The forespore line of gene expression in Bacillus subtilis

Journal of Molecular Biology

Volumn 358, Issue 1, 2006, Pages 16-37

  Wang, Stephanie T ^a   Setlow, Barbara ^b   Conlon, Erin M ^c   Lyon, Jessica L ^d   Imamura, Daisuke ^e   Sato, Tsutomu ^e   Setlow, Peter ^b   Losick, Richard ^a   Eichenberger, Patrick ^a,d  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d NEW YORK UNIVERSITY   (United States)

^e TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

Forespore; Promoters; Sigma factor; Sporulation; Transcriptional profiling

Indexed keywords

DNA BINDING PROTEIN; SIGMA FACTOR;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL SPORE; GENE EXPRESSION; GENE INACTIVATION; GENOMICS; MORPHOGENESIS; PRIORITY JOURNAL; REGULON; SPOROGENESIS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); LISTERIA;

EID: 33645097172     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.01.059     Document Type: Article

References (87)

1. P.J. Piggot, and R. Losick Sporulation genes and inter-compartmental regulation A.L. Sonenshein J.A. Hoch R. Losick Bacillus subtilis and its Closest Relatives: From Genes to Cells 2002 American Society for Microbiology Washington, DC 483 518
2. D.W. Hilbert, and P.J. Piggot Compartmentalization of gene expression during Bacillus subtilis spore formation Microbiol. Mol. Biol. Rev. 68 2004 234 262
3. J.A. Hoch Regulation of the phosphorelay and the initiation of sporulation in Bacillus subtilis Annu. Rev. Microbiol. 47 1993 441 465
4. K. Stephenson, and J.A. Hoch Evolution of signalling in the sporulation phosphorelay Mol. Microbiol. 46 2002 297 304
5. M.A. Strauch, G.B. Spiegelman, M. Perego, W.C. Johnson, D. Burbulys, and J.A. Hoch The transition state transcription regulator abrB of Bacillus subtilis is a DNA binding protein EMBO J. 8 1989 1615 1621
6. M. Fujita, and Y. Sadaie Feedback loops involving Spo0A and AbrB in in vitro transcription of the genes involved in the initiation of sporulation in Bacillus subtilis J. Biochem. (Tokyo) 124 1998 98 104
7. M. Perego, G.B. Spiegelman, and J.A. Hoch Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis Mol. Microbiol. 2 1988 689 699
8. P. Zuber, and R. Losick Role of AbrB in Spo0A- and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis J. Bacteriol. 169 1987 2223 2230
9. V. Molle, M. Fujita, S.T. Jensen, P. Eichenberger, J.E. Gonzalez-Pastor, J.S. Liu, and R. Losick The Spo0A regulon of Bacillus subtilis Mol. Microbiol. 50 2003 1683 1701
10. M. Fujita, and R. Losick Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A Genes Dev. 19 2005 2236 2244
11. R. Losick, and P. Stragier Crisscross regulation of cell-type-specific gene expression during development in B. subtilis Nature 355 1992 601 604
12. P. Eichenberger, S.T. Jensen, E.M. Conlon, C. van Ooij, J. Silvaggi, and J.E. Gonzalez-Pastor The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis J. Mol. Biol. 327 2003 945 972
13. P. Eichenberger, M. Fujita, S.T. Jensen, E.M. Conlon, D.Z. Rudner, and S.T. Wang The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis PLoS Biol. 2 2004 e328
14. R. Milo, S. Shen-Orr, S. Itzkovitz, N. Kashtan, D. Chklovskii, and U. Alon Network motifs: simple building blocks of complex networks Science 298 2002 824 827
15. S.S. Shen-Orr, R. Milo, S. Mangan, and U. Alon Network motifs in the transcriptional regulation network of Escherichia coli Nature Genet. 31 2002 64 68
16. S. Mangan, and U. Alon Structure and function of the feed-forward loop network motif Proc. Natl Acad. Sci. USA 100 2003 11980 11985
17. L. Juan Wu, and J. Errington Identification and characterization of a new prespore-specific regulatory gene, rsfA, of Bacillus subtilis J. Bacteriol. 182 2000 418 424
18. J.A. Londono-Vallejo, and P. Stragier Cell-cell signaling pathway activating a developmental transcription factor in Bacillus subtilis Genes Dev. 9 1995 503 508
19. M.L. Karow, P. Glaser, and P.J. Piggot Identification of a gene, spoIIR, that links the activation of sigma E to the transcriptional activity of sigma F during sporulation in Bacillus subtilis Proc. Natl Acad. Sci. USA 92 1995 2012 2016
20. I. Bagyan, J. Hobot, and S. Cutting A compartmentalized regulator of developmental gene expression in Bacillus subtilis J. Bacteriol. 178 1996 4500 4507
21. L. Steil, M. Serrano, A.O. Henriques, and U. Volker Genome-wide analysis of temporally regulated and compartment-specific gene expression in sporulating cells of Bacillus subtilis Microbiology 151 2005 399 420
22. A. Cabrera-Hernandez, J.L. Sanchez-Salas, M. Paidhungat, and P. Setlow Regulation of four genes encoding small, acid-soluble spore proteins in Bacillus subtilis Gene 232 1999 1 10
23. S. Ben-Yehuda, M. Fujita, X.S. Liu, B. Gorbatyuk, D. Skoko, and J. Yan Defining a centromere-like element in Bacillus subtilis by Identifying the binding sites for the chromosome-anchoring protein RacA Mol. Cell 17 2005 773 782
24. D. Sun, P. Fajardo-Cavazos, M.D. Sussman, F. Tovar-Rojo, R.M. Cabrera-Martinez, and P. Setlow Effect of chromosome location of Bacillus subtilis forespore genes on their spo gene dependence and transcription by E sigma F: identification of features of good E sigma F-dependent promoters J. Bacteriol. 173 1991 7867 7874
25. D.X. Sun, R.M. Cabrera-Martinez, and P. Setlow Control of transcription of the Bacillus subtilis spoIIIG gene, which codes for the forespore-specific transcription factor sigma G J. Bacteriol. 173 1991 2977 2984
26. E. Kruger, D. Zuhlke, E. Witt, H. Ludwig, and M. Hecker Clp-mediated proteolysis in Gram-positive bacteria is autoregulated by the stability of a repressor EMBO J. 20 2001 852 863
27. Y.L. Sun, M.D. Sharp, and K. Pogliano A dispensable role for forespore-specific gene expression in engulfment of the forespore during sporulation of Bacillus subtilis J. Bacteriol. 182 2000 2919 2927
28. T. Doan, K.A. Marquis, and D.Z. Rudner Subcellular localization of a sporulation membrane protein is achieved through a network of interactions along and across the septum Mol. Microbiol. 55 2005 1767 1781
29. B. Blaylock, X. Jiang, A. Rubio, C.P. Moran Jr, and K. Pogliano Zipper-like interaction between proteins in adjacent daughter cells mediates protein localization Genes Dev. 18 2004 2916 2928
30. J.A. Londono-Vallejo, C. Frehel, and P. Stragier SpoIIQ, a forespore-expressed gene required for engulfment in Bacillus subtilis Mol. Microbiol. 24 1997 29 39
31. I. Bagyan, L. Casillas-Martinez, and P. Setlow The katX gene, which codes for the catalase in spores of Bacillus subtilis, is a forespore-specific gene controlled by sigmaF, and KatX is essential for hydrogen peroxide resistance of the germinating spore J. Bacteriol. 180 1998 2057 2062
32. R. Schuch, and P.J. Piggot The dacF-spoIIA operon of Bacillus subtilis, encoding sigma F, is autoregulated J. Bacteriol. 176 1994 4104 4110
33. L.B. Pedersen, K. Ragkousi, T.J. Cammett, E. Melly, A. Sekowska, and E. Schopick Characterization of ywhE, which encodes a putative high-molecular- weight class A penicillin-binding protein in Bacillus subtilis Gene 246 2000 187 196
34. I.M. Feavers, J. Foulkes, B. Setlow, D. Sun, W. Nicholson, P. Setlow, and A. Moir The regulation of transcription of the gerA spore germination operon of Bacillus subtilis Mol. Microbiol. 4 1990 275 282
35. M.D. Sussman, and P. Setlow Cloning, nucleotide sequence, and regulation of the Bacillus subtilis gpr gene, which codes for the protease that initiates degradation of small, acid-soluble proteins during spore germination J. Bacteriol. 173 1991 291 300
36. J.L. Sanchez-Salas, and P. Setlow Proteolytic processing of the protease which initiates degradation of small, acid-soluble proteins during germination of Bacillus subtilis spores J. Bacteriol. 175 1993 2568 2577
37. T. Sato, and Y. Kobayashi The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite J. Bacteriol. 180 1998 1655 1661
38. P. Stragier, B. Kunkel, L. Kroos, and R. Losick Chromosomal rearrangement generating a composite gene for a developmental transcription factor Science 243 1989 507 512
39. M. Pedraza-Reyes, F. Gutierrez-Corona, and W.L. Nicholson Temporal regulation and forespore-specific expression of the spore photoproduct lyase gene by sigma-G RNA polymerase during Bacillus subtilis sporulation J. Bacteriol. 176 1994 3983 3991
40. Q. Pan, R. Losick, and D.Z. Rudner A second PDZ-containing serine protease contributes to activation of the sporulation transcription factor sigmaK in Bacillus subtilis J. Bacteriol. 185 2003 6051 6056
41. J. Sekiguchi, K. Akeo, H. Yamamoto, F.K. Khasanov, J.C. Alonso, and A. Kuroda Nucleotide sequence and regulation of a new putative cell wall hydrolase gene, cwlD, which affects germination in Bacillus subtilis J. Bacteriol. 177 1995 5582 5589
42. T. Fukushima, T. Kitajima, and J. Sekiguchi A polysaccharide deacetylase homologue, PdaA, in Bacillus subtilis acts as an N-acetylmuramic acid deacetylase in vitro J. Bacteriol. 187 2005 1287 1292
43. T. Fukushima, H. Yamamoto, A. Atrih, S.J. Foster, and J. Sekiguchi A polysaccharide deacetylase gene (pdaA) is required for germination and for production of muramic delta-lactam residues in the spore cortex of Bacillus subtilis J. Bacteriol. 184 2002 6007 6015
44. H. Takamatsu, T. Hiraoka, T. Kodama, H. Koide, S. Kozuka, K. Tochikubo, and K. Watabe Cloning of a novel gene yrbB, encoding a protein located in the spore integument of Bacillus subtilis FEMS Microbiol. Letters 166 1998 361 367
45. R. Moriyama, H. Fukuoka, S. Miyata, S. Kudoh, A. Hattori, and S. Kozuka Expression of a germination-specific amidase, SleB, of Bacilli in the forespore compartment of sporulating cells and its localization on the exterior side of the cortex in dormant spores J. Bacteriol. 181 1999 2373 2378
46. F. Tovar-Rojo, M. Chander, B. Setlow, and P. Setlow The products of the spoVA operon are involved in dipicolinic acid uptake into developing spores of Bacillus subtilis J. Bacteriol. 184 2002 584 587
47. B.M. Corfe, A. Moir, D. Popham, and P. Setlow Analysis of the expression and regulation of the gerB spore germination operon of Bacillus subtilis 168 Microbiology 140 1994 3079 3083
48. E.H. Kemp, R.L. Sammons, A. Moir, D. Sun, and P. Setlow Analysis of transcriptional control of the gerD spore germination gene of Bacillus subtilis 168 J. Bacteriol. 173 1991 4646 4652
49. M. Paidhungat, and P. Setlow Role of ger proteins in nutrient and nonnutrient triggering of spore germination in Bacillus subtilis J. Bacteriol. 182 2000 2513 2519
50. G. Lorca, B. Winnen, and M.H. Saier Jr Identification of the l-aspartate transporter in Bacillus subtilis J. Bacteriol. 185 2003 3218 3222
51. J.M. Silvaggi, D.L. Popham, A. Driks, P. Eichenberger, and R. Losick Unmasking novel sporulation genes in Bacillus subtilis J. Bacteriol. 186 2004 80898095
52. P. Stragier A gene odyssey: exploring the genomes of endospore-forming bacteria A.L. Sonenshein J.A. Hoch R. Losick Bacillus subtilis and its Closest Relatives: From Genes to Cells 2002 American Society for Microbiology Washington, DC 519 526
53. G.R. Weller, B. Kysela, R. Roy, L.M. Tonkin, E. Scanlan, and M. Della Identification of a DNA nonhomologous end-joining complex in bacteria Science 297 2002 1686 1689
54. B. Setlow, and P. Setlow Small, acid-soluble proteins bound to DNA protect Bacillus subtilis spores from killing by dry heat Appl. Environ. Microbiol. 61 1995 2787 2790
55. H. Fairhead, B. Setlow, and P. Setlow Prevention of DNA damage in spores and in vitro by small, acid-soluble proteins from Bacillus species J. Bacteriol. 175 1993 1367 1374
56. P. Setlow Mechanisms for the prevention of damage to DNA in spores of Bacillus species Annu. Rev. Microbiol. 49 1995 29 54
57. B. Setlow, and P. Setlow Binding of small, acid-soluble spore proteins to DNA plays a significant role in the resistance of Bacillus subtilis spores to hydrogen peroxide Appl. Environ. Microbiol. 59 1993 3418 3423
58. D. Frenkiel-Krispin, R. Sack, J. Englander, E. Shimoni, M. Eisenstein, and E. Bullitt Structure of the DNA-SspC complex: implications for DNA packaging, protection, and repair in bacterial spores J. Bacteriol. 186 2004 3525 3530
59. P. Fawcett, P. Eichenberger, R. Losick, and P. Youngman The transcriptional profile of early to middle sporulation in Bacillus subtilis Proc. Natl Acad. Sci. USA 97 2000 8063 8068
60. M. Fujita, J.E. Gonzalez-Pastor, and R. Losick High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis J. Bacteriol. 187 2005 135713 135768
61. R.A. Britton, P. Eichenberger, J.E. Gonzalez-Pastor, P. Fawcett, R. Monson, R. Losick, and A.D. Grossman Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis J. Bacteriol. 184 2002 4881 4890
62. M.A. Hamon, N.R. Stanley, R.A. Britton, A.D. Grossman, and B.A. Lazazzera Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis Mol. Microbiol. 52 2004 847 860
63. D.B. Kearns, F. Chu, S.S. Branda, R. Kolter, and R. Losick A master regulator for biofilm formation by Bacillus subtilis Mol. Microbiol. 55 2005 739 749
64. M. Fujita, and R. Losick The master regulator for entry into sporulation in Bacillus subtilis becomes a cell-specific transcription factor after asymmetric division Genes Dev. 17 2003 1166 1174
65. W.G. Murrell, and A.D. Warth Composition and heat resistance of bacterial spores L.L. Campbell H.O. Halvorson Spores III 1965 American Society for Microbiology Washington, DC 1 24
66. W.L. Nicholson, D.X. Sun, B. Setlow, and P. Setlow Promoter specificity of sigma G-containing RNA polymerase from sporulating cells of Bacillus subtilis: identification of a group of forespore-specific promoters J. Bacteriol. 171 1989 2708 2718
67. A. Abanes-De Mello, Y.L. Sun, S. Aung, and K. Pogliano A cytoskeleton-like role for the bacterial cell wall during engulfment of the Bacillus subtilis forespore Genes Dev. 16 2002 3253 3264
68. H. Kim, M. Hahn, P. Grabowski, D.C. McPherson, M.M. Otte, and R. Wang The Bacillus subtilis spore coat protein interaction network Mol. Microbiol. 59 2006 487 502
69. E.B. Simpson, T.W. Hancock, and C.E. Buchanan Transcriptional control of dacB, which encodes a major sporulation-specific penicillin-binding protein J. Bacteriol. 176 1994 7767 7769
70. M.E. Gilmore, D. Bandyopadhyay, A.M. Dean, S.D. Linnstaedt, and D.L. Popham Production of muramic delta-lactam in Bacillus subtilis spore peptidoglycan J. Bacteriol. 186 2004 80 89
71. D. Imamura, K. Kobayashi, J. Sekiguchi, N. Ogasawara, M. Takeuchi, and T. Sato spoIVH (ykvV), a requisite cortex formation gene, is expressed in both sporulating compartments of Bacillus subtilis J. Bacteriol. 186 2004 5450 5459
72. J. Dworkin, and R. Losick Developmental commitment in a bacterium Cell 121 2005 401 409
73. C. Karmazyn-Campelli, C. Bonamy, B. Savelli, and P. Stragier Tandem genes encoding sigma-factors for consecutive steps of development in Bacillus subtilis Genes Dev. 3 1989 150 157
74. A. Wach PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae Yeast 12 1996 259 265
75. R.L. Vellanoweth, and J.C. Rabinowitz The influence of ribosome-binding-site elements on translational efficiency in Bacillus subtilis and Escherichia coli in vivo Mol. Microbiol. 6 1992 1105 1114
76. C. van Ooij, P. Eichenberger, and R. Losick Dynamic patterns of subcellular protein localization during spore coat morphogenesis in Bacillus subtilis J. Bacteriol. 186 2004 4441 4448
77. J.M. Sterlini, and J. Mandelstam Commitment to sporulation in Bacillus subtilis and its relationship to development of actinomycin resistance Biochem. J. 113 1969 29 37
78. C.R. Harwood, and S.M. Cutting Molecular Biological Methods for Bacillus 1990 Wiley ChiChester,United Kingdom
79. G.C. Tseng, M.K. Oh, L. Rohlin, J.C. Liao, and W.H. Wong Issues in cDNA microarray analysis: quality filtering, channel normalization, models of variations and assessment of gene effects Nucl. Acids Res. 29 2001 2549 2557
80. X. Liu, D.L. Brutlag, and J.S. Liu BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes Pac. Symp. Biocomput. 6 2001 127 138
81. S.T. Jensen, and J.S. Liu BioOptimizer: a Bayesian scoring function approach to motif discovery Bioinformatics 20 2004 1557 1564
82. M.A. Frohman On beyond classic RACE (rapid amplification of cDNA ends) PCR Methods Appl. 4 1994 S40 S58
83. C.W. Price, P. Fawcett, H. Ceremonie, N. Su, C.K. Murphy, and P. Youngman Genome-wide analysis of the general stress response in Bacillus subtilis Mol. Microbiol. 41 2001 757 774
84. A. Driks, S. Roels, B. Beall, C.P. Moran Jr, and R. Losick Subcellular localization of proteins involved in the assembly of the spore coat of Bacillus subtilis Genes Dev. 8 1994 234 244
85. J.M. Mason, and P. Setlow Essential role of small, acid-soluble spore proteins in resistance of Bacillus subtilis spores to UV light J. Bacteriol. 167 1986 174 178
86. T.D. Schneider, and R.M. Stephens Sequence logos: a new way to display consensus sequences Nucl. Acids Res. 18 1990 6097 6100
87. M. Paidhungat, B. Setlow, A. Driks, and P. Setlow Characterization of spores of Bacillus subtilis which lack dipicolinic acid J. Bacteriol. 182 2000 5505 5512