1932

Abstract

This is a tale of how technology drove the discovery of the molecular basis for signal transduction in the initiation of sporulation in and in bacterial two-component systems. It progresses from genetics to cloning and sequencing to biochemistry to structural biology to an understanding of how proteins evolve interaction specificity and to identification of interaction surfaces by statistical physics. This is about how the people in my laboratory accomplished this feat; without them little would have been done.

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2017-09-08
2024-03-28
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Literature Cited

  1. Allen RW, Ferrone S, Hoch JA. 1.  1982. Characterization of antigens on human lymphocytes coded by messenger RNA translated in vitro. Mol. Immunol. 19:1127–38 [Google Scholar]
  2. Allen RW, Trach KA, Hoch JA. 2.  1987. Identification of the 37-kDa protein displaying a variable interaction with the erythroid cell membrane as glyceraldehyde-3-phosphate dehydrogenase. J. Biol. Chem. 262:649–53 [Google Scholar]
  3. Anagnostopoulos C, Spizizen J. 3.  1961. Requirements for transformation in Bacillus subtilis. J. Bacteriol. 81:741–46 [Google Scholar]
  4. Barrett JF, Goldschmidt RM, Lawrence LE, Foleno B, Chen R. 4.  et al. 1998. Antibacterial agents that inhibit two-component signal transduction systems. PNAS 95:5317–22 [Google Scholar]
  5. Binnie C, Lampe M, Losick R. 5.  1986. Gene encoding the σ37 species of RNA polymerase σ factor from Bacillus subtilis. PNAS 83:5943–47 [Google Scholar]
  6. Burbulys D, Trach KA, Hoch JA. 6.  1991. The initiation of sporulation in Bacillus subtilis is controlled by a multicomponent phosphorelay. Cell 64:545–52 [Google Scholar]
  7. Connors MJ, Howard B, Hoch JA, Setlow P. 7.  1986. Determination of the chromosomal location of four Bacillus subtilis genes which code for a family of small acid-soluble spore proteins. J. Bacteriol. 166:412–16 [Google Scholar]
  8. Curry RA, Dierich MP, Pellegrino MA, Hoch JA. 8.  1976. Evidence for linkage between HLA antigens and receptors for complement components C3b and C3d in human-mouse hybrids. Immunogenetics 3:465–71 [Google Scholar]
  9. Dago AE, Schug A, Procaccini A, Hoch JA, Weigt M, Szurmant H. 9.  2012. Structural basis of histidine kinase autophosphorylation deduced by integrating genomics, molecular dynamics, and mutagenesis. PNAS 109:E1733–42 [Google Scholar]
  10. Dartois V, Liu J, Hoch JA. 10.  1997. Alterations in the flow of one-carbon units affect KinB-dependent sporulation in Bacillus subtilis. Mol. Microbiol. 25:39–51 [Google Scholar]
  11. Fabret C, Hoch JA. 11.  1998. A two-component signal transduction system essential for growth of Bacillus subtilis: implications for anti-infective therapy. J. Bacteriol. 180:6375–83 [Google Scholar]
  12. Feher VA, Zapf JW, Hoch JA, Dahlquist FW, Whiteley JM, Cavanagh J. 12.  1995. 1H, 15N, and 13C backbone chemical shift assignments, secondary structure, and magnesium-binding characteristics of the Bacillus subtilis response regulator, Spo0F, determined by heteronuclear high-resolution NMR. Prot. Sci. 4:1801–14 [Google Scholar]
  13. Ferrari E, Henner DJ, Hoch JA. 13.  1981. Isolation of Bacillus subtilis genes from a Charon 4A library. J. Bacteriol. 146:430–32 [Google Scholar]
  14. Ferrari FA, Hoch JA. 14.  1982. Chromosomal location of Bacillus subtilis DNA fragment uniquely transcribed by sigma-28 containing DNA polymerase. J. Bacteriol. 152:780–85 [Google Scholar]
  15. Ferrari FA, Lang D, Ferrari E, Hoch JA. 15.  1982. Molecular cloning of the spo0B sporulation locus in bacteriophage lambda. J. Bacteriol. 152:809–14 [Google Scholar]
  16. Ferrari FA, Trach KA, Hoch JA. 16.  1985. Sequence analysis of the spo0B locus reveals a polycistronic transcription unit. J. Bacteriol. 161:556–62 [Google Scholar]
  17. Ferrari FA, Trach KA, LeCoq D, Hoch JA. 17.  1985. Molecular cloning and nucleotide sequence of the spo0A locus and its mutations. Molecular Biology of Microbial Differentiation JA Hoch, P Setlow 8–14 Washington, DC: Am. Soc. Microbiol. [Google Scholar]
  18. Ferrari FA, Trach KA, LeCoq D, Spence J, Ferrari E, Hoch JA. 18.  1985. Characterization of the spo0A locus and its deduced product. PNAS 82:2647–51 [Google Scholar]
  19. Fukushima T, Furihata I, Emmins R, Daniel RA, Hoch JA, Szurmant H. 19.  2011. A role for the essential YycG sensor histidine kinase in sensing cell division. Mol. Microbiol. 79:503–22 [Google Scholar]
  20. Fukushima T, Szurmant H, Kim EJ, Perego M, Hoch JA. 20.  2008. A sensor histidine kinase co-ordinates cell wall architecture with cell division in Bacillus subtilis. Mol. Microbiol. 69:621–32 [Google Scholar]
  21. Gay P, LeCoq D, Steinmetz M, Ferrari E, Hoch JA. 21.  1983. Cloning structural gene sacB, which codes for exoenzyme levansucrase of Bacillus subtilis: expression of the gene in Escherichia coli. J. Bacteriol. 153:1424–31 [Google Scholar]
  22. Held GA, Bulla LA Jr., Ferrari E, Hoch JA, Aronson AI, Minnich SA. 22.  1982. Cloning and localization of the lepidopteran protoxin gene of Bacillus thuringiensis subsp. kurstaki. PNAS 79:6065–69 [Google Scholar]
  23. Henner DJ, Ferrari E, Perego M, Hoch JA. 23.  1988. Location of the targets of the hpr-97, sacU32(Hy), and sacQ36(Hy) mutations to upstream regions of the subtilisin promoter. J. Bacteriol. 170:296–300 [Google Scholar]
  24. Higerd TB, Hoch JA, Spizizen J. 24.  1972. Hyperprotease-producing mutants of Bacillus subtilis. J. Bacteriol. 112:1026–28 [Google Scholar]
  25. Hoch JA. 25.  1971. Genetic analysis of pleiotropic negative sporulation mutants in Bacillus subtilis. J. Bacteriol. 105:896–901 [Google Scholar]
  26. Hoch JA. 26.  1976. Genetics of bacterial sporulation. Adv. Genet. 18:69–99 [Google Scholar]
  27. Hoch JA, Coukoulis HJ. 27.  1978. Genetics of the alpha-ketoglutarate dehydrogenase complex of Bacillus subtilis. J. Bacteriol. 133:265–69 [Google Scholar]
  28. Hoch JA, Dierich MP, Pellegrino MA, Ferrone S, Reisfeld RA. 28.  1975. Distinction between malignant L cells and normal mouse fibroblasts by rosette formation with sheep red blood cells. J. Immunol. 114:1638–40 [Google Scholar]
  29. Hoch JA, Mathews JL. 29.  1973. Chromosomal location of pleiotropic negative sporulation mutations in Bacillus subtilis. Genetics 73:215–28 [Google Scholar]
  30. Hoch JA, Nester EW. 30.  1973. Gene-enzyme relationships of aromatic acid biosynthesis in Bacillus subtilis. J. Bacteriol. 116:59–66 [Google Scholar]
  31. Hoch JA, Varughese KI. 31.  2001. Keeping signals straight in phosphorelay signal transduction. J. Bacteriol. 183:4941–49 [Google Scholar]
  32. Hranueli D, Piggot PJ, Mandelstam J. 32.  1974. Statistical estimate of the total number of operons specific for Bacillus subtilis sporulation. J. Bacteriol. 119:684–90 [Google Scholar]
  33. Ishikawa S, Core LJ, Perego M. 33.  2002. Biochemical characterization of aspartyl phosphate phosphatase interaction with a phosphorylated response regulator and its inhibition by a pentapeptide. J. Biol. Chem. 277:20483–89 [Google Scholar]
  34. Jacques DA, Langley DB, Hynson RM, Whitten AE, Kwan A. 34.  et al. 2011. A novel structure of an antikinase and its inhibitor. J. Mol. Biol. 405:214–26 [Google Scholar]
  35. Kallio PT, Fagelson JE, Hoch JA, Strauch MA. 35.  1991. The transition state regulator Hpr of Bacillus subtilis is a DNA-binding protein. J. Biol. Chem. 266:13411–17 [Google Scholar]
  36. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G. 36.  et al. 1997. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–56 [Google Scholar]
  37. Lepesant-Kejzlarova J, Lepesant J-A, Walle J, Billault A, Dedonder R. 37.  1975. Revision of the linkage map of Bacillus subtilis 168: indications for circularity of the chromosome. J. Bacteriol. 121:823–34 [Google Scholar]
  38. Losick R, Shorenstein R, Sonenshein AL. 38.  1970. Structural alteration of RNA polymerase during sporulation. Nature 227:910–13 [Google Scholar]
  39. Lunt B, Szurmant H, Procaccini A, Hoch JA, Hwa T, Weigt M. 39.  2010. Inference of direct residue contacts in two-component signaling. Methods Enzymol 471:17–41 [Google Scholar]
  40. Madhusudan, Zapf JW, Whiteley JM, Hoch JA, Xuong NH, Varughese KI. 40.  1996. Crystal structure of a phosphatase-resistant mutant of sporulation response regulator Spo0F from Bacillus subtilis. Structure 4:679–90 [Google Scholar]
  41. Moran CPJ, Losick R, Sonenshein AL. 41.  1980. Identification of a sporulation locus in cloned Bacillus subtilis deoxyribonucleic acid. J. Bacteriol. 142:331–34 [Google Scholar]
  42. Mueller JP, Bukusoglu G, Sonenshein AL. 42.  1992. Transcriptional regulation of Bacillus subtilis glucose starvation-inducible genes: control of gsiA by the ComP-ComA signal transduction system. J. Bacteriol. 174:4361–73 [Google Scholar]
  43. Mueller JP, Sonenshein AL. 43.  1992. Role of the Bacillus subtilis gsiA gene in regulation of early sporulation gene expression. J. Bacteriol. 174:4374–83 [Google Scholar]
  44. Ng WL, Kazmierczak KM, Winkler ME. 44.  2004. Defective cell wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator. Mol. Microbiol. 53:1161–75 [Google Scholar]
  45. Ng WL, Tsui HC, Winkler ME. 45.  2005. Regulation of the pspA virulence factor and essential pcsB murein biosynthetic genes by the phosphorylated VicR (YycF) response regulator in Streptococcus pneumoniae. J. Bacteriol. 187:7444–59 [Google Scholar]
  46. Ninfa AJ, Magasanik B. 46.  1986. Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. PNAS 83:5909–13 [Google Scholar]
  47. Ninfa AJ, Ninfa EG, Lupas AN, Stock A, Magasanik B, Stock J. 47.  1988. Crosstalk between bacterial chemotaxis signal transduction proteins and regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. PNAS 85:5492–96 [Google Scholar]
  48. Ohlsen KL, Grimsley JK, Hoch JA. 48.  1994. Deactivation of the sporulation transcription factor Spo0A by the Spo0E protein phosphatase. PNAS 91:1756–60 [Google Scholar]
  49. Olson AL, Tucker AT, Bobay BG, Soderblom EJ, Moseley MA. 49.  et al. 2014. Structure and DNA-binding traits of the transition state regulator AbrB. Structure 22:1650–56 [Google Scholar]
  50. Ordal GW, Nettleton DO, Hoch JA. 50.  1983. Genetics of Bacillus subtilis chemotaxis: isolation and mapping of mutations and cloning of chemotaxis genes. J. Bacteriol. 154:1088–97 [Google Scholar]
  51. Pellegrino MA, Curry RA, Pellegrino AG, Hoch JA. 51.  1975. Linkage between the B-cell specific receptor for monkey red blood cells and HL-A antigens in man-mouse hybrids. Immunogenetics 2:543–49 [Google Scholar]
  52. Perego M. 52.  1997. A peptide export-import control circuit modulating bacterial development regulates protein phosphatases of the phosphorelay. PNAS 94:8612–17 [Google Scholar]
  53. Perego M. 53.  2001. A new family of aspartyl-phosphate phosphatases targeting the sporulation transcription factor Spo0A of Bacillus subtilis. Mol. Microbiol. 42:133–44 [Google Scholar]
  54. Perego M. 54.  2013. Forty years in the making: understanding the molecular mechanism of peptide regulation in bacterial development. PLOS Biol 11:e1001516 [Google Scholar]
  55. Perego M, Brannigan JA. 55.  2001. Pentapeptide regulation of aspartyl-phosphate phosphatases. Peptides 22:1541–47 [Google Scholar]
  56. Perego M, Cole SP, Burbulys D, Trach KA, Hoch JA. 56.  1989. Characterization of the gene for a protein kinase which phosphorylates the sporulation-regulatory proteins Spo0A and Spo0F of Bacillus subtilis. J. Bacteriol. 171:6187–96 [Google Scholar]
  57. Perego M, Hanstein CG, Welsh KM, Djavakhishvili T, Glaser P, Hoch JA. 57.  1994. Multiple protein aspartate phosphatases provide a mechanism for the integration of diverse signals in the control of development in Bacillus subtilis. Cell 79:1047–55 [Google Scholar]
  58. Perego M, Higgins CF, Pearce SR, Gallagher MP, Hoch JA. 58.  1991. The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol. Microbiol. 5:173–85 [Google Scholar]
  59. Perego M, Hoch JA. 59.  1987. Isolation and sequence of the spo0E gene: its role in initiation of sporulation in Bacillus subtilis. Mol. Microbiol. 1:125–32 [Google Scholar]
  60. Perego M, Hoch JA. 60.  1988. Sequence analysis and regulation of the hpr locus, a regulatory gene for protease production and sporulation in Bacillus subtilis. J. Bacteriol. 170:2560–67 [Google Scholar]
  61. Perego M, Hoch JA. 61.  1991. Negative regulation of Bacillussubtilis sporulation by the spo0E gene product. J. Bacteriol. 173:2514–20 [Google Scholar]
  62. Perego M, Hoch JA. 62.  1996. Cell-cell communication regulates the effects of protein aspartate phosphatases on the phosphorelay controlling development in Bacillus subtilis. PNAS 93:1549–53 [Google Scholar]
  63. Perego M, Spiegelman GB, Hoch JA. 63.  1988. Structure of the gene for the transition state regulator, abrB: Regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis. Mol. Microbiol. 2:689–99 [Google Scholar]
  64. Perego M, Wu J-J, Spiegelman GB, Hoch JA. 64.  1991. Mutational dissociation of the positive and negative regulatory properties of the Spo0A sporulation transcription of Bacillus subtilis. Gene 100:207–12 [Google Scholar]
  65. Piggot PJ. 65.  1973. Mapping of asporogenous mutations of Bacillus subtilis: a minimum estimate of the number of sporulation operons. J. Bacteriol. 114:1241–53 [Google Scholar]
  66. Pottathil M, Lazazzera BA. 66.  2003. The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front. Biosci. 8:d32–45 [Google Scholar]
  67. Reizer J, Reizer A, Perego M, Saier MHJ. 67.  1997. Characterization of a family of bacterial response regulator aspartyl-phosphate (RAP) phosphatases. Microbial Comp. Genom. 2:103–11 [Google Scholar]
  68. Rutberg B, Hoch JA. 68.  1970. Citric acid cycle: gene-enzyme relationships in Bacillus subtilis. J. Bacteriol. 104:826–33 [Google Scholar]
  69. Santelli E, Liddington RC, Mohan MA, Hoch JA, Szurmant H. 69.  2007. The crystal structure of Bacillus subtilis YycI reveals a common fold for two members of an unusual class of sensor histidine kinase regulatory proteins. J. Bacteriol. 189:3290–95 [Google Scholar]
  70. Schug A, Weigt M, Hoch JA, Onuchic JN, Hwa T, Szurmant H. 70.  2010. Computational modeling of phosphotransfer complexes in two-component signaling. Methods Enzymol 471:43–58 [Google Scholar]
  71. Schug A, Weigt M, Onuchic JN, Hwa T, Szurmant H. 71.  2009. High-resolution protein complexes from integrating genomic information with molecular simulation. PNAS 106:22124–29 [Google Scholar]
  72. Shabbaz M, Hoch JA, Trach KA, Hural JA, Webber S, Whiteley JA. 72.  1987. Structural studies and isolation of cDNA clones providing the complete sequence of rat liver dihydropteridine reductase. J. Biol. Chem. 262:16412–16 [Google Scholar]
  73. Solomon JM, Lazazzera BA, Grossman AD. 73.  1996. Purification and characterization of an extracellular peptide factor that affects two different developmental pathways in Bacillus subtilis. Genes Dev. 10:2014–24 [Google Scholar]
  74. Spizizen J. 74.  1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. PNAS 44:1072–75 [Google Scholar]
  75. Steiner E, Dago AE, Young DI, Heap JT, Minton NP. 75.  et al. 2011. Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum. Mol. Microbiol. 80:641–54 [Google Scholar]
  76. Stock A, Koshland DE Jr, Stock J. 76.  1985. Homologies between the Salmonella typhimurium CheY protein and proteins involved in the regulation of chemotaxis, membrane protein synthesis, and sporulation. PNAS 82:7989–93 [Google Scholar]
  77. Strauch MA, Hoch JA. 77.  1993. Transition state regulators: sentinels of Bacillus subtilis post-exponential gene expression. Mol. Microbiol. 7:337–42 [Google Scholar]
  78. Strauch MA, Spiegelman GB, Perego M, Johnson WC, Burbulys D, Hoch JA. 78.  1989. The transition state transcription regulator abrB of Bacillus subtilis is a DNA-binding protein. EMBO J. 8:1615–21 [Google Scholar]
  79. Strauch MA, Webb V, Spiegelman G, Hoch JA. 79.  1990. The Spo0A protein of Bacillus subtilis is a repressor of the abrB gene. PNAS 87:1801–5 [Google Scholar]
  80. Sun D, Stragier P, Setlow P. 80.  1989. Identification of a new sigma-factor involved in compartmentalized gene expression during sporulation of Bacillus subtilis. Genes Dev. 3:141–49 [Google Scholar]
  81. Szurmant H, Bu L, Brooks CL III, Hoch JA. 81.  2008. An essential sensor histidine kinase controlled by transmembrane helix interactions with its auxiliary proteins. PNAS 105:5891–96 [Google Scholar]
  82. Szurmant H, Mohan MA, Imus PM, Hoch JA. 82.  2007. YycH and YycI interact to regulate the essential YycFG two-component system in Bacillus subtilis. J. Bacteriol. 189:3280–99 [Google Scholar]
  83. Szurmant H, Nelson K, Kim EJ, Perego M, Hoch JA. 83.  2005. YycH regulates the activity of the essential YycFG two-component system in Bacillus subtilis. J. Bacteriol. 187:5419–26 [Google Scholar]
  84. Szurmant H, Zhao H, Mohan MA, Hoch JA, Varughese KI. 84.  2006. The crystal structure of YycH involved in the regulation of the essential YycFG two-component system in Bacillus subtilis reveals a novel tertiary structure. Prot. Sci. 15:929–34 [Google Scholar]
  85. Trach KA, Chapman JW, Piggot PJ, Hoch JA. 85.  1985. Deduced product of the stage 0 sporulation gene spo0F shares homology with the Spo0A, OmpR and SfrA proteins. PNAS 82:7260–64 [Google Scholar]
  86. Trach KA, Hoch JA. 86.  1993. Multisensory activation of the phosphorelay initiating sporulation in Bacillus subtilis: identification and sequence of the protein kinase of the alternate pathway. Mol. Microbiol. 8:69–79 [Google Scholar]
  87. Trowsdale J, Chen SMH, Hoch JA. 87.  1978. Evidence that spo0A mutations are recessive in spo0A/spo0A+ merodiploid strains of Bacillus subtilis. J. Bacteriol. 135:99–113 [Google Scholar]
  88. Trowsdale J, Chen SMH, Hoch JA. 88.  1979. Genetic analysis of a class of polymyxin resistant partial revertants of stage 0 sporulation mutants of Bacillus subtilis: map of the chromosome region near the origin of replication. Mol. Gen. Genet. 173:61–70 [Google Scholar]
  89. Trowsdale J, Hoch JA. 89.  1982. Expression of alkaline phosphatase from cloned human tumor cell lines in human/mouse somatic cell hybrids. Oncodevelopmental Biol. Med. 3:391–402 [Google Scholar]
  90. Tzeng Y-L, Hoch JA. 90.  1997. Molecular recognition in signal transduction: the interaction surfaces of the Spo0F response regulator with its cognate phosphorelay proteins revealed by alanine scanning mutagenesis. J. Mol. Biol. 272:200–12 [Google Scholar]
  91. Tzeng Y-L, Zhou XZ, Hoch JA. 91.  1998. Phosphorylation of the Spo0B response regulator phosphotransferase of the phosphorelay initiating development in Bacillus subtilis. J. Biol. Chem. 273:23849–55 [Google Scholar]
  92. Varughese KI, Madhusudan, Zhou XZ, Whiteley JM, Hoch JA. 92.  1998. Formation of a novel four-helix bundle and molecular recognition sites by dimerization of a response regulator phosphotransferase. Mol. Cell 2:485–93 [Google Scholar]
  93. Vaughn JL, Feher V, Naylor S, Strauch MA, Cavanagh J. 93.  2000. Novel DNA binding domain and genetic regulation model of Bacillus subtilis transition state regulator AbrB. Nat. Struct. Biol. 7:1139–46 [Google Scholar]
  94. Wang L, Grau R, Perego M, Hoch JA. 94.  1997. A novel histidine kinase inhibitor regulating development in Bacillus subtilis. Genes Dev. 11:2569–79 [Google Scholar]
  95. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T. 95.  2009. Identification of direct residue contacts in protein-protein interaction by message passing. PNAS 106:67–72 [Google Scholar]
  96. White RA, Szurmant H, Hoch JA, Hwa T. 96.  2007. Features of protein-protein interactions in two-component signaling deduced from genomic libraries. Methods Enzymol 422:75–101 [Google Scholar]
  97. Yamaguchi M, Hatefi Y, Trach KA, Hoch JA. 97.  1988. Amino acid sequence of the signal peptide of mitochondrial nicotinamide nucleotide transhydrogenase as determined from the sequence of its messenger RNA. Biochem. Biophys. Res. Commun. 157:24–29 [Google Scholar]
  98. Yamaguchi M, Hatefi Y, Trach KA, Hoch JA. 98.  1988. The primary structure of the mitochondrial energy-linked nicotinamide nucleotide transhydrogenase deduced from the sequence of cDNA clones. J. Biol. Chem. 263:2761–67 [Google Scholar]
  99. Zapf JW, Madhusudan, Grimshaw CE, Hoch JA, Varughese KI, Whiteley JM. 99.  1998. A source of response regulator autophosphatase activity: the critical role of a residue adjacent to the Spo0F autophosphorylation active site. Biochemistry 37:7725–32 [Google Scholar]
  100. Zapf JW, Sen U, Madhusudan, Hoch JA, Varughese KI. 100.  2000. A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Struct. Fold. Des. 8:851–62 [Google Scholar]
  101. Zhao H, Msadek T, Zapf JW, Madhusudan, Hoch JA, Varughese KI. 101.  2002. DNA complexed structure of the key transcription factor initiating development in sporulating bacteria. Structure 10:1041–50 [Google Scholar]
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