Stormo,et al.  Translation initiation in Escherichia coli: sequences within the ribosome‐binding site , 1992, Molecular microbiology.

[78]  H. Margalit,et al.  Evolutionary patterns of Escherichia coli small RNAs and their regulatory interactions , 2014, RNA.

[79]  P. Babitzke,et al.  Ribosomal protein L10(L12)4 autoregulates expression of the Bacillus subtilis rplJL operon by a transcription attenuation mechanism , 2015, Nucleic acids research.

[80]  Reinhard Wolf,et al.  Coding-Sequence Determinants of Gene Expression in Escherichia coli , 2009 .

[81]  Manfred Kröger,et al.  Compilation of DNA sequences of Escherichia coli K12: description of the interactive databases ECD and ECDC , 1998, Nucleic Acids Res..

[82]  M. Grunberg‐Manago,et al.  Domains of the Escherichia coli threonyl-tRNA synthetase translational operator and their relation to threonine tRNA isoacceptors. , 1992, Journal of Molecular Biology.

[83]  C. Yanofsky.  Attenuation in the control of expression of bacterial operons , 1981, Nature.

[84]  C. Yanofsky,et al.  Biochemical Features and Functional Implications of the RNA-Based T-Box Regulatory Mechanism , 2009, Microbiology and Molecular Biology Reviews.

[85]  C. Dutta,et al.  Codon usage in highly expressed genes of Haemophillus influenzae and Mycobacterium tuberculosis: translational selection versus mutational bias. , 1998, Gene.

[86]  S. Marzi,et al.  Multiple ways to regulate translation initiation in bacteria: Mechanisms, regulatory circuits, dynamics. , 2015, Biochimie.

[87]  A. Kolb,et al.  Nucleic acid helix-unwinding properties of ribosomal protein S1 and the role of S1 in mRNA binding to ribosomes. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[88]  H. Schwalbe,et al.  Direct observation of the temperature-induced melting process of the Salmonella fourU RNA thermometer at base-pair resolution , 2010, Nucleic acids research.

[89]  G. Storz,et al.  Bacterial small RNA regulators: versatile roles and rapidly evolving variations. , 2011, Cold Spring Harbor perspectives in biology.

[90]  Tony Romeo,et al.  Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. , 2013, Environmental microbiology.

[91]  S. Ehrlich,et al.  The Bacillus subtilis chromosome region encoding homologues of the Escherichia coli mssA and rpsA gene products. , 1995, Microbiology.

[92]  S. Gottesman,et al.  A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[93]  L. Lindahl,et al.  Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. , 1994, Progress in nucleic acid research and molecular biology.

[94]  A. Serganov,et al.  Structural insights into amino acid binding and gene control by a lysine riboswitch , 2008, Nature.

[95]  M. Nomura,et al.  Localization of the target site for translational regulation of the L11 operon and direct evidence for translational coupling in Escherichia coli , 1983, Cell.

[96]  O. Berg,et al.  Mutational Robustness of Ribosomal Protein Genes , 2010, Science.

[97]  Christopher J. Marx,et al.  Good Codons, Bad Transcript: Large Reductions in Gene Expression and Fitness Arising from Synonymous Mutations in a Key Enzyme , 2012, Molecular biology and evolution.

[98]  J. Ilan.  Translational Regulation of Gene Expression 2 , 2012, Springer US.

[99]  J. van Duin,et al.  Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[100]  P. Gröbner,et al.  Control of ribosomal protein L1 synthesis in mesophilic and thermophilic archaea. , 1999, Genetics.

[101]  T. Henkin,et al.  The SMK box is a new SAM-binding RNA for translational regulation of SAM synthetase , 2006, Nature Structural &Molecular Biology.

[102]  M. Grunberg‐Manago,et al.  Autogenous control of Escherichia coli threonyl-tRNA synthetase expression in vivo. , 1985, Journal of molecular biology.

[103]  Betty L. Slinger,et al.  Co-evolution of Bacterial Ribosomal Protein S15 with Diverse mRNA Regulatory Structures , 2015, PLoS genetics.

[104]  Hashim M. Al-Hashimi,et al.  Functional complexity and regulation through RNA dynamics , 2012, Nature.

[105]  David H Burkhardt,et al.  Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources , 2014, Cell.

[106]  C. Pál,et al.  An integrated view of protein evolution , 2006, Nature Reviews Genetics.

[107]  C. Ehresmann,et al.  The expression of E.coli threonyl‐tRNA synthetase is regulated at the translational level by symmetrical operator‐repressor interactions. , 1996, The EMBO journal.

[108]  A. D. Jones,et al.  CsrA Regulates Translation of the Escherichia coli Carbon Starvation Gene, cstA, by Blocking Ribosome Access to the cstA Transcript , 2003, Journal of bacteriology.

[109]  C. Gualerzi,et al.  The cspA mRNA is a thermosensor that modulates translation of the cold-shock protein CspA. , 2010, Molecular cell.

[110]  G. Storz,et al.  The base-pairing RNA spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. , 2011, Molecular cell.

[111]  Christopher A. Vakulskas,et al.  Translational Repression of NhaR, a Novel Pathway for Multi-Tier Regulation of Biofilm Circuitry by CsrA , 2011, Journal of bacteriology.

[112]  S. Altuvia,et al.  Changes in transcriptional pausing modify the folding dynamics of the pH-responsive RNA element , 2013, Nucleic acids research.

[113]  P. Babitzke,et al.  CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli , 2002, Molecular microbiology.

[114]  P. Cossart,et al.  An RNA Thermosensor Controls Expression of Virulence Genes in Listeria monocytogenes , 2002, Cell.

[115]  Jean-François Jacques,et al.  The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis , 2007, Molecular microbiology.

[116]  A. Serganov,et al.  Structured mRNAs Regulate Translation Initiation by Binding to the Platform of the Ribosome , 2007, Cell.

[117]  S. Gottesman,et al.  Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. , 2003, Genes & development.

[118]  S. Joseph,et al.  Unfolding of mRNA secondary structure by the bacterial translation initiation complex. , 2006, Molecular cell.

[119]  P. Dennis,et al.  Cluster of genes in Escherichia coli for ribosomal proteins, ribosomal RNA, and RNA polymerase subunits. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[120]  M. Grunberg‐Manago,et al.  Escherichia coli threonyl-tRNA synthetase and tRNA(Thr) modulate the binding of the ribosome to the translational initiation site of the thrS mRNA. , 1990, Journal of molecular biology.

[121]  R. Micura,et al.  Escherichia coli Ribosomal Protein S1 Unfolds Structured mRNAs Onto the Ribosome for Active Translation Initiation , 2013, PLoS biology.

[122]  J. Richardson.  Rho-dependent transcription termination. , 1990, Biochimica et biophysica acta.

[123]  Zasha Weinberg,et al.  Structural, functional, and taxonomic diversity of three preQ1 riboswitch classes. , 2014, Chemistry & biology.

[124]  M. Meyer,et al.  An S6:S18 complex inhibits translation of E. coli rpsF , 2015, RNA.

[125]  Adam Roth,et al.  Confirmation of a second natural preQ1 aptamer class in Streptococcaceae bacteria. , 2008, RNA.

[126]  M. Nomura,et al.  E. coli ribosomal protein L10 inhibits translation of L10 and L7/L12 mRNAs by acting at a single site , 1981, Nature.

[127]  M. Gelfand,et al.  Riboswitches: the oldest mechanism for the regulation of gene expression? , 2004, Trends in genetics : TIG.

[128]  J. Rabinowitz,et al.  The effect of ribosomal protein S1 from Escherichia coli and Micrococcus luteus on protein synthesis in vitro by E. coli and Bacillus subtilis , 1992, Molecular microbiology.

[129]  J. Shine,et al.  Terminal-sequence analysis of bacterial ribosomal RNA. Correlation between the 3'-terminal-polypyrimidine sequence of 16-S RNA and translational specificity of the ribosome. , 1975, European journal of biochemistry.

[130]  Wenting Liu,et al.  Robust Identification of Noncoding RNA from Transcriptomes Requires Phylogenetically-Informed Sampling , 2014, PLoS Comput. Biol..

[131]  Z. She,et al.  Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes , 2011, BMC Genomics.

[132]  H. Noller,et al.  Interactions and dynamics of the Shine–Dalgarno helix in the 70S ribosome , 2007, Proceedings of the National Academy of Sciences.

[133]  Bernard Rees,et al.  Structural basis for messenger RNA movement on the ribosome , 2006, Nature.

[134]  W. Winkler,et al.  Expanding roles for metabolite-sensing regulatory RNAs. , 2009, Current opinion in microbiology.

[135]  Rotem Sorek,et al.  Differential translation tunes uneven production of operon-encoded proteins. , 2013, Cell reports.

[136]  P. Romby,et al.  When Ribonucleases Come into Play in Pathogens: A Survey of Gram-Positive Bacteria , 2012, International journal of microbiology.

[137]  Nicholas T. Ingolia,et al.  Genome-Wide Analysis in Vivo of Translation with Nucleotide Resolution Using Ribosome Profiling , 2009, Science.

[138]  D C Shields,et al.  Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens; a review of the considerable within-species diversity. , 1988, Nucleic acids research.

[139]  L. Bossi,et al.  RNA remodeling by bacterial global regulator CsrA promotes Rho-dependent transcription termination , 2014, Genes & development.

[140]  Gang Wu,et al.  Correlation of mRNA Expression and Protein Abundance Affected by Multiple Sequence Features Related to Translational Efficiency in Desulfovibrio vulgaris: A Quantitative Analysis , 2006, Genetics.

[141]  Florian C. Oberstrass,et al.  Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA , 2007, Nature Structural &Molecular Biology.

[142]  M. Springer,et al.  The relationship between translational control and mRNA degradation for the Escherichia coli threonyl-tRNA synthetase gene. , 2001, Journal of molecular biology.

[143]  J C Rabinowitz,et al.  The influence of ribosome‐binding‐site elements on translational efficiency in Bacillus subtilis and Escherichia coli in vivo , 1992, Molecular microbiology.

[144]  T. Henkin,et al.  Crystal structures of the SAM-III/SMK riboswitch reveal the SAM-dependent translation inhibition mechanism , 2008, Nature Structural &Molecular Biology.

[145]  Pascale Romby,et al.  Structural basis of translational control by Escherichia coli threonyl tRNA synthetase , 2002, Nature Structural Biology.

[146]  Xiangwu Nou,et al.  Coupled Changes in Translation and Transcription during Cobalamin-Dependent Regulation of btuB Expression inEscherichia coli , 1998, Journal of bacteriology.

[147]  P. Valentin‐Hansen,et al.  Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. , 2002, Genes & development.

[148]  T. Romeo,et al.  The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein , 1997, Journal of bacteriology.

[149]  Mark A. Ragan,et al.  Evolutionary Dynamics of Small RNAs in 27 Escherichia coli and Shigella Genomes , 2012, Genome biology and evolution.

[150]  G. Braus,et al.  One Juliet and four Romeos: VeA and its methyltransferases , 2015, Front. Microbiol..

[151]  Dan S. Tawfik,et al.  Mutational effects and the evolution of new protein functions , 2010, Nature Reviews Genetics.

[152]  M. Inouye,et al.  Nonsense Mutations in cspA Cause Ribosome Trapping Leading to Complete Growth Inhibition and Cell Death at Low Temperature in Escherichia coli * , 2001, The Journal of Biological Chemistry.

[153]  M. Tomita,et al.  Analysis of complete genomes suggests that many prokaryotes do not rely on hairpin formation in transcription termination. , 1998, Nucleic acids research.

[154]  Y. Kyōgoku,et al.  Translational induction of heat shock transcription factor sigma32: evidence for a built-in RNA thermosensor. , 1999, Genes & development.

[155]  M. Gong,et al.  Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties , 1993, Journal of bacteriology.

[156]  Gene-Wei Li,et al.  The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria , 2012, Nature.

[157]  Asaminew H. Aytenfisu,et al.  Molecular mechanism for preQ1-II riboswitch function revealed by molecular dynamics , 2015, RNA.

[158]  J. Richardson,et al.  Phylogenetic analysis of sequences from diverse bacteria with homology to the Escherichia coli rho gene , 1994, Journal of bacteriology.

[159]  Chantal Ehresmann,et al.  Structural elements of rps0 mRNA involved in the modulation of translational initiation and regulation of E. coli ribosomal protein S15 , 1994, Nucleic Acids Res..

[160]  G. Storz,et al.  Bacterial antisense RNAs: how many are there, and what are they doing? , 2010, Annual review of genetics.

[161]  E. Marcotte,et al.  Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation , 2007, Nature Biotechnology.

[162]  P. Babitzke,et al.  Complex regulation of the global regulatory gene csrA: CsrA‐mediated translational repression, transcription from five promoters by Eσ70 and EσS, and indirect transcriptional activation by CsrA , 2011, Molecular microbiology.

[163]  P. Sharp,et al.  Codon usage and gene expression level in Dictyostelium discoideum: highly expressed genes do 'prefer' optimal codons. , 1989, Nucleic acids research.

[164]  R. Montange,et al.  Structure of the S-adenosylmethionine riboswitch regulatory mRNA element , 2006, Nature.

[165]  C. Ehresmann,et al.  Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[166]  M. Yusupov,et al.  One core, two shells: bacterial and eukaryotic ribosomes , 2012, Nature Structural &Molecular Biology.

[167]  C. Gualerzi,et al.  Leaderless mRNAs in bacteria: surprises in ribosomal recruitment and translational control , 2002, Molecular microbiology.

[168]  A. Serganov,et al.  A Decade of Riboswitches , 2013, Cell.

[169]  D. Draper,et al.  Translational repression of the Escherichia coli alpha operon mRNA: importance of an mRNA conformational switch and a ternary entrapment complex. , 2001, The Journal of biological chemistry.

[170]  R. Aebersold,et al.  Quantification of mRNA and protein and integration with protein turnover in a bacterium , 2011, Molecular systems biology.

[171]  B. S. Laursen,et al.  Initiation of Protein Synthesis in Bacteria , 2005, Microbiology and Molecular Biology Reviews.

[172]  Adrianne N. Edwards,et al.  Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. , 2009, Journal of molecular biology.

[173]  G. Storz,et al.  Regulation by small RNAs in bacteria: expanding frontiers. , 2011, Molecular cell.

[174]  T. D. Schneider,et al.  Characterization of Translational Initiation Sites in E. Coui , 1982 .

[175]  M. Springer,et al.  Messenger RNA secondary structure and translational coupling in the Escherichia coli operon encoding translation initiation factor IF3 and the ribosomal proteins, L35 and L20. , 1992, Journal of molecular biology.

[176]  J. van Duin,et al.  Translational standby sites: how ribosomes may deal with the rapid folding kinetics of mRNA. , 2003, Journal of molecular biology.

[177]  S. Gottesman,et al.  Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA , 2010, The EMBO journal.

[178]  P. Babitzke,et al.  Positive regulation of motility and flhDC expression by the RNA‐binding protein CsrA of Escherichia coli , 2001, Molecular microbiology.

[179]  M. Gouy,et al.  Codon usage in bacteria: correlation with gene expressivity. , 1982, Nucleic acids research.

[180]  Wade C. Winkler,et al.  A riboswitch-containing sRNA controls gene expression by sequestration of a response regulator , 2014, Science.

[181]  N. V. Tzareva,et al.  Ribosome‐messenger recognition in the absence of the Shine‐Dalgarno interactions , 1994, FEBS letters.

[182]  M. DePristo,et al.  Missense meanderings in sequence space: a biophysical view of protein evolution , 2005, Nature Reviews Genetics.

[183]  T. D. Schneider,et al.  Quantitative analysis of ribosome binding sites in E.coli. , 1994, Nucleic acids research.

[184]  M. Waldor,et al.  Characterization of the Small Untranslated RNA RyhB and Its Regulon in Vibrio cholerae , 2005, Journal of bacteriology.

[185]  Xin Wang,et al.  A novel sRNA component of the carbon storage regulatory system of Escherichia coli , 2003, Molecular microbiology.

[186]  P. Babitzke,et al.  RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. , 2005, RNA.

[187]  T. Henkin,et al.  T box riboswitches in Actinobacteria: Translational regulation via novel tRNA interactions , 2015, Proceedings of the National Academy of Sciences.

[188]  Sean R. Eddy,et al.  Infernal 1.1: 100-fold faster RNA homology searches , 2013, Bioinform..

[189]  Ryan T Fuchs,et al.  The SAM‐responsive SMK box is a reversible riboswitch , 2010, Molecular microbiology.

[190]  J. Richardson,et al.  Transcription termination factor rho activity is altered in Escherichia coli with suA gene mutations. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[191]  S. Karlin,et al.  Correlations between Shine-Dalgarno Sequences and Gene Features Such as Predicted Expression Levels and Operon Structures , 2002, Journal of bacteriology.