Identification of essential alphaproteobacterial genes reveals operational variability in conserved developmental and cell cycle systems

Molecular Microbiology

Volumn 93, Issue 4, 2014, Pages 713-735

  Curtis, Patrick D ^a   Brun, Yves V ^b  

^a UNIVERSITY OF MISSISSIPPI   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; DNA METHYLTRANSFERASE; PROTEIN CCRM; UNCLASSIFIED DRUG;

AGROBACTERIUM TUMEFACIENS; ALPHAPROTEOBACTERIA; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BREVUNDIMONAS SUBVIBRIOIDES; CAULOBACTER VIBRIOIDES; CELL CYCLE; CELL CYCLE REGULATION; CONTROLLED STUDY; DIVJ GENE; DIVK GENE; GENETIC CONSERVATION; GENETIC DISTANCE; GENETIC VARIABILITY; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; CAULOBACTERACEAE; COMPARATIVE STUDY; ESSENTIAL GENE; GENETICS; METABOLISM; PHYSIOLOGY;

AGROBACTERIUM TUMEFACIENS; ALPHAPROTEOBACTERIA; BREVUNDIMONAS SUBVIBRIOIDES; CAULOBACTER VIBRIOIDES; CAULOBACTERALES; RHIZOBIALES;

AGROBACTERIUM TUMEFACIENS; CAULOBACTERACEAE; CELL CYCLE; CELL CYCLE PROTEINS; GENES, ESSENTIAL;

EID: 84925883643     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12686     Document Type: Article

References (101)

1. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006 0008.
2. Barnett, M.J., Hung, D.Y., Reisenauer, A., Shapiro, L., and Long, S.R. (2001) A homolog of the CtrA cell cycle regulator is present and essential in Sinorhizobium meliloti. J Bacteriol 183: 3204-3210.
3. Bellefontaine, A.F., Pierreux, C.E., Mertens, P., Vandenhaute, J., Letesson, J.J., and De Bolle, X. (2002) Plasticity of a transcriptional regulation network among alpha-proteobacteria is supported by the identification of CtrA targets in Brucella abortus. Mol Microbiol 43: 945-960.
4. Bernhardt, T.G., and de Boer, P.A. (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18: 555-564.
5. Biondi, E.G., Reisinger, S.J., Skerker, J.M., Arif, M., Perchuk, B.S., Ryan, K.R., and Laub, M.T. (2006a) Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444: 899-904.
6. Biondi, E.G., Skerker, J.M., Arif, M., Prasol, M.S., Perchuk, B.S., and Laub, M.T. (2006b) A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus. Mol Microbiol 59: 386-401.
7. Bird, T.H., and MacKrell, A. (2011) A CtrA homolog affects swarming motility and encystment in Rhodospirillum centenum. Arch Microbiol 193: 451-459.
8. de Boer, P.A., Crossley, R.E., and Rothfield, L.I. (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56: 641-649.
9. Brassinga, A.K., Siam, R., McSween, W., Winkler, H., Wood, D., and Marczynski, G.T. (2002) Conserved response regulator CtrA and IHF binding sites in the alpha-proteobacteria Caulobacter crescentus and Rickettsia prowazekii chromosomal replication origins. J Bacteriol 184: 5789-5799.
10. Brilli, M., Fondi, M., Fani, R., Mengoni, A., Ferri, L., Bazzicalupo, M., and Biondi, E.G. (2010) The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis. BMC Syst Biol 4: 52.
11. Brown, P.J., de Pedro, M.A., Kysela, D.T., Van der Henst, C., Kim, J., De Bolle, X., etal. (2012) Polar growth in the Alphaproteobacterial order Rhizobiales. Proc Natl Acad Sci USA 109: 1697-1701.
12. Chen, Y.E., Tsokos, C.G., Biondi, E.G., Perchuk, B.S., and Laub, M.T. (2009) Dynamics of two phosphorelays controlling cell cycle progression in Caulobacter crescentus. J Bacteriol 191: 7417-7429.
13. Christen, B., Abeliuk, E., Collier, J.M., Kalogeraki, V.S., Passarelli, B., Coller, J.A., etal. (2011) The essential genome of a bacterium. Mol Syst Biol 7: 528.
14. Collier, J., McAdams, H.H., and Shapiro, L. (2007) A DNA methylation ratchet governs progression through a bacterial cell cycle. Proc Natl Acad Sci USA 104: 17111-17116.
15. Curtis, N.A., Eisenstadt, R.L., Turner, K.A., and White, A.J. (1985) Inhibition of penicillin-binding protein 3 of Escherichia coli K-12. Effects upon growth, viability and outer membrane barrier function. J Antimicrob Chemother 16: 287-296.
16. Curtis, P.D., and Brun, Y.V. (2010) Getting in the loop: regulation of development in Caulobacter crescentus. Microbiol Mol Biol Rev 74: 13-41.
17. Curtis, P.D., Quardokus, E.M., Lawler, M.L., Guo, X., Klein, D., Chen, J.C., etal. (2012) The scaffolding and signalling functions of a localization factor impact polar development. Mol Microbiol 84: 712-735.
18. Curtis, P.D., Klein, D., and Brun, Y.V. (2013) Effect of a ctrA promoter mutation, causing a reduction in CtrA abundance, on the cell cycle and development of Caulobacter crescentus. BMC Microbiol 13: 166.
19. Deich, J., Judd, E.M., McAdams, H.H., and Moerner, W.E. (2004) Visualization of the movement of single histidine kinase molecules in live Caulobacter cells. Proc Natl Acad Sci USA 101: 15921-15926.
20. Derouaux, A., Wolf, B., Fraipont, C., Breukink, E., Nguyen-Disteche, M., and Terrak, M. (2008) The monofunctional glycosyltransferase of Escherichia coli localizes to the cell division site and interacts with penicillin-binding protein 3, FtsW, and FtsN. J Bacteriol 190: 1831-1834.
21. Doublet, P., van Heijenoort, J., and Mengin-Lecreulx, D. (1992) Identification of the Escherichia coli murI gene, which is required for the biosynthesis of D-glutamic acid, a specific component of bacterial peptidoglycan. J Bacteriol 174: 5772-5779.
22. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
23. Edwards, D.H., and Errington, J. (1997) The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24: 905-915.
24. Fioravanti, A., Fumeaux, C., Mohapatra, S.S., Bompard, C., Brilli, M., Frandi, A., etal. (2013) DNA binding of the cell cycle transcriptional regulator GcrA depends on N6-adenosine methylation in Caulobacter crescentus and other Alphaproteobacteria. PLoS Genet 9: e1003541.
25. French, C.T., Lao, P., Loraine, A.E., Matthews, B.T., Yu, H., and Dybvig, K. (2008) Large-scale transposon mutagenesis of Mycoplasma pulmonis. Mol Microbiol 69: 67-76.
26. Gallagher, L.A., Ramage, E., Jacobs, M.A., Kaul, R., Brittnacher, M., and Manoil, C. (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci USA 104: 1009-1014.
27. Gil, R., Silva, F.J., Pereto, J., and Moya, A. (2004) Determination of the core of a minimal bacterial gene set. Microbiol Mol Biol Rev 68: 518-537, table of contents.
28. Glass, J.I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M.R., Maruf, M., etal. (2006) Essential genes of a minimal bacterium. Proc Natl Acad Sci USA 103: 425-430.
29. Goley, E.D., Yeh, Y.C., Hong, S.H., Fero, M.J., Abeliuk, E., McAdams, H.H., and Shapiro, L. (2011) Assembly of the Caulobacter cell division machine. Mol Microbiol 80: 1680-1698.
30. Gonzalez, D., and Collier, J. (2013) DNA methylation by CcrM activates the transcription of two genes required for the division of Caulobacter crescentus. Mol Microbiol 88: 203-218.
31. Gonzalez, D., Kozdon, J.B., McAdams, H.H., Shapiro, L., and Collier, J. (2014) The functions of DNA methylation by CcrM in Caulobacter crescentus: a global approach. Nucleic Acids Res 42: 3720-3735.
32. Goodner, B., Hinkle, G., Gattung, S., Miller, N., Blanchard, M., Qurollo, B., etal. (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294: 2323-2328.
33. Gora, K.G., Tsokos, C.G., Chen, Y.E., Srinavasan, B.S., Perchuk, B.S., and Laub, M.T. (2010) A cell-type-specific protein-protein interaction modulates transcriptional activity of a master regulator in Caulobacter crescentus. Mol Cell 39: 455-467.
34. Gora, K.G., Cantin, A., Wohlever, M., Joshi, K.K., Perchuk, B.S., Chien, P., and Laub, M.T. (2013) Regulated proteolysis of a transcription factor complex is critical to cell cycle progression in Caulobacter crescentus. Mol Microbiol 87: 1277-1289.
35. Greene, S.E., Brilli, M., Biondi, E.G., and Komeili, A. (2012) Analysis of the CtrA pathway in Magnetospirillum reveals an ancestral role in motility in alphaproteobacteria. J Bacteriol 194: 2973-2986.
36. Hallez, R., Mignolet, J., Van Mullem, V., Wery, M., Vandenhaute, J., Letesson, J.J., etal. (2007) The asymmetric distribution of the essential histidine kinase PdhS indicates a differentiation event in Brucella abortus. EMBO J 26: 1444-1455.
37. Hardy, G.G., Allen, R.C., Toh, E., Long, M., Brown, P.J., Cole-Tobian, J.L., and Brun, Y.V. (2010) A localized multimeric anchor attaches the Caulobacter holdfast to the cell pole. Mol Microbiol 76: 409-427.
38. Hecht, G.B., Lane, T., Ohta, N., Sommer, J.M., and Newton, A. (1995) An essential single domain response regulator required for normal cell division and differentiation in Caulobacter crescentus. EMBO J 14: 3915-3924.
39. Hinz, A.J., Larson, D.E., Smith, C.S., and Brun, Y.V. (2003) The Caulobacter crescentus polar organelle development protein PodJ is differentially localized and is required for polar targeting of the PleC development regulator. Mol Microbiol 47: 929-941.
40. Hiraga, S., Niki, H., Ogura, T., Ichinose, C., Mori, H., Ezaki, B., and Jaffe, A. (1989) Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. J Bacteriol 171: 1496-1505.
41. Holtzendorff, J., Hung, D., Brende, P., Reisenauer, A., Viollier, P.H., McAdams, H.H., and Shapiro, L. (2004) Oscillating global regulators control the genetic circuit driving a bacterial cell cycle. Science 304: 983-987.
42. Hottes, A.K., Meewan, M., Yang, D., Arana, N., Romero, P., McAdams, H.H., and Stephens, C. (2004) Transcriptional profiling of Caulobacter crescentus during growth on complex and minimal media. J Bacteriol 186: 1448-1461.
43. Hottes, A.K., Shapiro, L., and McAdams, H.H. (2005) DnaA coordinates replication initiation and cell cycle transcription in Caulobacter crescentus. Mol Microbiol 58: 1340-1353.
44. Iniesta, A.A., and Shapiro, L. (2008) A bacterial control circuit integrates polar localization and proteolysis of key regulatory proteins with a phospho-signaling cascade. Proc Natl Acad Sci USA 105: 16602-16607.
45. Iniesta, A.A., McGrath, P.T., Reisenauer, A., McAdams, H.H., and Shapiro, L. (2006) A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc Natl Acad Sci USA 103: 10935-10940.
46. Jacobs, C., Domian, I.J., Maddock, J.R., and Shapiro, L. (1999) Cell cycle-dependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division. Cell 97: 111-120.
47. Jacobs, C., Hung, D., and Shapiro, L. (2001) Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle. Proc Natl Acad Sci USA 98: 4095-4100.
48. Jacobs, C., Ausmees, N., Cordwell, S.J., Shapiro, L., and Laub, M.T. (2003) Functions of the CckA histidine kinase in Caulobacter cell cycle control. Mol Microbiol 47: 1279-1290.
49. Janakiraman, R.S., and Brun, Y.V. (1999) Cell cycle control of a holdfast attachment gene in Caulobacter crescentus. J Bacteriol 181: 1118-1125.
50. Kahng, L.S., and Shapiro, L. (2001) The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J Bacteriol 183: 3065-3075.
51. Kelly, A.J., Sackett, M.J., Din, N., Quardokus, E., and Brun, Y.V. (1998) Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes Dev 12: 880-893.
52. Kim, J., Heindl, J.E., and Fuqua, C. (2013) Coordination of division and development influences complex multicellular behavior in Agrobacterium tumefaciens. PLoS ONE 8: e56682.
53. Kozdon, J.B., Melfi, M.D., Luong, K., Clark, T.A., Boitano, M., Wang, S., etal. (2013) Global methylation state at base-pair resolution of the Caulobacter genome throughout the cell cycle. Proc Natl Acad Sci USA 110: E4658-E4667.
54. Kuru, E., Hughes, H.V., Brown, P.J., Hall, E., Tekkam, S., Cava, F., etal. (2012) In situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew Chem Int Ed Engl 51: 12519-12523.
55. Lam, H., Schofield, W.B., and Jacobs-Wagner, C. (2006) A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124: 1011-1023.
56. Lang, A.S., and Beatty, J.T. (2000) Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus. Proc Natl Acad Sci USA 97: 859-864.
57. Langridge, G.C., Phan, M.D., Turner, D.J., Perkins, T.T., Parts, L., Haase, J., etal. (2009) Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 19: 2308-2316.
58. Laub, M.T., Chen, S.L., Shapiro, L., and McAdams, H.H. (2002) Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci USA 99: 4632-4637.
59. de Leeuw, E., Graham, B., Phillips, G.J., ten Hagen-Jongman, C.M., Oudega, B., and Luirink, J. (1999) Molecular characterization of Escherichia coli FtsE and FtsX. Mol Microbiol 31: 983-993.
60. Li, H., and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
61. Li, H., and Durbin, R. (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595.
62. Lutkenhaus, J., Pichoff, S., and Du, S. (2012) Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton 69: 778-790.
63. Malakooti, J., and Ely, B. (1995) Principal sigma subunit of the Caulobacter crescentus RNA polymerase. J Bacteriol 177: 6854-6860.
64. Malakooti, J., Wang, S.P., and Ely, B. (1995) A consensus promoter sequence for Caulobacter crescentus genes involved in biosynthetic and housekeeping functions. J Bacteriol 177: 4372-4376.
65. Matroule, J.Y., Lam, H., Burnette, D.T., and Jacobs-Wagner, C. (2004) Cytokinesis monitoring during development; rapid pole-to-pole shuttling of a signaling protein by localized kinase and phosphatase in Caulobacter. Cell 118: 579-590.
66. Murray, S.M., Panis, G., Fumeaux, C., Viollier, P.H., and Howard, M. (2013) Computational and genetic reduction of a cell cycle to its simplest, primordial components. PLoS Biol 11: e1001749.
67. Ogura, T., Bouloc, P., Niki, H., D'Ari, R., Hiraga, S., and Jaffe, A. (1989) Penicillin-binding protein 2 is essential in wild-type Escherichia coli but not in lov or cya mutants. J Bacteriol 171: 3025-3030.
68. Ohta, N., Lane, T., Ninfa, E.G., Sommer, J.M., and Newton, A. (1992) A histidine protein kinase homologue required for regulation of bacterial cell division and differentiation. Proc Natl Acad Sci USA 89: 10297-10301.
69. Pierce, D.L., O'Donnol, D.S., Allen, R.C., Javens, J.W., Quardokus, E.M., and Brun, Y.V. (2006) Mutations in DivL and CckA rescue a divJ null mutant of Caulobacter crescentus by reducing the activity of CtrA. J Bacteriol 188: 2473-2482.
70. Poindexter, J.S. (1964) Biological properties and classification of the Caulobacter group. Bacteriol Rev 28: 231-295.
71. Quon, K.C., Marczynski, G.T., and Shapiro, L. (1996) Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84: 83-93.
72. Radhakrishnan, S.K., Pritchard, S., and Viollier, P.H. (2010) Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog. Dev Cell 18: 90-101.
73. Reisenauer, A., and Shapiro, L. (2002) DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter. EMBO J 21: 4969-4977.
74. Reisinger, S.J., Huntwork, S., Viollier, P.H., and Ryan, K.R. (2007) DivL performs critical cell cycle functions in Caulobacter crescentus independent of kinase activity. J Bacteriol 189: 8308-8320.
75. Rico, A.I., Krupka, M., and Vicente, M. (2013) In the beginning, Escherichia coli assembled the proto-ring: an initial phase of division. J Biol Chem 288: 20830-20836.
76. Roberts, R.J., Vincze, T., Posfai, J., and Macelis, D. (2010) REBASE - a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 38: D234-D236.
77. Robertson, G.T., Reisenauer, A., Wright, R., Jensen, R.B., Jensen, A., Shapiro, L., and Roop, R.M., 2nd (2000) The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182: 3482-3489.
78. Sciochetti, S.A., Ohta, N., and Newton, A. (2005) The role of polar localization in the function of an essential Caulobacter crescentus tyrosine kinase. Mol Microbiol 56: 1467-1480.
79. Skerker, J.M., and Shapiro, L. (2000) Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J 19: 3223-3234.
80. Sliusarenko, O., Heinritz, J., Emonet, T., and Jacobs-Wagner, C. (2011) High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80: 612-627.
81. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
82. Stephens, C., Zweiger, G., and Shapiro, L. (1995) Coordinate cell cycle control of a Caulobacter DNA methyltransferase and the flagellar genetic hierarchy. J Bacteriol 177: 1662-1669.
83. Stephens, C., Reisenauer, A., Wright, R., and Shapiro, L. (1996) A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc Natl Acad Sci USA 93: 1210-1214.
84. Strobel, W., Moll, A., Kiekebusch, D., Klein, K.E., and Thanbichler, M. (2014) Function and localization dynamics of bifunctional penicillin-binding proteins in Caulobacter crescentus. J Bacteriol 196: 1627-1639.
85. Subramanian, K., Paul, M.R., and Tyson, J.J. (2013) Potential role of a bistable histidine kinase switch in the asymmetric division cycle of Caulobacter crescentus. PLoS Comput Biol 9: e1003221.
86. Tan, M.H., Kozdon, J.B., Shen, X., Shapiro, L., and McAdams, H.H. (2010) An essential transcription factor, SciP, enhances robustness of Caulobacter cell cycle regulation. Proc Natl Acad Sci USA 107: 18985-18990.
87. Terrana, B., and Newton, A. (1975) Pattern of unequal cell division and development in Caulobacter crescentus. Dev Biol 44: 380-385.
88. Thanbichler, M., and Shapiro, L. (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126: 147-162.
89. Toh, E., Kurtz, H.D., Jr, and Brun, Y.V. (2008) Characterization of the Caulobacter crescentus holdfast polysaccharide biosynthesis pathway reveals significant redundancy in the initiating glycosyltransferase and polymerase steps. J Bacteriol 190: 7219-7231.
90. Tsokos, C.G., Perchuk, B.S., and Laub, M.T. (2011) A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Dev Cell 20: 329-341.
91. Typas, A., Banzhaf, M., Gross, C.A., and Vollmer, W. (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10: 123-136.
92. Viollier, P.H., Sternheim, N., and Shapiro, L. (2002a) A dynamically localized histidine kinase controls the asymmetric distribution of polar pili proteins. EMBO J 21: 4420-4428.
93. Viollier, P.H., Sternheim, N., and Shapiro, L. (2002b) Identification of a localization factor for the polar positioning of bacterial structural and regulatory proteins. Proc Natl Acad Sci USA 99: 13831-13836.
94. Wheeler, R.T., and Shapiro, L. (1999) Differential localization of two histidine kinases controlling bacterial cell differentiation. Mol Cell 4: 683-694.
95. Wood, D.W., Setubal, J.C., Kaul, R., Monks, D.E., Kitajima, J.P., Okura, V.K., etal. (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294: 2317-2323.
96. Wright, R., Stephens, C., and Shapiro, L. (1997) The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J Bacteriol 179: 5869-5877.
97. Wu, J., Ohta, N., Zhao, J.L., and Newton, A. (1999) A novel bacterial tyrosine kinase essential for cell division and differentiation. Proc Natl Acad Sci USA 96: 13068-13073.
98. Wu, L.J., and Errington, J. (2012) Nucleoid occlusion and bacterial cell division. Nat Rev Microbiol 10: 8-12.
99. Yakhnina, A.A., and Gitai, Z. (2013) Diverse functions for six glycosyltransferases in Caulobacter crescentus cell wall assembly. J Bacteriol 195: 4527-4535.
100. Zweiger, G., and Shapiro, L. (1994) Expression of Caulobacter dnaA as a function of the cell cycle. J Bacteriol 176: 401-408.
101. Zweiger, G., Marczynski, G., and Shapiro, L. (1994) A Caulobacter DNA methyltransferase that functions only in the predivisional cell. J Mol Biol 235: 472-485.