Genome-wide analysis of in vivo binding of the master regulator DasR in streptomyces coelicolor identifies novel non-canonical targets

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  ͆wiatek Połatyńska, Magdalena A ^a   Bucca, Giselda ^b   Laing, Emma ^b   Gubbens, Jacob ^a   Titgemeyer, Fritz ^c   Smith, Colin P ^b   Rigali, Sébastien ^d   Van Wezel, Gilles P ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c MÜNSTER UNIVERSITY OF APPLIED SCIENCES   (Germany)

^d UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; N ACETYLGLUCOSAMINE; PROTEIN DASR; REGULATOR PROTEIN; RNA; TRANSCRIPTOME; TRANSPOSASE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CONTROLLED STUDY; GENETIC ASSOCIATION; IN VIVO STUDY; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN METABOLISM; REGULON; STREPTOMYCES COELICOLOR; TRANSCRIPTOMICS; BACTERIAL GENOME; DNA MICROARRAY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

STREPTOMYCES COELICOLOR; STREPTOMYCINEAE;

ACETYLGLUCOSAMINE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REGULON; RESPONSE ELEMENTS; STREPTOMYCES COELICOLOR; TRANSCRIPTION FACTORS;

EID: 84929461408     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0122479     Document Type: Article

References (91)

1. Martinez-Antonio A, Collado-Vides J (2003) Identifying global regulators in transcriptional regulatory networks in bacteria. Curr Opin Microbiol 6: 482-489. PMID: 14572541
2. Sonenshein AL (2007) Control of key metabolic intersections in Bacillus subtilis. Nat Rev Microbiol 5: 917-927. PMID: 17982469
3. Claessen D, Rozen DE, Kuipers OP, Sogaard-Andersen L, van Wezel GP (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12: 115-124. doi: 10.1038/nrmicro3178 PMID: 24384602
4. Hutchings MI, Hoskisson PA, Chandra G, Buttner MJ (2004) Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 150: 2795-2806. PMID: 15347739
5. Chater KF, Losick R (1997) Mycelial life style of Streptomyces coelicolor A3(2) and its relatives. In: Shapiro JA, Dworkin M, editors. Bacteria as multicellular organisms. New York: Oxford University Press. pp. 149-182.
6. Hopwood DA (2007) Streptomyces in nature and medicine: the antibiotic makers. New York: Oxford University Press.
7. van Wezel GP, McDowall KJ (2011) The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep 28: 1311-1333. doi: 10.1039/c1np00003a PMID: 21611665
8. Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, et al. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147. PMID: 12000953
9. Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F, Girard G, Yanez-Guerra LA, Ramos-Aboites HE, et al. (2013) The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island. Genome Biol Evol 5: 1165-1175. doi: 10.1093/gbe/evt082 PMID: 23709624
10. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, et al. (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21: 526-531. PMID: 12692562
11. Ohnishi Y, Ishikawa J, Hara H, Suzuki H, Ikenoya M, Ikeda H, et al. (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 190: 4050-4060. doi: 10.1128/JB.00204-08 PMID: 18375553
12. Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci U S A 100: 14555-14561. PMID: 12970466
13. Cooper MA, Shlaes D (2011) Fix the antibiotics pipeline. Nature 472: 32. doi: 10.1038/472032a PMID: 21475175
14. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL (2007) Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat Rev Drug Discov 6: 29-40. PMID: 17159923
15. Baltz RH (2008) Renaissance in antibacterial discovery from actinomycetes. Current Opin Pharmacol 8: 557-563. doi: 10.1016/j.coph.2008.04.008 PMID: 18524678
16. Zhu H, Sandiford SK, van Wezel GP (2014) Triggers and cues that activate antibiotic production by actinomycetes. J Ind Microbiol Biotechnol 41: 371-386. doi: 10.1007/s10295-013-1309-z PMID: 23907251
17. Sanchez S, Chavez A, Forero A, Garcia-Huante Y, Romero A, Sanchez M, et al. (2010) Carbon source regulation of antibiotic production. J Antibiot (Tokyo) 63: 442-459. doi: 10.1038/ja.2010.78 PMID: 20664603
18. van Wezel GP, McKenzie NL, Nodwell JR (2009) Chapter 5. Applying the genetics of secondary metabolism in model actinomycetes to the discovery of new antibiotics. Methods Enzymol 458: 117-141. doi: 10.1016/S0076-6879(09)04805-8 PMID: 19374981
19. Brückner R, Titgemeyer F (2002) Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol Lett 209: 141-148. PMID: 12007797
20. Deutscher J (2008) The mechanisms of carbon catabolite repression in bacteria. Curr Opin Microbiol 11: 87-93. doi: 10.1016/j.mib.2008.02.007 PMID: 18359269
21. Gorke B, Stülke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6: 613-624. doi: 10.1038/nrmicro1932 PMID: 18628769
22. Angell S, Lewis CG, Buttner MJ, Bibb MJ (1994) Glucose repression in Streptomyces coelicolor A3(2): a likely regulatory role for glucose kinase. Mol Gen Genet 244: 135-143. PMID: 8052232
23. van Wezel GP, Konig M, Mahr K, Nothaft H, Thomae AW, Bibb M, et al. (2007) A new piece of an old jigsaw: glucose kinase is activated posttranslationally in a glucose transport-dependent manner in Streptomyces coelicolor A3(2). J Mol Microbiol Biotechnol 12: 67-74. PMID: 17183213
24. van Wezel GP, Mahr K, Konig M, Traag BA, Pimentel-Schmitt EF, Willimek A, et al. (2005) GlcP constitutes the major glucose uptake system of Streptomyces coelicolor A3(2). Mol Microbiol 55: 624-636. PMID: 15659175
25. Nothaft H, Dresel D, Willimek A, Mahr K, Niederweis M, Titgemeyer F (2003) The phosphotransferase system of Streptomyces coelicolor is biased for N-acetylglucosamine metabolism. J Bacteriol 185: 7019-7023. PMID: 14617669
26. Nothaft H, Rigali S, Boomsma B, Swiatek M, McDowall KJ, van Wezel GP, et al. (2010) The permease gene nagE2 is the key to N-acetylglucosamine sensing and utilization in Streptomyces coelicolor and is subject to multi-level control. Mol Microbiol 75: 1133-1144. doi: 10.1111/j.1365-2958.2009.07020.x PMID: 20487300
27. Rigali S, Nothaft H, Noens EE, Schlicht M, Colson S, Muller M, et al. (2006) The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links Nacetylglucosamine metabolism to the control of development. Mol Microbiol 61: 1237-1251. PMID: 16925557
28. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, et al. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9: 670-675. doi: 10.1038/embor.2008.83 PMID: 18511939
29. Rigali S, Schlicht M, Hoskisson P, Nothaft H, Merzbacher M, Joris B, et al. (2004) Extending the classification of bacterial transcription factors beyond the helix-turn-helix motif as an alternative approach to discover new cis/trans relationships. Nucleic Acids Res 32: 3418-3426. PMID: 15247334
30. Swiatek MA, Tenconi E, Rigali S, van Wezel GP (2012) Functional analysis of the N-acetylglucosamine metabolic genes of Streptomyces coelicolor and role in the control of development and antibiotic production. J Bacteriol 194: 1136-1144. doi: 10.1128/JB.06370-11 PMID: 22194457
31. Colson S, Stephan J, Hertrich T, Saito A, van Wezel GP, Titgemeyer F, et al. (2007) Conserved cisacting elements upstream of genes composing the chitinolytic system of streptomycetes are DasR-responsive elements. J Mol Microbiol Biotechnol 12: 60-66. PMID: 17183212
32. Craig M, Lambert S, Jourdan S, Tenconi E, Colson S, Maciejewska M, et al. (2012) Unsuspected control of siderophore production by N-acetylglucosamine in streptomycetes. Env Microbiol Rep.
33. Nazari B, Kobayashi M, Saito A, Hassaninasab A, Miyashita K, Fujii T (2012) Chitin-induced gene expression involved in secondary metabolic pathways in Streptomyces coelicolor A3(2) grown in soil. Appl Environ Microbiol 79: 707-713. doi: 10.1128/AEM.02217-12 PMID: 23124229
34. Hiard S, Maree R, Colson S, Hoskisson PA, Titgemeyer F, van Wezel GP, et al. (2007) PREDetector: a new tool to identify regulatory elements in bacterial genomes. Biochem Biophys Res Commun 357: 861-864. PMID: 17451648
35. Swiercz JP, Hindra, Bobek J, Haiser HJ, Di Berardo C, Tjaden B, et al. (2008) Small non-coding RNAs in Streptomyces coelicolor. Nucleic Acids Res 36: 7240-7251. doi: 10.1093/nar/gkn898 PMID: 19008244
36. Vockenhuber MP, Suess B (2012) Streptomyces coelicolor sRNA scr5239 inhibits agarase expression by direct base pairing to the dagA coding region. Microbiology 158: 424-435. doi: 10.1099/mic.0.054205-0 PMID: 22075028
37. van Wezel GP, Vijgenboom E, Bosch L (1991) A comparative study of the ribosomal RNA operons of Streptomyces coelicolor A3(2) and sequence analysis of rrnA. Nucleic Acids Res 19: 4399-4403. PMID: 1715981
38. Bucca G, Laing E, Mersinias V, Allenby N, Hurd D, Holdstock J, et al. (2009) Development and application of versatile high density microarrays for genome-wide analysis of Streptomyces coelicolor: characterization of the HspR regulon. Genome Biol 10: R5. doi: 10.1186/gb-2009-10-1-r5 PMID: 19146703
39. Pawlik K, Kotowska M, Chater KF, Kuczek K, Takano E (2007) A cryptic type I polyketide synthase (cpk) gene cluster in Streptomyces coelicolor A3(2). Arch Microbiol 187: 87-99. PMID: 17009021
40. Uguru GC, Stephens KE, Stead JA, Towle JE, Baumberg S, McDowall KJ (2005) Transcriptional activation of the pathway-specific regulator of the actinorhodin biosynthetic genes in Streptomyces coelicolor. Mol Microbiol 58: 131-150. PMID: 16164554
41. Colson S, van Wezel GP, Craig M, Noens EE, Nothaft H, Mommaas AM, et al. (2008) The chitobiose-binding protein, DasA, acts as a link between chitin utilization and morphogenesis in Streptomyces coelicolor. Microbiology 154: 373-382. doi: 10.1099/mic.0.2007/011940-0 PMID: 18227241
42. Saito A, Shinya T, Miyamoto K, Yokoyama T, Kaku H, Minami E, et al. (2007) The dasABC gene cluster, adjacent to dasR, encodes a novel ABC transporter for the uptake of N,N'-diacetylchitobiose in Streptomyces coelicolor A3(2). Appl Environ Microbiol 73: 3000-3008. PMID: 17351098
43. Wang F, Xiao X, Saito A, Schrempf H (2002) Streptomyces olivaceoviridis possesses a phosphotransferase system that mediates specific, phosphoenolpyruvate-dependent uptake of N-acetylglucosamine. Mol Genet Genomics 268: 344-351. PMID: 12436256
44. Hsiao NH, Soding J, Linke D, Lange C, Hertweck C, Wohlleben W, et al. (2007) ScbA from Streptomyces coelicolor A3(2) has homology to fatty acid synthases and is able to synthesize gamma-butyrolactones. Microbiology 153: 1394-1404. PMID: 17464053
45. Li W, Ying X, Guo Y, Yu Z, Zhou X, Deng Z, et al. (2006) Identification of a gene negatively affecting antibiotic production and morphological differentiation in Streptomyces coelicolor A3(2). J Bacteriol 188: 8368-8375. PMID: 17041057
46. Zhang L, Li WC, Zhao CH, Chater KF, Tao MF (2007) NsdB, a TPR-like-domain-containing protein negatively affecting production of antibiotics in Streptomyces coelicolor A3 (2). Wei Sheng Wu Xue Bao 47: 849-854. PMID: 18062261
47. Wang LY, Li ST, Li Y (2003) Identification and characterization of a new exopolysaccharide biosynthesis gene cluster from Streptomyces. FEMS Microbiol Lett 220: 21-27. PMID: 12644223
48. Nodwell JR, Losick R (1998) Purification of an extracellular signaling molecule involved in production of aerial mycelium by Streptomyces coelicolor. J Bacteriol 180: 1334-1337. PMID: 9495776
49. Nodwell JR, McGovern K, Losick R (1996) An oligopeptide permease responsible for the import of an extracellular signal governing aerial mycelium formation in Streptomyces coelicolor. Mol Microbiol 22: 881-893. PMID: 8971710
50. Bibb MJ, Molle V, Buttner MJ (2000) sigma(BldN), an extracytoplasmic function RNA polymerase sigma factor required for aerial mycelium formation in Streptomyces coelicolor A3(2). J Bacteriol 182: 4606-4616. PMID: 10913095
51. Derouaux A, Halici S, Nothaft H, Neutelings T, Moutzourelis G, Dusart J, et al. (2004) Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. J Bacteriol 186: 1893-1897. PMID: 14996821
52. Piette A, Derouaux A, Gerkens P, Noens EE, Mazzucchelli G, Vion S, et al. (2005) From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant. J Proteome Res 4: 1699-1708. PMID: 16212423
53. Fowler-Goldsworthy K, Gust B, Mouz S, Chandra G, Findlay KC, Chater KF (2011) The actinobacteria-specific gene wblA controls major developmental transitions in Streptomyces coelicolor A3(2). Microbiology 157: 1312-1328. doi: 10.1099/mic.0.047555-0 PMID: 21330440
54. Claessen D, de Jong W, Dijkhuizen L, Wösten HA (2006) Regulation of Streptomyces development: reach for the sky! Trends Microbiol 14: 313-319. PMID: 16759865
55. Wösten HA, Willey JM (2000) Surface-active proteins enable microbial aerial hyphae to grow into the air. Microbiology 146: 767-773. PMID: 10784034
56. Willey J, Santamaria R, Guijarro J, Geistlich M, Losick R (1991) Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor. Cell 65: 641-650. PMID: 2032288
57. Rigali S, Derouaux A, Giannotta F, Dusart J (2002) Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J Biol Chem 277: 12507-12515. PMID: 11756427
58. Hodgson DA (2000) Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42: 47-238. PMID: 10907551
59. Grainger DC, Hurd D, Harrison M, Holdstock J, Busby SJ (2005) Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci U S A: 17693-17698. PMID: 16301522
60. Wade JT, Reppas NB, Church GM, Struhl K (2005) Genomic analysis of LexA binding reveals the permissive nature of the Escherichia coli genome and identifies unconventional target sites. Genes Dev 19: 2619-2630. PMID: 16264194
61. Gao Z, Li F, Wu G, Zhu Y, Yu T, Yu S (2012) Roles of hinge region, loops 3 and 4 in the activation of Escherichia coli cyclic AMP receptor protein. Int J Biol Macromol 50: 1-6. doi: 10.1016/j.ijbiomac.2011.08.016 PMID: 21889533
62. Grainger DC, Aiba H, Hurd D, Browning DF, Busby SJ (2007) Transcription factor distribution in Escherichia coli: studies with FNR protein. Nucleic Acids Res 35: 269-278. PMID: 17164287
63. Molle V, Fujita M, Jensen ST, Eichenberger P, Gonzalez-Pastor JE, Liu JS, et al. (2003) The Spo0A regulon of Bacillus subtilis. Mol Microbiol 50: 1683-1701. PMID: 14651647
64. Laub MT, Chen SL, Shapiro L, McAdams HH (2002) Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci U S A 99: 4632-4637. PMID: 11930012
65. Gao C, Hindra, Mulder D, Yin C, Elliot MA (2012) Crp is a global regulator of antibiotic production in Streptomyces. MBio 3: 00407-00412.
66. Pullan ST, Chandra G, Bibb MJ, Merrick M (2011) Genome-wide analysis of the role of GlnR in Streptomyces venezuelae provides new insights into global nitrogen regulation in actinomycetes. BMC Genomics 12: 175. doi: 10.1186/1471-2164-12-175 PMID: 21463507
67. Allenby NE, Laing E, Bucca G, Kierzek AM, Smith CP (2012) Diverse control of metabolism and other cellular processes in Streptomyces coelicolor by the PhoP transcription factor: genome-wide identification of in vivo targets. Nucleic Acids Res 40:: 9543-9556. doi: 10.1093/nar/gks766 PMID: 22904076
68. Higo A, Hara H, Horinouchi S, Ohnishi Y (2012) Genome-wide distribution of AdpA, a global regulator for secondary metabolism and morphological differentiation in Streptomyces, revealed the extent and complexity of the AdpA regulatory network. DNA Res 19: 259-273. doi: 10.1093/dnares/dss010 PMID: 22449632
69. Wade JT, Belyaeva TA, Hyde EI, Busby SJ (2001) A simple mechanism for co-dependence on two activators at an Escherichia coli promoter. EMBO J 20: 7160-7167. PMID: 11742992
70. Bertram R, Rigali S, Wood N, Lulko AT, Kuipers OP, Titgemeyer F (2011) Regulon of the N-acetylglucosamine utilization regulator NagR in Bacillus subtilis. J Bacteriol 193: 3525-3536. doi: 10.1128/JB.00264-11 PMID: 21602348
71. Jakimowicz D, van Wezel GP (2012) Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol Microbiol 85: 393-404. doi: 10.1111/j.1365-2958.2012.08107.x PMID: 22646484
72. Noens EE, Mersinias V, Willemse J, Traag BA, Laing E, Chater KF, et al. (2007) Loss of the controlled localization of growth stage-specific cell-wall synthesis pleiotropically affects developmental gene expression in an ssgA mutant of Streptomyces coelicolor. Mol Microbiol 64: 1244-1259. PMID: 17542918
73. den Hengst CD, Tran NT, Bibb MJ, Chandra G, Leskiw BK, Buttner MJ (2010) Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol Microbiol 78: 361-379. PMID: 20979333
74. Nazari B, Saito A, Kobayashi M, Miyashita K, Wang Y, Fujii T (2011) High expression levels of chitinase genes in Streptomyces coelicolor A3(2) grown in soil. FEMS Microbiol Ecol 77: 623-635. doi: 10.1111/j.1574-6941.2011.01143.x PMID: 21631548
75. Chakraburtty R, Bibb M (1997) The ppGpp synthetase gene (relA) of Streptomyces coelicolor A3(2) plays a conditional role in antibiotic production and morphological differentiation. J Bacteriol 179: 5854-5861. PMID: 9294445
76. Floriano B, Bibb M (1996) afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 21: 385-396. PMID: 8858592
77. Gramajo HC, Takano E, Bibb MJ (1993) Stationary-phase production of the antibiotic actinorhodin in Streptomyces coelicolor A3(2) is transcriptionally regulated. Mol Microbiol 7: 837-845. PMID: 7683365
78. Liu G, Chater KF, Chandra G, Niu G, Tan H (2013) Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev 77: 112-143. doi: 10.1128/MMBR.00054-12 PMID: 23471619
79. Altermann E, Klaenhammer TR (2005) PathwayVoyager: pathway mapping using the Kyoto Encyclopedia of Genes and Genomes (KEGG) database. BMC Genomics 6: 60. PMID: 15869710
80. Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21: 3787-3793. PMID: 15817693
81. Bibb MJ, Domonkos A, Chandra G, Buttner MJ (2012) Expression of the chaplin and rodlin hydrophobic sheath proteins in Streptomyces venezuelae is controlled by sigma(BldN) and a cognate anti-sigma factor, RsbN. Mol Microbiol 84: 1033-1049. doi: 10.1111/j.1365-2958.2012.08070.x PMID: 22582857
82. Sambrook J, Fritsch E.F., and Maniatis T. (1989) Molecular cloning: a laboratory manual. Cold Spring harbor, NY: Cold Spring Harbor laboratory press.
83. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces genetics. The John Innes Foundation, Norwich, United Kingdom.
84. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, Schoner BE (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43-49. PMID: 1628843
85. Mahr K, van Wezel GP, Svensson C, Krengel U, Bibb MJ, Titgemeyer F (2000) Glucose kinase of Streptomyces coelicolor A3(2): large-scale purification and biochemical analysis. Antonie Van Leeuwenhoek 78: 253-261. PMID: 11386347
86. Bucca G, Brassington AM, Hotchkiss G, Mersinias V, Smith CP (2003) Negative feedback regulation of dnaK, clpB and lon expression by the DnaK chaperone machine in Streptomyces coelicolor, identified by transcriptome and in vivo DnaK-depletion analysis. Mol Microbiol 50: 153-166. PMID: 14507371
87. Smyth GK, Speed T (2003) Normalization of cDNA microarray data. Methods 31: 265-273. PMID: 14597310
88. Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573: 83-92. PMID: 15327980
89. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, Chory J (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827. PMID: 16982708
90. Laing E, Smith CP (2010) RankProdIt: A web-interactive Rank Products analysis tool. BMC Res Notes 3: 221. doi: 10.1186/1756-0500-3-221 PMID: 20691047
91. Hesketh A, Bucca G, Laing E, Flett F, Hotchkiss G, Smith CP, et al. (2007) New pleiotropic effects of eliminating a rare tRNA from Streptomyces coelicolor, revealed by combined proteomic and transcriptomic analysis of liquid cultures. BMC Genomics 8: 261. PMID: 17678549