全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS Biology  2004 

The Program of Gene Transcription for a Single Differentiating Cell Type during Sporulation in Bacillus subtilis

DOI: 10.1371/journal.pbio.0020328

Full-Text   Cite this paper   Add to My Lib

Abstract:

Asymmetric division during sporulation by Bacillus subtilis generates a mother cell that undergoes a 5-h program of differentiation. The program is governed by a hierarchical cascade consisting of the transcription factors: σE, σK, GerE, GerR, and SpoIIID. The program consists of the activation and repression of 383 genes. The σE factor turns on 262 genes, including those for GerR and SpoIIID. These DNA-binding proteins downregulate almost half of the genes in the σE regulon. In addition, SpoIIID turns on ten genes, including genes involved in the appearance of σK. Next, σK activates 75 additional genes, including that for GerE. This DNA-binding protein, in turn, represses half of the genes that had been activated by σK while switching on a final set of 36 genes. Evidence is presented that repression and activation contribute to proper morphogenesis. The program of gene expression is driven forward by its hierarchical organization and by the repressive effects of the DNA-binding proteins. The logic of the program is that of a linked series of feed-forward loops, which generate successive pulses of gene transcription. Similar regulatory circuits could be a common feature of other systems of cellular differentiation.

References

[1]  Baldus JM, Green BD, Youngman P, Moran CP (1994) Phosphorylation of transcription factor Spo0A stimulates transcription from the spoIIG promoter by enhancing binding to weak 0A boxes. J Bacteriol 176: 296–306.
[2]  Ben-Yehuda S, Rudner DZ, Losick R (2003) RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299: 532–536.
[3]  Bonsen PP, Spudich JA, Nelson DL, Kornberg A (1969) Biochemical studies of bacterial sporulation and germination. XII. A sulfonic acid as a major sulfur compound of spores. J Bacteriol 98: 62–68.
[4]  Britton RA, Eichenberger P, Gonzalez-Pastor JE, Fawcett P, Monson R, et al. (2002) Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of . J Bacteriol 184: 4881–4890.
[5]  Brown PO, Botstein D (1999) Exploring the new world of the genome with DNA microarrays. Nat Genet 21: (Suppl 1)33–37.
[6]  Chada VG, Sanstad EA, Wang R, Driks A (2003) Morphogenesis of Bacillus spore surfaces. J Bacteriol 185: 6255–6261.
[7]  Conlon EM, Eichenberger P, Liu JS (2004) Determining and analyzing differentially expressed genes from cDNA microarray experiments with complementary designs. J Multivariate Anal 90: 1–18.
[8]  Cutting S, Mandelstam J (1986) The nucleotide sequence and the transcription during sporulation of the gerE gene of . J Gen Microbiol 132: 3013–3024.
[9]  Cutting S, Panzer S, Losick R (1989) Regulatory studies on the promoter for a gene governing synthesis and assembly of the spore coat in . J Mol Biol 207: 393–404.
[10]  Cutting S, Oke V, Driks A, Losick R, Lu S, et al. (1990) A forespore checkpoint for mother cell gene expression during development in . Cell 62: 239–250.
[11]  Cutting S, Driks A, Schmidt R, Kunkel B, Losick R (1991a) Forespore-specific transcription of a gene in the signal transduction pathway that governs Pro-sigma K processing in . Genes Dev 5: 456–466.
[12]  Cutting S, Roels S, Losick R (1991b) Sporulation operon spoIVF and the characterization of mutations that uncouple mother-cell from forespore gene expression in . J Mol Biol 221: 1237–1256.
[13]  Cutting S, Zheng LB, Losick R (1991c) Gene encoding two alkali-soluble components of the spore coat from . J Bacteriol 173: 2915–2919.
[14]  Driks A (2002) Proteins of the spore coat and coat. In: Sonenshein AL, Hoch JA, Losick R, editors. Bacillus subtilis and its closest relatives: From genes to cells. Washington (DC): American Society for Microbiology. pp. 527–536.
[15]  Driks A, Roels S, Beall B, Moran CP, Losick R (1994) Subcellular localization of proteins involved in the assembly of the spore coat of . Genes Dev 8: 234–244.
[16]  Eichenberger P, Fawcett P, Losick R (2001) A three-protein inhibitor of polar septation during sporulation in . Mol Microbiol 42: 1147–1162.
[17]  Eichenberger P, Jensen ST, Conlon EM, van Ooij C, Silvaggi J, et al. (2003) The sigmaE regulon and the identification of additional sporulation genes in . J Mol Biol 327: 945–972.
[18]  Errington J (2003) Regulation of endospore formation in . Nat Rev Microbiol 1: 117–126.
[19]  Fawcett P, Eichenberger P, Losick R, Youngman P (2000) The transcriptional profile of early to middle sporulation in . Proc Natl Acad Sci U S A 97: 8063–8068.
[20]  Feucht A, Evans L, Errington J (2003) Identification of sporulation genes by genome-wide analysis of the sigmaE regulon of . Microbiology 149: 3023–3034.
[21]  Foulger D, Errington J (1991) Sequential activation of dual promoters by different sigma factors maintains spoVJ expression during successive developmental stages of . Mol Microbiol 5: 1363–1373.
[22]  Frandsen N, Stragier P (1995) Identification and characterization of the Bacillus subtilis spoIIP locus. J Bacteriol 177: 716–722.
[23]  Frohman MA (1994) On beyond classic RACE (rapid amplification of cDNA ends). PCR Methods Appl 4: S40–S58.
[24]  Fujita M, Losick R (2002) An investigation into the compartmentalization of the sporulation transcription factor sigmaE in . Mol Microbiol 43: 27–38.
[25]  Fujita M, Losick R (2003) The master regulator for entry into sporulation in becomes a cell-specific transcription factor after asymmetric division. Genes Dev 17: 1166–1174.
[26]  Fujita M, Sadaie Y (1998) Promoter selectivity of the RNA polymerase sigmaA and sigmaH holoenzymes. J Biochem (Tokyo) 124: 89–97.
[27]  Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, et al. (2001) Comparative genomics of Listeria species. Science 294: 849–852.
[28]  Graham DE, Xu H, White RH (2002) Identification of coenzyme M biosynthetic phosphosulfolactate synthase: A new family of sulfonate-biosynthesizing enzymes. J Biol Chem 277: 13421–13429.
[29]  Grundy FJ, Henkin TM (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: 737–749.
[30]  Guerout-Fleury AM, Frandsen N, Stragier P (1996) Plasmids for ectopic integration in . Gene 180: 57–61.
[31]  Halberg R, Kroos L (1994) Sporulation regulatory protein SpoIIID from activates and represses transcription by both mother-cell-specific forms of RNA polymerase. J Mol Biol 243: 425–436.
[32]  Harwood CR, Cutting SM (1990) Molecular biological methods for Bacillus. Chichester (United Kingdom): Wiley. 581 p.
[33]  Helmann JD, Moran CP (2002) RNA polymerase and sigma factors. In: Sonenshein AL, Hoch JA, Losick R, editors. Bacillus subtilis and its closest relatives: From genes to cells. Washington (DC): American Society for Microbiology. pp. 289–312.
[34]  Hofmeister AE, Londono-Vallejo A, Harry E, Stragier P, Losick R (1995) Extracellular signal protein triggering the proteolytic activation of a developmental transcription factor in . Cell 83: 219–226.
[35]  Illing N, Errington J (1991) The spoIIIA operon of defines a new temporal class of mother-cell-specific sporulation genes under the control of the sigma E form of RNA polymerase. Mol Microbiol 5: 1927–1940.
[36]  Itaya M, Kondo K, Tanaka T (1989) A neomycin resistance gene cassette selectable in a single copy state in the chromosome. Nucleic Acids Res 17: 4410.
[37]  Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B, et al. (2003) Genome sequence of and comparative analysis with . Nature 423: 87–91.
[38]  Jensen ST, Liu JS (2004) BioOptimizer: A Bayesian scoring function approach to motif discovery. Bioinformatics 20: 1557–1564.
[39]  Jensen ST, Liu XS, Zhou Q, Liu JS (2004) Computational discovery of gene regulatory binding motifs: A Bayesian perspective. Stat Sci 19: 188–204.
[40]  Karmazyn-Campelli C, Bonamy C, Savelli B, Stragier P (1989) Tandem genes encoding sigma-factors for consecutive steps of development in . Genes Dev 3: 150–157.
[41]  Karow ML, Glaser P, Piggot PJ (1995) Identification of a gene, spoIIR that links the activation of sigma E to the transcriptional activity of sigma F during sporulation in . Proc Natl Acad Sci U S A 92: 2012–2016.
[42]  Kroos L, Kunkel B, Losick R (1989) Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor. Science 243: 526–529.
[43]  Kunkel B, Kroos L, Poth H, Youngman P, Losick R (1989) Temporal and spatial control of the mother-cell regulatory gene spoIIID of . Genes Dev 3: 1735–1744.
[44]  Kunkel B, Losick R, Stragier P (1990) The gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. Genes Dev 4: 525–535.
[45]  Kuroda A, Asami Y, Sekiguchi J (1993) Molecular cloning of a sporulation-specific cell wall hydrolase gene of . J Bacteriol 175: 6260–6268.
[46]  Kuwana R, Kasahara Y, Fujibayashi M, Takamatsu H, Ogasawara N, et al. (2002) Proteomics characterization of novel spore proteins of . Microbiology 148: 3971–3982.
[47]  Kuwana R, Yamamura S, Ikejiri H, Kobayashi K, Ogasawara N, et al. (2003) Bacillus subtilis spoVIF (yjcC) gene, involved in coat assembly and spore resistance. Microbiology 149: 3011–3021.
[48]  LaBell TL, Trempy JE, Haldenwang WG (1987) Sporulation-specific sigma factor sigma 29 of is synthesized from a precursor protein, P31. Proc Natl Acad Sci U S A 84: 1784–1788.
[49]  Lai EM, Phadke ND, Kachman MT, Giorno R, Vazquez S, et al. (2003) Proteomic analysis of the spore coats of and . J Bacteriol 185: 1443–1454.
[50]  Li Z, Piggot PJ (2001) Development of a two-part transcription probe to determine the completeness of temporal and spatial compartmentalization of gene expression during bacterial development. Proc Natl Acad Sci U S A 98: 12538–12543.
[51]  Liu X, Brutlag DL, Liu JS (2001) BioProspector: Discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes. Pac Symp Biocomput 6: 127–138.
[52]  Liu XS, Brutlag DL, Liu JS (2002) An algorithm for finding protein–DNA binding sites with applications to chromatin-immunoprecipitation microarray experiments. Nat Biotechnol 20: 835–839.
[53]  Londono-Vallejo JA, Stragier P (1995) Cell–cell signaling pathway activating a developmental transcription factor in . Genes Dev 9: 503–508.
[54]  Lopez-Diaz I, Clarke S, Mandelstam J (1986) spoIID operon of : Cloning and sequence. J Gen Microbiol 132: 341–354.
[55]  Lu S, Kroos L (1994) Overproducing the mother cell sigma factor precursor, Pro-sigma K, uncouples sigma K-dependent gene expression from dependence on intercompartmental communication. J Bacteriol 176: 3936–3943.
[56]  Lu S, Halberg R, Kroos L (1990) Processing of the mother-cell sigma factor, sigma K, may depend on events occurring in the forespore during development. Proc Natl Acad Sci U S A 87: 9722–9726.
[57]  Mangan S, Alon U (2003) Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci U S A 100: 11980–11985.
[58]  Mangan S, Zaslaver A, Alon U (2003) The coherent feedforward loop serves as a sign-sensitive delay element in transcription networks. J Mol Biol 334: 197–204.
[59]  Mekjian KR, Bryan EM, Beall BW, Moran CP (1999) Regulation of hexuronate utilization in . J Bacteriol 181: 426–433.
[60]  Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor (New York): Cold Spring Harbor Laboratory Press. 466 p.
[61]  Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, et al. (2002) Network motifs: Simple building blocks of complex networks. Science 298: 824–827.
[62]  Molle V, Fujita M, Jensen ST, Eichenberger P, Gonzalez-Pastor JE, et al. (2003a) The Spo0A regulon of . Mol Microbiol 50: 1683–1701.
[63]  Molle V, Nakaura Y, Shivers RP, Yamaguchi H, Losick R, et al. (2003b) Additional targets of the global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol 185: 1911–1922.
[64]  Moqtaderi Z, Struhl K (2004) Genome-wide occupancy profile of the RNA polymerase III machinery in reveals loci with incomplete transcription complexes. Mol Cell Biol 24: 4118–4127.
[65]  Nicholson WL, Setlow P (1990) Sporulation, germination and outgrowth. In: Harwood CR, Cutting SM, editors. Molecular biological methods for Bacillus. Chichester (United Kingdom): Wiley. pp. 391–450.
[66]  Nolling J, Breton G, Omelchenko MV, Makarova KS, Zeng Q, et al. (2001) Genome sequence and comparative analysis of the solvent-producing bacterium . J Bacteriol 183: 4823–4838.
[67]  Nugroho FA, Yamamoto H, Kobayashi Y, Sekiguchi J (1999) Characterization of a new sigma-K-dependent peptidoglycan hydrolase gene that plays a role in mother cell lysis. J Bacteriol 181: 6230–6237.
[68]  Pan Q, Losick R, Rudner DZ (2003) A second PDZ-containing serine protease contributes to activation of the sporulation transcription factor sigmaK in . J Bacteriol 185: 6051–6056.
[69]  Piggot PJ, Coote JG (1976) Genetic aspects of bacterial endospore formation. Bacteriol Rev 40: 908–962.
[70]  Piggot PJ, Losick R (2002) Sporulation genes and intercompartmental regulation. In: Sonenshein AL, Hoch JA, Losick R, editors. Bacillus subtilis and its closest relatives: From genes to cells. Washington (DC): American Society for Microbiology. pp. 483–518.
[71]  Price CW, Fawcett P, Ceremonie H, Su N, Murphy CK, et al. (2001) Genome-wide analysis of the general stress response in . Mol Microbiol 41: 757–774.
[72]  Price KD, Losick R (1999) A four-dimensional view of assembly of a morphogenetic protein during sporulation in . J Bacteriol 181: 781–790.
[73]  Read TD, Peterson SN, Tourasse N, Baillie LW, Paulsen IT, et al. (2003) The genome sequence of Ames and comparison to closely related bacteria. Nature 423: 81–86.
[74]  Resnekov O, Alper S, Losick R (1996) Subcellular localization of proteins governing the proteolytic activation of a developmental transcription factor in . Genes Cells 1: 529–542.
[75]  Ricca E, Cutting S, Losick R (1992) Characterization of bofA a gene involved in intercompartmental regulation of pro-sigma K processing during sporulation in . J Bacteriol 174: 3177–3184.
[76]  Roels S, Driks A, Losick R (1992) Characterization of spoIVA a sporulation gene involved in coat morphogenesis in . J Bacteriol 174: 575–585.
[77]  Rudner DZ, Losick R (2002) A sporulation membrane protein tethers the pro-sigmaK processing enzyme to its inhibitor and dictates its subcellular localization. Genes Dev 16: 1007–1018.
[78]  Rudner DZ, Pan Q, Losick RM (2002) Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. Proc Natl Acad Sci U S A 99: 8701–8706.
[79]  Satola SW, Baldus JM, Moran CP (1992) Binding of Spo0A stimulates spoIIG promoter activity in . J Bacteriol 174: 1448–1453.
[80]  Schneider TD, Stephens RM (1990) Sequence logos: A new way to display consensus sequences. Nucleic Acids Res 18: 6097–6100.
[81]  Setlow P (2003) Spore germination. Curr Opin Microbiol 6: 550–556.
[82]  Shen-Orr SS, Milo R, Mangan S, Alon U (2002) Network motifs in the transcriptional regulation network of . Nat Genet 31: 64–68.
[83]  Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, et al. (2002) Complete genome sequence of Clostridium perfringens an anaerobic flesh-eater. Proc Natl Acad Sci U S A 99: 996–1001.
[84]  Smith K, Youngman P (1993) Evidence that the spoIIM gene of is transcribed by RNA polymerase associated with sigma E. J Bacteriol 175: 3618–3627.
[85]  Smith K, Bayer ME, Youngman P (1993) Physical and functional characterization of the Bacillus subtilis spoIIM gene. J Bacteriol 175: 3607–3617.
[86]  Smith MC, Czaplewski L, North AK, Baumberg S, Stockley PG (1989) Sequences required for regulation of arginine biosynthesis promoters are conserved between and . Mol Microbiol 3: 23–28.
[87]  Smith TJ, Foster SJ (1995) Characterization of the involvement of two compensatory autolysins in mother cell lysis during sporulation of 168. J Bacteriol 177: 3855–3862.
[88]  Sterlini JM, Mandelstam J (1969) Commitment to sporulation in and its relationship to development of actinomycin resistance. Biochem J 113: 29–37.
[89]  Stevens CM, Errington J (1990) Differential gene expression during sporulation in Bacillus subtilis Structure and regulation of the spoIIID gene. Mol Microbiol 4: 543–551.
[90]  Stevens CM, Daniel R, Illing N, Errington J (1992) Characterization of a sporulation gene, spoIVA involved in spore coat morphogenesis in . J Bacteriol 174: 586–594.
[91]  Stragier P (2002) A gene odyssey: Exploring the genomes of endospore-forming bacteria. In: Sonenshein AL, Hoch JA, Losick R, editors. Bacillus subtilis and its closest relatives: From genes to cells. Washington (DC): American Society for Microbiology. pp. 519–526.
[92]  Stragier P, Losick R (1996) Molecular genetics of sporulation in . Annu Rev Genet 30: 297–241.
[93]  Stragier P, Bonamy C, Karmazyn-Campelli C (1988) Processing of a sporulation sigma factor in : How morphological structure could control gene expression. Cell 52: 697–704.
[94]  Stragier P, Kunkel B, Kroos L, Losick R (1989) Chromosomal rearrangement generating a composite gene for a developmental transcription factor. Science 243: 507–512.
[95]  Takamatsu H, Watabe K (2002) Assembly and genetics of spore protective structures. Cell Mol Life Sci 59: 434–444.
[96]  Takami H, Takaki Y, Uchiyama I (2002) Genome sequence of isolated from the Iheya Ridge and its unexpected adaptive capabilities to extreme environments. Nucleic Acids Res 30: 3927–3935.
[97]  Takami H, Nakasone K, Takaki Y, Maeno G, Sasaki R, et al. (2000) Complete genome sequence of the alkaliphilic bacterium and genomic sequence comparison with . Nucleic Acids Res 28: 4317–4331.
[98]  Tatti KM, Jones CH, Moran CP (1991) Genetic evidence for interaction of sigma E with the spoIIID promoter in . J Bacteriol 173: 7828–7833.
[99]  Tatti KM, Shuler MF, Moran CP (1995) Sequence-specific interactions between promoter DNA and the RNA polymerase sigma factor E. J Mol Biol 253: 8–16.
[100]  van Ooij C, Eichenberger P, Losick R (2004) Dynamic patterns of subcellular protein localization during spore coat morphogenesis in . J Bacteriol 186: 4441–4448.
[101]  Wach A (1996) PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in . Yeast 12: 259–265.
[102]  Wu LJ, Errington J (2000) Identification and characterization of a new prespore-specific regulatory gene, rsfA of . J Bacteriol 182: 418–424.
[103]  Yoshida K, Fujita Y, Ehrlich SD (1999) Three asparagine synthetase genes of . J Bacteriol 181: 6081–6091.
[104]  Zhang B, Daniel RA, Errington J, Kroos L (1997) SpoIIID protein binds to two sites in the spoVD promoter and represses transcription by sigmaE RNA polymerase. J Bacteriol 179: 972–975.
[105]  Zheng L, Halberg R, Roels S, Ichikawa H, Kroos L, et al. (1992) Sporulation regulatory protein GerE from binds to and can activate or repress transcription from promoters for mother-cell-specific genes. J Mol Biol 226: 1037–1050.
[106]  Zheng LB, Losick R (1990) Cascade regulation of spore coat gene expression in . J Mol Biol 212: 645–660.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133