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Science 27 January 1989:
Vol. 243. no. 4890, pp. 507 - 512
DOI: 10.1126/science.2536191
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Articles

Science, Vol 243, Issue 4890, 507-512
Copyright © 1989 by American Association for the Advancement of Science

articles

Chromosomal rearrangement generating a composite gene for a developmental transcription factor

P Stragier, B Kunkel, L Kroos, and R Losick

Department of Cellular and Developmental Biology, Harvard University, Cambridge, MA 02138.

Differential gene expression in the mother cell chamber of sporulating cells of Bacillus subtilis is determined in part by an RNA polymerase sigma factor called sigma K (or sigma 27). The sigma K factor was assigned as the product of the sporulation gene spoIVCB on the basis of the partial aminoterminal amino acid sequence of the purified protein. The spoIVCB gene is now shown to be a truncated gene capable of specifying only the amino terminal half of sigma K. The carboxyl terminal half is specified by another sporulation gene, spoIIIC, to which spoIVCB becomes joined inframe at an intermediate stage of sporulation by site-specific recombination within a 5-base pair repeated sequence. Juxtaposition of spoIVCB and spoIIIC need not be reversible in that the mother cell and its chromosome are discarded at the end of the developmental cycle. The rearrangement of chromosomal DNA could account for the presence of sigma K selectively in the mother cell and may be a precedent for the generation of cell type-specific regulatory proteins in other developmental systems where cells undergo terminal differentiation.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
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K. H. Harry, R. Zhou, L. Kroos, and S. B. Melville (2009)
J. Bacteriol. 191, 2728-2742
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One Perturbation of the Mother Cell Gene Regulatory Network Suppresses the Effects of Another during Sporulation of Bacillus subtilis.
L. Wang, J. Perpich, A. Driks, and L. Kroos (2007)
J. Bacteriol. 189, 8467-8473
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Maintaining the Transcription Factor SpoIIID Level Late during Sporulation Causes Spore Defects in Bacillus subtilis.
L. Wang, J. Perpich, A. Driks, and L. Kroos (2007)
J. Bacteriol. 189, 7302-7309
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Cytological Analysis of the Mother Cell Death Process during Sporulation in Bacillus subtilis.
S. Hosoya, Z. Lu, Y. Ozaki, M. Takeuchi, and T. Sato (2007)
J. Bacteriol. 189, 2561-2565
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Bacillus subtilis Aconitase Is Required for Efficient Late-Sporulation Gene Expression..
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J. Bacteriol. 188, 6396-6405
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Characterization of the Global Transcriptional Responses to Different Types of DNA Damage and Disruption of Replication in Bacillus subtilis..
A. I. Goranov, E. Kuester-Schoeck, J. D. Wang, and A. D. Grossman (2006)
J. Bacteriol. 188, 5595-5605
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Substrate Requirements for Regulated Intramembrane Proteolysis of Bacillus subtilis Pro-{sigma}K.
H. Prince, R. Zhou, and L. Kroos (2005)
J. Bacteriol. 187, 961-971
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Comparative Analysis of Physical Maps of Four Bacillus subtilis (natto) Genomes.
D. Qiu, K. Fujita, Y. Sakuma, T. Tanaka, Y. Ohashi, H. Ohshima, M. Tomita, and M. Itaya (2004)
Appl. Envir. Microbiol. 70, 6247-6256
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Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation.
D. W. Hilbert and P. J. Piggot (2004)
Microbiol. Mol. Biol. Rev. 68, 234-262
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BofA protein inhibits intramembrane proteolysis of pro-{sigma}K in an intercompartmental signaling pathway during Bacillus subtilis sporulation.
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PNAS 101, 6385-6390
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Genome Engineering Reveals Large Dispensable Regions in Bacillus subtilis.
H. Westers, R. Dorenbos, J. M. van Dijl, J. Kabel, T. Flanagan, K. M. Devine, F. Jude, S. J. Seror, A. C. Beekman, E. Darmon, et al. (2003)
Mol. Biol. Evol. 20, 2076-2090
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Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis.
S. Nakano, E. Kuster-Schock, A. D. Grossman, and P. Zuber (2003)
PNAS 100, 13603-13608
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Novel Genomic Rearrangement That Affects Expression of the Streptococcus pyogenes Streptolysin O (slo) Gene.
D. J. Savic and J. J. Ferretti (2003)
J. Bacteriol. 185, 1857-1869
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Structural Comparison of Three Types of Staphylococcal Cassette Chromosome mec Integrated in the Chromosome in Methicillin-Resistant Staphylococcus aureus.
T. Ito, Y. Katayama, K. Asada, N. Mori, K. Tsutsumimoto, C. Tiensasitorn, and K. Hiramatsu (2001)
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Evidence that SpoIVFB Is a Novel Type of Membrane Metalloprotease Governing Intercompartmental Communication during Bacillus subtilis Sporulation.
Y.-T. N. Yu and L. Kroos (2000)
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The Bacillus subtilis yabG Gene Is Transcribed by SigK RNA Polymerase during Sporulation, and yabG Mutant Spores Have Altered Coat Protein Composition.
H. Takamatsu, T. Kodama, A. Imamura, K. Asai, K. Kobayashi, T. Nakayama, N. Ogasawara, and K. Watabe (2000)
J. Bacteriol. 182, 1883-1888
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Role of the Sporulation Protein BofA in Regulating Activation of the Bacillus subtilis Developmental Transcription Factor sigma K.
O. Resnekov (1999)
J. Bacteriol. 181, 5384-5388
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The Bacillus subtilis yaaH Gene Is Transcribed by SigE RNA Polymerase during Sporulation, and Its Product Is Involved in Germination of Spores.
T. Kodama, H. Takamatsu, K. Asai, K. Kobayashi, N. Ogasawara, and K. Watabe (1999)
J. Bacteriol. 181, 4584-4591
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A Region of sigma K Involved in Promoter Activation by GerE in Bacillus subtilis.
K. H. Wade, G. Schyns, J. A. Opdyke, and C. P. Moran Jr. (1999)
J. Bacteriol. 181, 4365-4373
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sigma K Can Negatively Regulate sigE Expression by Two Different Mechanisms during Sporulation of Bacillus subtilis.
B. Zhang, P. Struffi, and L. Kroos (1999)
J. Bacteriol. 181, 4081-4088
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Cloning and Nucleotide Sequence Determination of the Entire mec DNA of Pre-Methicillin-Resistant Staphylococcus aureus N315.
T. Ito, Y. Katayama, and K. Hiramatsu (1999)
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Bacillus subtilis Spore Coat.
A. Driks (1999)
Microbiol. Mol. Biol. Rev. 63, 1-20
   Abstract »    Full Text »    PDF »
A Four-Dimensional View of Assembly of a Morphogenetic Protein during Sporulation in Bacillus subtilis.
K. D. Price and R. Losick (1999)
J. Bacteriol. 181, 781-790
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In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family.
H. M. Thorpe and M. C. M. Smith (1998)
PNAS 95, 5505-5510
   Abstract »    Full Text »    PDF »
The Prosequence of Pro-sigma K Promotes Membrane Association and Inhibits RNA Polymerase Core Binding.
B. Zhang, A. Hofmeister, and L. Kroos (1998)
J. Bacteriol. 180, 2434-2441
   Abstract »    Full Text »
The ars Operon in the skin Element of Bacillus subtilis Confers Resistance to Arsenate and Arsenite.
T. Sato and Y. Kobayashi (1998)
J. Bacteriol. 180, 1655-1661
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Negative regulation of the proteolytic activation of a developmental transcription factor in Bacillus subtilis.
O. Resnekov and R. Losick (1998)
PNAS 95, 3162-3167
   Abstract »    Full Text »    PDF »
Anabaena xisF gene encodes a developmentally regulated site-specific recombinase..
C D Carrasco, K S Ramaswamy, T S Ramasubramanian, and J W Golden (1994)
Genes & Dev. 8, 74-83
   Abstract »    PDF »
Amino-terminal amino acids modulate sigma-factor DNA-binding activity..
A J Dombroski, W A Walter, and C A Gross (1993)
Genes & Dev. 7, 2446-2455
   Abstract »    PDF »
Forespore-specific transcription of a gene in the signal transduction pathway that governs Pro-sigma K processing in Bacillus subtilis..
S Cutting, A Driks, R Schmidt, B Kunkel, and R Losick (1991)
Genes & Dev. 5, 456-466
   Abstract »    PDF »
Development-specific sigma-factor essential for late-stage differentiation of Myxococcus xanthus..
D Apelian and S Inouye (1990)
Genes & Dev. 4, 1396-1403
   Abstract »    PDF »
The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene..
B Kunkel, R Losick, and P Stragier (1990)
Genes & Dev. 4, 525-535
   Abstract »    PDF »
Temporal and spatial control of the mother-cell regulatory gene spoIIID of Bacillus subtilis..
B Kunkel, L Kroos, H Poth, P Youngman, and R Losick (1989)
Genes & Dev. 3, 1735-1744
   Abstract »    PDF »
Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor.
L Kroos, B Kunkel, and R Losick (1989)
Science 243, 526-529
   Abstract »    PDF »


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