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ppGpp DNA-binding transcriptional dual regulator

Summary:
The nucleotides ppGpp (guanosine 3'-diphosphate 5'-diphosphate) and pppGpp (guanosine 3'-diphosphate 5'-triphosphate), referred to collectively as (p)ppGpp, have been shown to regulate gene expression during the stringent response in some bacteria. Their levels become elevated during this response and they are key indicators and regulators of it. The stringent response is a global regulatory system that operates under conditions of nutrient or energy starvation or other environmental stress. It has varying effects on gene expression and metabolism.
To identify transcripts regulated by ppGpp, this compound was produced by conditional expression of RelA 30971496. In general, biosynthesis genes (including amino acid biosynthesis, fatty acid biosynthesis, and nucleotide biosynthesis genes) responded to ppGpp induction. Many amino acid biosynthesis pathways showed increased expression, but ppGpp did not increase expression of all amino acid biosynthesis pathways to the same extent 30971496.
Many genes involved in response to stimulus, including genes for the response to DNA damage, osmotic stress, oxidants, and environmental treatments, unexpectedly responded to ppGpp. These results suggest that ppGpp senses not only nutrition-based stresses. For example, a high percentage of cold response genes appear to be sensitive to ppGpp 30971496.
A large number of genes related to nucleotide, protein, and RNA metabolism, translation, and DNA synthesis are negatively regulated by ppGpp.
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Transcription factor      
Gene name: dksA
  Genome position: 160149-160604
  Length: 456 bp / 151 aa
Operon name: sfsA-dksA-gluQ
TU(s) encoding the TF:
Transcription unit        Promoter
dksA-gluQ
dksAp3
dksA-yadB
dksAp1
dksA-yadB
dksAp2
sfsA-dksA
sfsAp


Regulon       
Regulated gene(s) alaT, alaU, alaV, argI, argS, argT, argX, bolA, cfa, crp, csgD, csgE, csgF, csgG, cspA, cspD, dksA, dnaA, dnaN, dusB, efp, fadD, fadL, fimB, fis, fkpA, folK, frr, ftsA, ftsK, ftsQ, ftsZ, gabD, gabP, gabT, gadA, gadX, glaH, glgA, glgC, glgP, glnU, glnV, glnW, glnX, glsA, gltT, gltU, gltV, gltW, gluQ, glyT, grxB, hisJ, hisM, hisP, hisQ, hisR, hmp, idlP, ileT, ileU, ileV, ilvA, ilvB,
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Multifun term(s) of regulated gene(s) MultiFun Term (List of genes associated to the multifun term)
tRNA (33)
translation (33)
ribosomes (28)
rRNA, stable RNA (22)
Transcription related (13)
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Regulated operon(s) argI, argS, argT-hisJQMP, argX-hisR-leuT-proM, asnC-mioC-mnmG-rsmG, bdm-sra, bolA, cfa, crp, csgDEFG, cspA, cspD, dnaAN-recF, dusB-fis, efp, fadD-sroD, fadL, fimB, fkpA, frr, ftsK, gadAXW, glaH-lhgD-gabDTP, glgBXCAP, glsA-ybaT, grxB, hmp, ilvIH, ilvLXGMEDA, infA-serW, iraP, ivbL-ilvBN-uhpABC, leuLABCD, leuO, leuX, livJ, lrp, metT-leuW-glnUW-metU-glnVX, metY-rimP-nusA-infB-rbfA-truB-rpsO-pnp, metZWV, mraZ-rsmH-ftsLI-murEF-mraY-murD-ftsW-murGC-ddlB-ftsQAZ-lpxC, nlpD-rpoS, pcnB-folK, pyrLBI, qorA, queA, relA-mazEFG, rmf, rpmE, rrsA-ileT-alaT-rrlA-rrfA, rrsB-gltT-rrlB-rrfB, rrsC-gltU-rrlC-rrfC, rrsD-ileU-alaU-rrlD-rrfD-thrV-rrfF, rrsE-gltV-rrlE-rrfE, rrsG-gltW-rrlG-rrfG, rrsH-ileV-alaV-rrlH-rrfH, rseD-rpoE-rseABC, sfsA-dksA-gluQ, sgrR-sroA-thiBPQ, sgrST-setA, speC, tff-rpsB-tsf, thrU-tyrU-glyT-thrT-tufB, trxA, tyrTV-tpr,
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First gene in the operon(s) argI, argS, argT, argX, bolA, cfa, crp, csgD, glaH, cspA, cspD, dksA, dnaA, dnaA, dusB, efp, fadD, fadL, fimB, fkpA, frr, ftsK, ftsQ, ftsZ, ftsZ, gadA, glgC, glgC, glsA, grxB, hmp, ilvI, ilvL, ilvL, idlP, ytiC, iraP, ivbL, ivbL, leuL, leuL, leuO, leuX, livJ, lrp, mazE, metT, metZ, mioC, mnmG, pcnB, pcnB, pyrL, qorA, queA, relA, rmf, rpmE, rpoE, rpoS, tff, rpsO, rpsO, rrsA, rrsB,
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Simple and complex regulatory phrases Regulatory phrase (List of promoters regulated by the phrase)


Transcription factor regulation    


Transcription factor binding sites (TFBSs) arrangements
      

  Functional conformation Function Promoter Sigma factor Central Rel-Pos Distance to first Gene Genes Sequence LeftPos RightPos Evidence (Confirmed, Strong, Weak) References
  ppGpp activation argIp Sigma70 nd nd argI nd nd [GEA] [1]
  ppGpp inhibition argSp Sigma70 nd nd argS nd nd [GEA] [2]
  ppGpp inhibition argTp Sigma54 nd nd argT, hisJ, hisQ, hisM, hisP nd nd [GEA], [IEP] [3], [4]
  ppGpp inhibition argXp Sigma70 nd nd argX, hisR, leuT, proM nd nd [IDA] [5]
  ppGpp activation bolAp1 Sigma38, Sigma70 nd nd bolA nd nd [GEA], [IEP] [2], [6]
  ppGpp activation cfap1 Sigma38, Sigma70 nd nd cfa nd nd [GEA] [6]
  ppGpp inhibition crpp2 nd nd nd crp nd nd [IEP] [7]
  ppGpp activation csgDp1 Sigma38, Sigma70 nd nd csgD, csgE, csgF, csgG nd nd [GEA] [8]
  ppGpp activation csiDp Sigma38 nd nd glaH, lhgD, gabD, gabT, gabP nd nd [2]
  ppGpp inhibition cspAp1 Sigma70 nd nd cspA nd nd [GEA] [9]
  ppGpp activation cspDp Sigma70 nd nd cspD nd nd [GEA] [8]
  ppGpp inhibition dksAp2 Sigma70 nd nd dksA, gluQ nd nd [GEA] [10]
  ppGpp inhibition dnaAp1 nd nd nd dnaA, dnaN, recF nd nd [GEA] [11]
  ppGpp inhibition dnaAp2 Sigma70 nd nd dnaA, dnaN, recF nd nd [GEA] [11]
  ppGpp inhibition dusBp Sigma70 nd nd dusB, fis nd nd [GEA], [IMP] [12]
  ppGpp inhibition efpp Sigma70 nd nd efp nd nd [GEA] [2]
  ppGpp activation fadDp Sigma70 nd nd fadD, sroD nd nd [GEA] [13]
  ppGpp activation fadLp Sigma38 nd nd fadL nd nd [GEA] [6]
  ppGpp activation fimBp2 nd nd nd fimB nd nd [GEA], [IDA] [14]
  ppGpp activation fkpAp1 Sigma24 nd nd fkpA nd nd [IEP] [15], [16]
  ppGpp inhibition frrp Sigma70 nd nd frr nd nd [GEA] [2]
  ppGpp activation ftsKp1 Sigma70 nd nd ftsK nd nd [GEA] [17]
  ppGpp activation ftsQp1 Sigma38, Sigma70 nd nd ftsQ, ftsA, ftsZ nd nd [IMP] [18], [19]
  ppGpp activation ftsZp3 nd nd nd ftsZ nd nd [IMP] [18], [19]
  ppGpp activation ftsZp4 nd nd nd ftsZ nd nd [IMP] [18], [19]
  ppGpp activation gadAp Sigma38, Sigma70, Sigma38, Sigma70 nd nd gadA, gadX nd nd [2]
  ppGpp activation glgCp1 Sigma70 nd nd glgC, glgA, glgP nd nd [IMP] [20]
  ppGpp activation glgCp2 nd nd nd glgC, glgA, glgP nd nd [IMP] [20]
  ppGpp activation glsAp Sigma38 nd nd glsA, ybaT nd nd [2]
  ppGpp activation grxBp Sigma70 nd nd grxB nd nd [GEA], [IMP] [21]
  ppGpp activation hmpp Sigma38 nd nd hmp nd nd [GEA] [22]
  ppGpp inhibition ilvIp2 nd nd nd ilvI, ilvH nd nd [GEA] [23]
  ppGpp activation ilvLp2 Sigma70 nd nd ilvL, ilvX, ilvG, ilvM, ilvE, ilvD, ilvA nd nd [GEA] [24]
  ppGpp activation iraDp1 Sigma70 nd nd ytiC, ytiD, idlP, iraD nd nd [GEA], [IMP] [25]
  ppGpp activation iraDp2 Sigma38, Sigma70 nd nd idlP, iraD nd nd [GEA], [IMP] [25]
  ppGpp activation iraPp1 Sigma70 nd nd iraP nd nd [GEA], [IMP] [26]
  ppGpp activation ivbLp Sigma70 nd nd ivbL, ilvB, ilvN nd nd [GEA] [24]
  ppGpp activation leuLp Sigma70 nd nd leuL, leuA, leuB, leuC, leuD nd nd [GEA], [IEP] [24], [27]
  ppGpp activation leuOp Sigma70 nd nd leuO nd nd [GEA], [IMP] [28]
  ppGpp inhibition leuXp Sigma70 nd nd leuX nd nd [IEP] [3]
  ppGpp activation livJp Sigma70 nd nd livJ nd nd [GEA] [1]
  ppGpp activation lrpp Sigma70 nd nd lrp nd nd [GEA] [29]
  ppGpp inhibition mazEp1 nd nd nd mazE, mazF, mazG nd nd [GEA] [30], [31]
  ppGpp inhibition metTp Sigma70 nd nd metT, leuW, glnU, glnW, metU, glnV, glnX nd nd [IEP] [3]
  ppGpp inhibition metZp Sigma70 nd nd metZ, metW, metV nd nd [IDA], [IHBCE] [32]
  ppGpp inhibition mioCp nd nd nd mioC nd nd [IEP] [33]
  ppGpp inhibition mnmGp Sigma38, Sigma70 nd nd mnmG, rsmG nd nd [IEP] [33]
  ppGpp inhibition pcnBp3 Sigma70, Sigma38 nd nd pcnB, folK nd nd [GEA] [34]
  ppGpp inhibition pcnBp4 Sigma38 nd nd pcnB, folK nd nd [GEA] [34]
  ppGpp inhibition pyrLp2 nd nd nd pyrL, pyrB, pyrI nd nd [GEA], [IMP] [35]
  ppGpp activation qorAp nd nd nd qorA nd nd [IEP] [2], [36]
  ppGpp inhibition queAp nd nd nd queA nd nd [2]
  ppGpp activation relAp2 Sigma70 nd nd relA, mazE, mazF nd nd [IMP] [37]
  ppGpp activation rmfp nd nd nd rmf nd nd [IEP] [38]
  ppGpp inhibition rpmEp Sigma32 nd nd rpmE nd nd [GEA] [2]
  ppGpp activation rpoEp2a Sigma70, Sigma24 nd nd rpoE, rseA, rseB, rseC nd nd [GEA] [39]
  ppGpp inhibition rpoSp Sigma70 nd nd rpoS nd nd [GEA] [40]
  ppGpp inhibition rpsBp Sigma70 nd nd tff, rpsB, tsf nd nd [GEA] [41]
  ppGpp inhibition rpsOp nd nd nd rpsO, pnp nd nd [GEA] [2]
  ppGpp inhibition rrsAp1 Sigma32, Sigma70 nd nd rrsA, ileT, alaT, rrlA, rrfA nd nd [IMP] [42]
  ppGpp inhibition rrsBp1 Sigma32, Sigma70 nd nd rrsB, gltT, rrlB, rrfB nd nd [IMP] [42]
  ppGpp inhibition rrsCp1 Sigma32, Sigma70 nd nd rrsC, gltU, rrlC, rrfC nd nd [IMP] [42]
  ppGpp inhibition rrsDp1 Sigma32, Sigma70 nd nd rrsD, ileU, alaU, rrlD, rrfD, thrV, rrfF nd nd [IMP] [42]
  ppGpp inhibition rrsEp Sigma32, Sigma70 nd nd rrsE, gltV, rrlE, rrfE nd nd [IMP] [42]
  ppGpp inhibition rrsGp1 Sigma32, Sigma70 nd nd rrsG, gltW, rrlG, rrfG nd nd [IMP] [42]
  ppGpp inhibition rrsHp1 Sigma32, Sigma70 nd nd rrsH, ileV, alaV, rrlH, rrfH nd nd [IMP] [42]
  ppGpp activation rseAp3 Sigma24 nd nd rseA, rseB, rseC nd nd [IEP] [16]
  ppGpp inhibition serWp2 Sigma70 nd nd serW nd nd [IHBCE] [43]
  ppGpp activation sgrRp Sigma70 nd nd sgrR, sroA, thiB, thiP, thiQ nd nd [GEA] [44]
  ppGpp activation sgrSp Sigma70, Sigma38 nd nd sgrS, sgrT, setA nd nd [GEA] [44]
  ppGpp inhibition speCp Sigma38 nd nd speC nd nd [GEA], [IMP] [45]
  ppGpp activation srap Sigma38 nd nd sra nd nd [GEA], [IEP] [2], [46]
  ppGpp inhibition thrUp Sigma70 nd nd thrU, tyrU, glyT, thrT, tufB nd nd [IEP], [IMP] [47]
  ppGpp activation trxAp1 Sigma70 nd nd trxA nd nd [IMP] [48]
  ppGpp activation trxAp2 Sigma70 nd nd trxA nd nd [IMP] [48]
  ppGpp inhibition tyrTp Sigma70 nd nd tyrT, tyrV, tpr nd nd [IEP] [49]
  ppGpp activation uspAp1 Sigma70 nd nd uspA nd nd [GEA] [13], [50]
  ppGpp activation uspBp Sigma38 nd nd uspB nd nd [GEA] [6]
  ppGpp activation uspEp nd nd nd uspE nd nd [IEP] [51]
  ppGpp activation yiiSp Sigma24 nd nd yiiS, uspD nd nd [IEP] [51]


Evolutionary conservation of regulatory elements    
     Note: Evolutionary conservation of regulatory interactions and promoters is limited to gammaproteobacteria.
Promoter-target gene evolutionary conservation


Evidence    

 [GEA] Gene expression analysis

 [IEP] Inferred from expression pattern

 [IDA] Inferred from direct assay

 [EME] Expression microarray evidence

 [IMP] Inferred from mutant phenotype

 [IHBCE] Inferred by a human based on computational evidence



Reference(s)    

 [1] Barker MM., Gaal T., Josaitis CA., Gourse RL., 2001, Mechanism of regulation of transcription initiation by ppGpp. I. Effects of ppGpp on transcription initiation in vivo and in vitro., J Mol Biol 305(4):673-88

 [2] Traxler MF., Summers SM., Nguyen HT., Zacharia VM., Hightower GA., Smith JT., Conway T., 2008, The global, ppGpp-mediated stringent response to amino acid starvation in Escherichia coli., Mol Microbiol 68(5):1128-48

 [3] Rowley KB., Elford RM., Roberts I., Holmes WM., 1993, In vivo regulatory responses of four Escherichia coli operons which encode leucyl-tRNAs., J Bacteriol 175(5):1309-15

 [4] Toulokhonov II., Shulgina I., Hernandez VJ., 2001, Binding of the transcription effector ppGpp to Escherichia coli RNA polymerase is allosteric, modular, and occurs near the N terminus of the beta'-subunit., J Biol Chem 276(2):1220-5

 [5] Lyzen R., Maitra A., Milewska K., Kochanowska-Lyzen M., Hernandez VJ., Szalewska-Palasz A., 2016, The dual role of DksA protein in the regulation of Escherichia coli pArgX promoter., Nucleic Acids Res 44(21):10316-10325

 [6] Kvint K., Farewell A., Nystrom T., 2000, RpoS-dependent promoters require guanosine tetraphosphate for induction even in the presence of high levels of sigma(s)., J Biol Chem 275(20):14795-8

 [7] Johansson J., Balsalobre C., Wang SY., Urbonaviciene J., Jin DJ., Sonden B., Uhlin BE., 2000, Nucleoid proteins stimulate stringently controlled bacterial promoters: a link between the cAMP-CRP and the (p)ppGpp regulons in Escherichia coli., Cell 102(4):475-85

 [8] Yamanaka K., Inouye M., 1997, Growth-phase-dependent expression of cspD, encoding a member of the CspA family in Escherichia coli., J Bacteriol 179(16):5126-30

 [9] Brandi A., Giangrossi M., Giuliodori AM., Falconi M., 2016, An Interplay among FIS, H-NS, and Guanosine Tetraphosphate Modulates Transcription of the Escherichia coli cspA Gene under Physiological Growth Conditions., Front Mol Biosci 3:19

 [10] Chandrangsu P., Lemke JJ., Gourse RL., 2011, The dksA promoter is negatively feedback regulated by DksA and ppGpp., Mol Microbiol 80(5):1337-48

 [11] Chiaramello AE., Zyskind JW., 1990, Coupling of DNA replication to growth rate in Escherichia coli: a possible role for guanosine tetraphosphate., J Bacteriol 172(4):2013-9

 [12] Mallik P., Paul BJ., Rutherford ST., Gourse RL., Osuna R., 2006, DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli., J Bacteriol 188(16):5775-82

 [13] Kvint K., Hosbond C., Farewell A., Nybroe O., Nystrom T., 2000, Emergency derepression: stringency allows RNA polymerase to override negative control by an active repressor., Mol Microbiol 35(2):435-43

 [14] Aberg A., Shingler V., Balsalobre C., 2008, Regulation of the fimB promoter: a case of differential regulation by ppGpp and DksA in vivo., Mol Microbiol 67(6):1223-41

 [15] Costanzo A., Ades SE., 2006, Growth phase-dependent regulation of the extracytoplasmic stress factor, sigmaE, by guanosine 3',5'-bispyrophosphate (ppGpp)., J Bacteriol 188(13):4627-34

 [16] Costanzo A., Nicoloff H., Barchinger SE., Banta AB., Gourse RL., Ades SE., 2008, ppGpp and DksA likely regulate the activity of the extracytoplasmic stress factor sigmaE in Escherichia coli by both direct and indirect mechanisms., Mol Microbiol 67(3):619-32

 [17] Diez A., Gustavsson N., Nystrom T., 2000, The universal stress protein A of Escherichia coli is required for resistance to DNA damaging agents and is regulated by a RecA/FtsK-dependent regulatory pathway., Mol Microbiol 36(6):1494-503

 [18] Vinella D., Bouloc P., D'Ari R., 1993, GTPase enters the ring., Curr Biol 3(1):65-6

 [19] Vinella D., Joseleau-Petit D., Thevenet D., Bouloc P., D'Ari R., 1993, Penicillin-binding protein 2 inactivation in Escherichia coli results in cell division inhibition, which is relieved by FtsZ overexpression., J Bacteriol 175(20):6704-10

 [20] Romeo T., Preiss J., 1989, Genetic regulation of glycogen biosynthesis in Escherichia coli: in vitro effects of cyclic AMP and guanosine 5'-diphosphate 3'-diphosphate and analysis of in vivo transcripts., J Bacteriol 171(5):2773-82

 [21] Klein RZ., Haddow JE., Faix JD., Brown RS., Hermos RJ., Pulkkinen A., Mitchell ML., 1991, Prevalence of thyroid deficiency in pregnant women., Clin Endocrinol (Oxf) 35(1):41-6

 [22] Membrillo-Hernandez J., Cook GM., Poole RK., 1997, Roles of RpoS (sigmaS), IHF and ppGpp in the expression of the hmp gene encoding the flavohemoglobin (Hmp) of Escherichia coli K-12., Mol Gen Genet 254(5):599-603

 [23] Baccigalupi L., Marasco R., Ricca E., De Felice M., Sacco M., 1995, Control of ilvIH transcription during amino acid downshift in stringent and relaxed strains of Escherichia coli., FEMS Microbiol Lett 131(1):95-8

 [24] Durfee T., Hansen AM., Zhi H., Blattner FR., Jin DJ., 2008, Transcription profiling of the stringent response in Escherichia coli., J Bacteriol 190(3):1084-96

 [25] Merrikh H., Ferrazzoli AE., Lovett ST., 2009, Growth phase and (p)ppGpp control of IraD, a regulator of RpoS stability, in Escherichia coli., J Bacteriol 191(24):7436-46

 [26] Bougdour A., Gottesman S., 2007, ppGpp regulation of RpoS degradation via anti-adaptor protein IraP., Proc Natl Acad Sci U S A 104(31):12896-901

 [27] Reimers JM., Schmidt KH., Longacre A., Reschke DK., Wright BE., 2004, Increased transcription rates correlate with increased reversion rates in leuB and argH Escherichia coli auxotrophs., Microbiology 150(Pt 5):1457-66

 [28] Fang M., Majumder A., Tsai KJ., Wu HY., 2000, ppGpp-dependent leuO expression in bacteria under stress., Biochem Biophys Res Commun 276(1):64-70

 [29] Landgraf JR., Wu J., Calvo JM., 1996, Effects of nutrition and growth rate on Lrp levels in Escherichia coli., J Bacteriol 178(23):6930-6

 [30] Aizenman E., Engelberg-Kulka H., Glaser G., 1996, An Escherichia coli chromosomal "addiction module" regulated by guanosine [corrected] 3',5'-bispyrophosphate: a model for programmed bacterial cell death., Proc Natl Acad Sci U S A 93(12):6059-63

 [31] Gross M., Marianovsky I., Glaser G., 2006, MazG - a regulator of programmed cell death in Escherichia coli., Mol Microbiol 59(2):590-601

 [32] Nagase T., Ishii S., Imamoto F., 1988, Differential transcriptional control of the two tRNA(fMet) genes of Escherichia coli K-12., Gene 67(1):49-57

 [33] Ogawa T., Okazaki T., 1991, Concurrent transcription from the gid and mioC promoters activates replication of an Escherichia coli minichromosome., Mol Gen Genet 230(1-2):193-200

 [34] Nadratowska-Wesolowska B., Slominska-Wojewodzka M., Lyzen R., Wegrzyn A., Szalewska-Palasz A., Wegrzyn G., 2010, Transcription regulation of the Escherichia coli pcnB gene coding for poly(A) polymerase I: roles of ppGpp, DksA and sigma factors., Mol Genet Genomics 284(4):289-305

 [35] Donahue JP., Turnbough CL., 1990, Characterization of transcriptional initiation from promoters P1 and P2 of the pyrBI operon of Escherichia coli K12., J Biol Chem 265(31):19091-9

 [36] Chang DE., Smalley DJ., Conway T., 2002, Gene expression profiling of Escherichia coli growth transitions: an expanded stringent response model., Mol Microbiol 45(2):289-306

 [37] Goodman C., 2012, Regulation: positively alarming., Nat Chem Biol 8(9):738

 [38] Izutsu K., Wada A., Wada C., 2001, Expression of ribosome modulation factor (RMF) in Escherichia coli requires ppGpp., Genes Cells 6(8):665-76

 [39] Gopalkrishnan S., Nicoloff H., Ades SE., 2014, Co-ordinated regulation of the extracytoplasmic stress factor, sigmaE, with other Escherichia coli sigma factors by (p)ppGpp and DksA may be achieved by specific regulation of individual holoenzymes., Mol Microbiol 93(3):479-93

 [40] Gentry DR., Hernandez VJ., Nguyen LH., Jensen DB., Cashel M., 1993, Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp., J Bacteriol 175(24):7982-9

 [41] Aseev LV., Koledinskaya LS., Boni IV., 2014, Dissecting the extended "-10" Escherichia coli rpsB promoter activity and regulation in vivo., Biochemistry (Mosc) 79(8):776-84

 [42] Paul BJ., Barker MM., Ross W., Schneider DA., Webb C., Foster JW., Gourse RL., 2004, DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP., Cell 118(3):311-22

 [43] Cummings HS., Sands JF., Fraser J., Hershey JW., 1994, Characterization and expression of a gene encoding serine tRNA5 from Escherichia coli., Biochimie 76(1):83-7

 [44] Kessler JR., Cobe BL., Richards GR., 2017, Stringent Response Regulators Contribute to Recovery from Glucose Phosphate Stress in Escherichia coli., Appl Environ Microbiol 83(24)

 [45] Holtta E., Janne J., Pispa J., 1974, The regulation of polyamine synthesis during the stringent control in Escherichia coli., Biochem Biophys Res Commun 59(3):1104-11

 [46] Izutsu K., Wada C., Komine Y., Sako T., Ueguchi C., Nakura S., Wada A., 2001, Escherichia coli ribosome-associated protein SRA, whose copy number increases during stationary phase., J Bacteriol 183(9):2765-73

 [47] Mizushima-Sugano J., Kaziro Y., 1985, Regulation of the expression of the tufB operon: DNA sequences directly involved in the stringent control., EMBO J 4(4):1053-8

 [48] Lim CJ., Daws T., Gerami-Nejad M., Fuchs JA., 2000, Growth-phase regulation of the Escherichia coli thioredoxin gene., Biochim Biophys Acta 1491(1-3):1-6

 [49] Travers AA., Lamond AI., Mace HA., Berman ML., 1983, RNA polymerase interactions with the upstream region of the E. coli tyrT promoter., Cell 35(1):265-73

 [50] Farewell A., Diez AA., DiRusso CC., Nystrom T., 1996, Role of the Escherichia coli FadR regulator in stasis survival and growth phase-dependent expression of the uspA, fad, and fab genes., J Bacteriol 178(22):6443-50

 [51] Gustavsson N., Diez A., Nystrom T., 2002, The universal stress protein paralogues of Escherichia coli are co-ordinately regulated and co-operate in the defence against DNA damage., Mol Microbiol 43(1):107-17



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