Cited by 306Bacterial Genetics and BiotechnologyBiochemical and Molecular ResearchMicrobial Metabolic Engineering and Bioproduction

The DOI matches its Crossref record; 96 of the 96 references it cites were found in a registry or an index.

Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis

Open access

Eymann, Christine, Homuth, Georg, Scharf, Christian, Hecker, Michael·2002·Journal of Bacteriology

DOI 10.1128/jb.184.9.2500-2520.2002PMC PMC134987

Open this paper in CoChat — free account

Abstract

The stringent response in Bacillus subtilis was characterized by using proteome and transcriptome approaches. Comparison of protein synthesis patterns of wild-type and relA mutant cells cultivated under conditions which provoke the stringent response revealed significant differences. According to their altered synthesis patterns in response to dl-norvaline, proteins were assigned to four distinct classes: (i) negative stringent control, i.e., strongly decreased protein synthesis in the wild type but not in the relA mutant (e.g., r-proteins); (ii) positive stringent control, i.e., induction of protein synthesis in the wild type only (e.g., YvyD and LeuD); (iii) proteins that were induced independently of RelA (e.g., YjcI); and (iv) proteins downregulated independently of RelA (e.g., glycolytic enzymes). Transcriptome studies based on DNA macroarray techniques were used to complement the proteome data, resulting in comparable induction and repression patterns of almost all corresponding genes. However, a comparison of both approaches revealed that only a subset of RelA-dependent genes or proteins was detectable by proteomics, demonstrating that the transcriptome approach allows a more comprehensive global gene expression profile analysis. The present study presents the first comprehensive description of the stringent response of a bacterial species and an almost complete map of protein-encoding genes affected by (p)ppGpp. The negative stringent control concerns reactions typical of growth and reproduction (ribosome synthesis, DNA synthesis, cell wall synthesis, etc.). Negatively controlled unknown y-genes may also code for proteins with a specific function during growth and reproduction (e.g., YlaG). On the other hand, many genes are induced in a RelA-dependent manner, including genes coding for already-known and as-yet-unknown proteins. A passive model is preferred to explain this positive control relying on the redistribution of the RNA polymerase under the influence of (p)ppGpp.

Integrity signals

Registry

Crossref · 10.1128/jb.184.9.2500-2520.2002

Cites

96 of 96 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Escherichia coli and Salmonella :cellular and molecular biology
Neidhardt, F. C. (1996) · ASM Press eBooks · Cited by 8,197
The complete genome sequence of the gram-positive bacterium Bacillus subtilis.
Kunst, F., Ogasawara, N., Moszer, I., Albertini, A. M., Alloni, G., Azevedo, V., Bertero, M. G., Bessières, P., Bolotin, A., Borchert, S., et al. (1997) · Nature · doi:10.1038/36786 · Cited by 3,679
Bacterial Stress Responses
Storz, G., & Hengge, R. (2010) · ASM Press eBooks · doi:10.1128/9781555816841 · Cited by 1,107
The stringent response
Cashel, M. (1996) · Medical Entomology and Zoology · Cited by 860
Residual guanosine 3‘,5‘-bispyrophosphate synthetic activity of relA null mutants can be eliminated by spoT null mutations.
Xiao, H., Kálmán, M., Ikehara, K., Zemel, S., Glaser, G., & Cashel, M. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)67694-5 · Cited by 721
Synthesis of the stationary-phase sigma factor sigma s is positively regulated by ppGpp
Gentry, D. R., Hernandez, V. J., Nguyen, L. H., Jensen, D. B., & Cashel, M. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.24.7982-7989.1993 · Cited by 448
Global Analysis of the General Stress Response of Bacillus subtilis
Petersohn, A., Brigulla, M., Haas, S. A., Hoheisel, J. D., Völker, U., & Hecker, M. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.19.5617-5631.2001 · Cited by 433
Self-citation
Getting Newly Synthesized Proteins into Shape
Bukau, B., Deuerling, E., Pfund, C., & Craig, E. A. (2000) · Cell · doi:10.1016/s0092-8674(00)80806-5 · Cited by 428
Transcription Regulation by Initiating NTP Concentration: rRNA Synthesis in Bacteria
Gaál, T., Bartlett, M. S., Ross, W., Turnbough, C. L., & Gourse, R. L. (1997) · Science · doi:10.1126/science.278.5346.2092 · Cited by 367
Revisiting the stringent response, ppGpp and starvation signaling
Chatterji, D., & Ojha, A. K. (2001) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00182-x · Cited by 366

Show all 96 references

Research works printed but not linked: 1

Lopez, J., C. Marks, and E. Freese. 1981. The decrease in guanosine nucleotides initiates the sporulation in Bacillus subtilis.Biochim. Biophys. Acta587:238-252.

Sorted by citations

Pseudomonas aeruginosa Lifestyle: A Paradigm for Adaptation, Survival, and Persistence
Moradali, M. F., Ghods, S., & Rehm, B. H. A. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00039 · Cited by 1,554
Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis
Nicolas, P., Mäder, U., Dervyn, E., Rochat, T., Leduc, A., Pigeonneau, N., Bidnenko, E., Marchadier, E., Hoebeke, M., Aymerich, S., et al. (2012) · Science · doi:10.1126/science.1206848 · Cited by 910
Self-citation
Disease proteomics
Hanash, S. (2003) · Nature · doi:10.1038/nature01514 · Cited by 908
Metabolomics: Current technologies and future trends
Hollywood, K. A., Brison, D. R., & Goodacre, R. (2006) · PROTEOMICS · doi:10.1002/pmic.200600106 · Cited by 609
Metarhizium spp., Cosmopolitan Insect-Pathogenic Fungi: Mycological Aspects
Roberts, D. W., & Leger, R. J. S. (2004) · Advances in applied microbiology · doi:10.1016/s0065-2164(04)54001-7 · Cited by 478
Control of key metabolic intersections in Bacillus subtilis
Sonenshein, A. L. (2007) · Nature Reviews Microbiology · doi:10.1038/nrmicro1772 · Cited by 424
Proteomic Approach to Understanding Antibiotic Action
Bandow, J. E., Brötz, H., Leichert, L. I. O., Labischinski, H., & Hecker, M. (2003) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.47.3.948-955.2003 · Cited by 391
Self-citation
Control of bacterial transcription, translation and replication by (p)ppGpp
Srivatsan, A., & Wang, J. D. (2008) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.02.001 · Cited by 388
Transcription Profiling of the Stringent Response in Escherichia coli
Durfee, T., Hansen, A., Zhi, H., Blattner, F. R., & Jin, D. J. (2007) · Journal of Bacteriology · doi:10.1128/jb.01092-07 · Cited by 374
CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria
Sonenshein, A. L. (2005) · Current Opinion in Microbiology · doi:10.1016/j.mib.2005.01.001 · Cited by 361
DNA supercoiling — a global transcriptional regulator for enterobacterial growth?
TRAVERS, A. A., & Muskhelishvili, G. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1088 · Cited by 357
Advances in bacterial promoter recognition and its control by factors that do not bind DNA
Haugen, S. P., Ross, W., & Gourse, R. L. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1912 · Cited by 320
Additional Targets of the Bacillus subtilis Global Regulator CodY Identified by Chromatin Immunoprecipitation and Genome-Wide Transcript Analysis
Molle, V., Nakaura, Y., Shivers, R. P., Yamaguchi, H., Losick, R. M., Fujita, Y., & Sonenshein, A. L. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.6.1911-1922.2003 · Cited by 296
Depiction of metabolome changes in histidine-starved Escherichia coli by CE-TOFMS
Ohashi, Y., Hirayama, A., Ishikawa, T., Nakamura, S., Shimizu, K., Ueno, Y., Tomita, M., & Soga, T. (2007) · Molecular BioSystems · doi:10.1039/b714176a · Cited by 291
Nutritional Control of Elongation of DNA Replication by (p)ppGpp
Wang, J. D., Sanders, G. M., & Grossman, A. D. (2007) · Cell · doi:10.1016/j.cell.2006.12.043 · Cited by 288
Extracellular signals that define distinct and coexisting cell fates inBacillus subtilis
López, D., & Kolter, R. (2009) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2009.00199.x · Cited by 305
Integration of Proteomics and Genomics in Platelets
McRedmond, J. P., Park, S. D., Reilly, D. F., Coppinger, J. A., Maguire, P. B., Shields, D. C., & Fitzgerald, D. J. (2003) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m300063-mcp200 · Cited by 285
The Stringent Response of Staphylococcus aureus and Its Impact on Survival after Phagocytosis through the Induction of Intracellular PSMs Expression
Geiger, T., François, P., Liebeke, M., Fraunholz, M. J., Goerke, C., Krismer, B., Schrenzel, J., Lalk, M., & Wolz, C. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003016 · Cited by 238
Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress
Mostertz, J., Scharf, C., Hecker, M., & Homuth, G. (2004) · Microbiology · doi:10.1099/mic.0.26665-0 · Cited by 240
Self-citation
Integrated metatranscriptomic and metagenomic analyses of stratified microbial assemblages in the open ocean
Shi, Y., Tyson, G. W., Eppley, J. M., & DeLong, E. F. (2010) · The ISME Journal · doi:10.1038/ismej.2010.189 · Cited by 226
Transcriptional profiling of gene expression in response to glucose in Bacillus subtilis: regulation of the central metabolic pathways
Blencke, H., Homuth, G., Ludwig, H., Mäder, U., Hecker, M., & Stülke, J. (2003) · Metabolic Engineering · doi:10.1016/s1096-7176(03)00009-0 · Cited by 227
Self-citation
Physiological and Transcriptional Response ofLactobacillus caseiATCC 334 to Acid Stress
Broadbent, J. R., Larsen, R. L., Deibel, V., & Steele, J. L. (2010) · Journal of Bacteriology · doi:10.1128/jb.01618-09 · Cited by 215
Bacterial Cold Shock Responses
Weber, M. H. W., & Marahiel, M. A. (2003) · Science Progress · doi:10.3184/003685003783238707 · Cited by 210
The essential YycFG two‐component system controls cell wall metabolism in Bacillus subtilis
Bisicchia, P., Noone, D., Lioliou, E. E., Howell, A., Quigley, S., Jensen, T. S., Jarmer, H. Ø., & Devine, K. M. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.05782.x · Cited by 202
Megadalton Complexes in the Chloroplast Stroma of Arabidopsis thaliana Characterized by Size Exclusion Chromatography, Mass Spectrometry, and Hierarchical Clustering
Olinares, P. D. B., Ponnala, L., & van Wijk, K. J. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m000038-mcp201 · Cited by 202
Transcriptional regulation is insufficient to explain substrate-induced flux changes in Bacillus subtilis
Chubukov, V., Uhr, M., Le Chat, L., Kleijn, R. J., Jules, M., Link, H., Aymerich, S., Stelling, J., & Sauer, U. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.66 · Cited by 191
Two Small (p)ppGpp Synthases in Staphylococcus aureus Mediate Tolerance against Cell Envelope Stress Conditions
Geiger, T., Kästle, B., Gratani, F. L., Goerke, C., & Wolz, C. (2013) · Journal of Bacteriology · doi:10.1128/jb.01201-13 · Cited by 183
Many Means to a Common End: the Intricacies of (p)ppGpp Metabolism and Its Control of Bacterial Homeostasis
Gaca, A. O., Colomer‐Winter, C., & Lemos, J. A. C. (2015) · Journal of Bacteriology · doi:10.1128/jb.02577-14 · Cited by 195
A Comprehensive Proteomics and Transcriptomics Analysis of Bacillus subtilis Salt Stress Adaptation
Hahne, H., Mäder, U., Otto, A., Bonn, F., Steil, L., Bremer, E., Hecker, M., & Becher, D. (2010) · Journal of Bacteriology · doi:10.1128/jb.01106-09 · Cited by 183
Self-citation
Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis
Otto, A., Bernhardt, J., Meyer, H., Schaffer, M., Herbst, F., Siebourg‐Polster, J., Mäder, U., Lalk, M., Hecker, M., & Becher, D. (2010) · Nature Communications · doi:10.1038/ncomms1137 · Cited by 190
Self-citation
Microarray expression profiling: capturing a genome‐wide portrait of the transcriptome
Conway, T., Gary, K., & Schoolnik (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03338.x · Cited by 181
Global Characterization of Disulfide Stress inBacillus subtilis
Leichert, L. I. O., Scharf, C., & Hecker, M. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.6.1967-1975.2003 · Cited by 182
Self-citation
The σB regulon in Staphylococcus aureus and its regulation
Pané‐Farré, J., Jonas, B., Förstner, K. U., Engelmann, S., & Hecker, M. (2006) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.11.011 · Cited by 175
Self-citation
Genes controlled by the essential YycG/YycF two‐component system of Bacillus subtilis revealed through a novel hybrid regulator approach
Howell, A., Dubrac, S., Andersen, K. K., Noone, D., Fert, J., Msadek, T., & Devine, K. M. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03661.x · Cited by 165
Transcriptional profiling of Helicobacter pylori Fur- and iron-regulated gene expression
Ernst, F. D., Bereswill, S., Waidner, B., Stoof, J., Mäder, U., Kusters, J. G., Kuipers, E. J., Kist, M., van Vliet, A. H. M., & Homuth, G. (2005) · Microbiology · doi:10.1099/mic.0.27404-0 · Cited by 160
Self-citation
The global role of ppGpp synthesis in morphological differentiation and antibiotic production in Streptomyces coelicolor A3(2)
Hesketh, A. R., chen, W., Ryding, J., Chang, S. H., & Bibb, M. J. (2007) · Genome biology · doi:10.1186/gb-2007-8-8-r161 · Cited by 159
Bacillus subtilis functional genomics: genome-wide analysis of the DegS-DegU regulon by transcriptomics and proteomics
Mäder, U., Antelmann, H., Buder, T., Dahl, M. K., Hecker, M., & Homuth, G. (2002) · Molecular Genetics and Genomics · doi:10.1007/s00438-002-0774-2 · Cited by 149
Self-citation
Role of the (p)ppGpp Synthase RSH, a RelA/SpoT Homolog, in Stringent Response and Virulence ofStaphylococcus aureus
Geiger, T., Goerke, C., Fritz, M., Schäfer, T., Ohlsen, K., Liebeke, M., Lalk, M., & Wolz, C. (2010) · Infection and Immunity · doi:10.1128/iai.01439-09 · Cited by 146
Indicators of milk and beef quality
Cassandro, M., GALLO, L., Carnier, P., Bittante, G., Povinelli, M., Marcomin, D., R, D. Z., & Valorz, C. (2005) · Wageningen Academic Publishers eBooks · doi:10.3920/978-90-8686-537-6 · Cited by 147
Transcriptomic and Proteomic Characterization of the Fur Modulon in the Metal-Reducing Bacterium Shewanella oneidensis
Wan, X., VerBerkmoes, N. C., McCue, L. A., Stanek, D., Connelly, H. M., Hauser, L., Wu, L., Liu, X., Yan, T., Leaphart, A. B., et al. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.24.8385-8400.2004 · Cited by 132
Toxicogenomics of bromobenzene hepatotoxicity: a combined transcriptomics and proteomics approach
Heijne, W. H. M., Stierum, R. H., Slijper, M., van BLADEREN, P. J., & van Ommen, B. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(02)01613-1 · Cited by 130
Bacillus subtilis During Feast and Famine: Visualization of the Overall Regulation of Protein Synthesis During Glucose Starvation by Proteome Analysis
Bernhardt, J., Weibezahn, J., Scharf, C., & Hecker, M. (2003) · Genome Research · doi:10.1101/gr.905003 · Cited by 125
Self-citation
A metazoan ortholog of SpoT hydrolyzes ppGpp and functions in starvation responses
Sun, D., Lee, G., Lee, J. H., Kim, H. Y., Rhee, H., Park, S., Kim, K. J., Kim, Y., Kim, B. Y., Hong, J.-I., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1906 · Cited by 125
Global Transcriptional Response of Bacillus subtilis to Treatment with Subinhibitory Concentrations of Antibiotics That Inhibit Protein Synthesis
Lin, J. T., Connelly, M. B., Amolo, C., Otani, S., & Yaver, D. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.5.1915-1926.2005 · Cited by 121
The identity of the transcription +1 position is crucial for changes in gene expression in response to amino acid starvation in Bacillus subtilis
Krásný, L., Tišerová, H., Jonák, J., Rejman, D., & Šanderová, H. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06256.x · Cited by 117
Metaproteomic analysis of Chesapeake Bay microbial communities
Kan, J., Hanson, T. E., Ginter, J. M., Wang, K., & Chen, F. (2005) · Saline Systems · doi:10.1186/1746-1448-1-7 · Cited by 116
Proteomic analysis of antioxidant strategies of Staphylococcus aureus: Diverse responses to different oxidants
Wolf, C., Hochgräfe, F., Kusch, H., Albrecht, D., Hecker, M., & Engelmann, S. (2008) · PROTEOMICS · doi:10.1002/pmic.200701062 · Cited by 115
Self-citation
mRNA processing by RNases J1 and J2 affects Bacillus subtilis gene expression on a global scale
Mäder, U., Zig, L., Kretschmer, J., Homuth, G., & Putzer, H. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06400.x · Cited by 114
Self-citation
GTP Dysregulation in Bacillus subtilis Cells Lacking (p)ppGpp Results in Phenotypic Amino Acid Auxotrophy and Failure To Adapt to Nutrient Downshift and Regulate Biosynthesis Genes
Kriel, A., Brinsmade, S. R., Tse, J. L., Tehranchi, A. K., Bittner, A. N., Sonenshein, A. L., & Wang, J. D. (2013) · Journal of Bacteriology · doi:10.1128/jb.00918-13 · Cited by 109
Effectiveness and limitation of two-dimensional gel electrophoresis in bacterial membrane protein proteomics and perspectives
Bunai, K., & Yamane, K. (2004) · Journal of Chromatography B · doi:10.1016/j.jchromb.2004.08.030 · Cited by 109
Elaborate transcription regulation of the Bacillus subtilis ilv‐leu operon involved in the biosynthesis of branched‐chain amino acids through global regulators of CcpA, CodY and TnrA
Tojo, S., Satomura, T., Morisaki, K., Deutscher, J., Hirooka, K., & Fujita, Y. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04635.x · Cited by 108
Regulation of the stringent response is the essential function of the conserved bacterial G protein CgtA in Vibrio cholerae
Raskin, D. M., Judson, N., & Mekalanos, J. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611650104 · Cited by 108
Adaptation of B acillus subtilis carbon core metabolism to simultaneous nutrient limitation and osmotic challenge: a multi‐omics perspective
Kohlstedt, M., Sappa, P. K., Meyer, H., Maaß, S., Zaprasis, A., Hoffmann, T., Becker, J., Steil, L., Hecker, M., van Dijl, J. M., et al. (2014) · Environmental Microbiology · doi:10.1111/1462-2920.12438 · Cited by 109
Self-citation
Clp-Dependent Proteolysis Down-Regulates Central Metabolic Pathways in Glucose-Starved Bacillus subtilis
Gerth, U., Kock, H., Küsters, I., Michalik, S., Switzer, R. L., & Hecker, M. (2007) · Journal of Bacteriology · doi:10.1128/jb.01233-07 · Cited by 106
Self-citation
Superoxide dismutase activity confers (p)ppGpp-mediated antibiotic tolerance to stationary-phase Pseudomonas aeruginosa
Martins, D., McKay, G. A., Sampathkumar, G., Khakimova, M., English, A. M., & Nguyen, D. M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1804525115 · Cited by 105
The repressor and co‐activator HsfB1 regulates the major heat stress transcription factors in tomato
Fragkostefanakis, S., Simm, S., El‐Shershaby, A., Hu, Y., Bublak, D., Mesihović, A., Darm, K., Mishra, S. K., Tschiersch, B., Theres, K., et al. (2018) · Plant Cell & Environment · doi:10.1111/pce.13434 · Cited by 105
Self-citation
Discovering the Mechanism of Action of Novel Antibacterial Agents through Transcriptional Profiling of Conditional Mutants
Freiberg, C., Fischer, H. P., & Brunner, N. A. (2005) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.2.749-759.2005 · Cited by 105
Psychrobacter arcticus 273-4 Uses Resource Efficiency and Molecular Motion Adaptations for Subzero Temperature Growth
Bergholz, P. W., Bakermans, C., & Tiedje, J. M. (2009) · Journal of Bacteriology · doi:10.1128/jb.01377-08 · Cited by 105
Global Analysis of the Staphylococcus aureus Response to Mupirocin
Reiß, S., Pané‐Farré, J., Fuchs, S., François, P., Liebeke, M., Schrenzel, J., Lindequist, U., Lalk, M., Wolz, C., Hecker, M., et al. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.05363-11 · Cited by 104
Self-citation
Proteomic characterization of the acid tolerance response in Lactococcus lactis MG1363
Budin‐Verneuil, A., Pichereau, V., Auffray, Y., Ehrlich, S. D., & Maguin, E. (2005) · PROTEOMICS · doi:10.1002/pmic.200401327 · Cited by 103
Differential gene expression in response to phenol and catechol reveals different metabolic activities for the degradation of aromatic compounds in Bacillus subtilis
Tam, L. T., Eymann, C., Albrecht, D., Sietmann, R., Schauer, F., Hecker, M., & Antelmann, H. (2006) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01034.x · Cited by 102
Self-citation
Mutation of RNA Polymerase β Subunit ( rpoB ) Promotes hVISA-to-VISA Phenotypic Conversion of Strain Mu3
Matsuo, M., Hishinuma, T., Katayama, Y., Cui, L., Kapi, M., & Hiramatsu, K. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00398-11 · Cited by 100
Linking the nutritional status of Streptococcus pyogenes to alteration of transcriptional gene expression: The action of CodY and RelA
Malke, H., Steiner, K., McShan, W. M., & Ferretti, J. J. (2006) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.11.008 · Cited by 100
Regulation of the central glycolytic genes in Bacillus subtilis: binding of the repressor CggR to its single DNA target sequence is modulated by fructose‐1,6‐bisphosphate
Doan, T., & Aymerich, S. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03404.x · Cited by 100
RNA Polymerase Mutation Activates the Production of a Dormant Antibiotic 3,3′-Neotrehalosadiamine via an Autoinduction Mechanism in Bacillus subtilis
Inaoka, T., Takahashi, K., Yada, H., Yoshida, M., & Ochi, K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m309925200 · Cited by 95
Ribosome Hibernation Facilitates Tolerance of Stationary-Phase Bacteria to Aminoglycosides
McKay, S. L., & Portnoy, D. A. (2015) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01532-15 · Cited by 91
Towards a comprehensive understanding of Bacillus subtilis cell physiology by physiological proteomics
Hecker, M., & Völker, U. (2004) · PROTEOMICS · doi:10.1002/pmic.200401017 · Cited by 93
Self-citation
Folate Acts in E. coli to Accelerate C. elegans Aging Independently of Bacterial Biosynthesis
Virk, B., Jia, J., Maynard, C., Raimundo, A., Lefebvre, J., Richards, S. A., Chetina, N., Liang, Y., Helliwell, N., Cipinska, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.051 · Cited by 91
Transcriptomics, proteomics and interactomics: unique approaches to track the insights of bioremediation
Singh, O. V. (2006) · Briefings in Functional Genomics and Proteomics · doi:10.1093/bfgp/eli006 · Cited by 90
MurAA, catalysing the first committed step in peptidoglycan biosynthesis, is a target of Clp‐dependent proteolysis in Bacillus subtilis
Kock, H., Gerth, U., & Hecker, M. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03875.x · Cited by 88
Self-citation
Proteome analyses of Staphylococcus aureus in growing and non-growing cells: A physiological approach
Köhler, C., Wolff, S., Albrecht, D., Fuchs, S., Becher, D., Büttner, K., Engelmann, S., & Hecker, M. (2005) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2005.08.002 · Cited by 87
Self-citation
Proteome signatures for stress and starvation in Bacillus subtilis as revealed by a 2‐D gel image color coding approach
Tam, L. T., Antelmann, H., Eymann, C., Albrecht, D., Bernhardt, J., & Hecker, M. (2006) · PROTEOMICS · doi:10.1002/pmic.200600100 · Cited by 87
Self-citation
Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp0 mutant of Bacillus subtilis triggers YvyD‐dependent dimerization of ribosome
Tagami, K., Nanamiya, H., Kazo, Y., Maehashi, M., Suzuki, S., Namba, E., Hoshiya, M., Hanai, R., Tozawa, Y., Morimoto, T., et al. (2012) · MicrobiologyOpen · doi:10.1002/mbo3.16 · Cited by 84
The complex logic of stringent response regulation in Caulobacter crescentus: starvation signalling in an oligotrophic environment
Boutte, C. C., & Crosson, S. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07602.x · Cited by 81
Protein CoAlation and antioxidant function of coenzyme A in prokaryotic cells
Tsuchiya, Y., Zhyvoloup, A., Baković, J., Thomas, N., Yu, B. Y. K., Das, S., Orengo, C. A., Newell, C. L., Ward, J. M., Saladino, G., et al. (2018) · Biochemical Journal · doi:10.1042/bcj20180043 · Cited by 87
The impact of transcriptome and proteome analyses on antibiotic drug discovery
Freiberg, C., Brötz‐Oesterhelt, H., & Labischinski, H. (2004) · Current Opinion in Microbiology · doi:10.1016/j.mib.2004.08.010 · Cited by 83
The Stringent Response Determines the Ability of a Commensal Bacterium to Survive Starvation and to Persist in the Gut
Schofield, W. B., Zimmermann‐Kogadeeva, M., Zimmermann, M., Barry, N. A., & Goodman, A. L. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.06.002 · Cited by 81
Zinc-Responsive Regulation of Alternative Ribosomal Protein Genes inStreptomyces coelicolorInvolves Zur and σR
Owen, G. A., Pascoe, B., Kallifidas, D., & Paget, M. S. B. (2007) · Journal of Bacteriology · doi:10.1128/jb.01901-06 · Cited by 82
Genetic Evidence for a Link Between Glycolysis and DNA Replication
Jannière, L., Canceill, D., Suski, C., Kanga, S., Dalmais, B., Lestini, R., Monnier, A.-F., Chapuis, J., Bolotin, A., Алексеевна, Т. М., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000447 · Cited by 85
Roles of relSpn in stringent response, global regulation and virulence of serotype 2 Streptococcus pneumoniae D39
Kazmierczak, K. M., Wayne, K. J., Rechtsteiner, A., & Winkler, M. E. (2009) · Molecular Microbiology · doi:10.1111/j.1365-2958.2009.06669.x · Cited by 80
Stress response regulators identified through genome-wide transcriptome analysis of the (p)ppGpp-dependent response in Rhizobium etli
Vercruysse, M., Fauvart, M., Jans, A., Beullens, S., Braeken, K., Cloots, L., Engelen, K., Kathleen Marchal, D., & Michiels, J. J. (2011) · Genome biology · doi:10.1186/gb-2011-12-2-r17 · Cited by 80
Bacterial proteomics and its role in antibacterial drug discovery
Brötz‐Oesterhelt, H., Bandow, J. E., & Labischinski, H. (2004) · Mass Spectrometry Reviews · doi:10.1002/mas.20030 · Cited by 78
Construction and usage of a onefold‐coverage shotgun DNA microarray to characterize the metabolism of the archaeon Haloferax volcanii
Zaigler, A., Schuster, S. C., & Soppa, J. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03497.x · Cited by 77
New Class of Bacterial Phenylalanyl-tRNA Synthetase Inhibitors with High Potency and Broad-Spectrum Activity
Beyer, D., Kroll, H., Endermann, R., Schiffer, G., Siegel, S., Bauser, M., Pohlmann, J., Brands, M., Ziegelbauer, K. B., Haebich, D., et al. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.48.2.525-532.2004 · Cited by 76
Self-citation
Adaptation ofCorynebacterium glutamicumto Ammonium Limitation: a Global Analysis Using Transcriptome and Proteome Techniques
Silberbach, M., Schäfer, M., Hüser, A. T., Kalinowski, J., Pühler, A., Krämer, R., & Burkovski, A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.5.2391-2402.2005 · Cited by 76
Novel Role of mfd : Effects on Stationary-Phase Mutagenesis in Bacillus subtilis
Ross, C. A., Pybus, C. A., Pedraza‐Reyes, M., Sung, H., Yasbin, R. E., & Robleto, E. A. (2006) · Journal of Bacteriology · doi:10.1128/jb.00980-06 · Cited by 78
Second Messenger Signaling in Bacillus subtilis: Accumulation of Cyclic di-AMP Inhibits Biofilm Formation
Gundlach, J., Rath, H., Herzberg, C., Mäder, U., & Stülke, J. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00804 · Cited by 81
Combined Effect of Improved Cell Yield and Increased Specific Productivity Enhances Recombinant Enzyme Production in Genome-Reduced Bacillus subtilis Strain MGB874
Manabe, K., Kageyama, Y., Morimoto, T., Ozawa, T., Sawada, K., Endo, K., Tohata, M., Ara, K., Ozaki, K., & Ogasawara, N. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.06136-11 · Cited by 74
Transcriptome Analysis of the Progressive Adaptation of Lactococcus lactis to Carbon Starvation
Redon, E., Loubière, P., & Cocaign‐Bousquet, M. (2005) · Journal of Bacteriology · doi:10.1128/jb.187.10.3589-3592.2005 · Cited by 74
The alarmones (p)ppGpp are part of the heat shock response of Bacillus subtilis
Schäfer, H., Beckert, B., Frese, C. K., Steinchen, W., Nuss, A. M., Beckstette, M., Hantke, I., Driller, K., Sudzinová, P., Krásný, L., et al. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008275 · Cited by 70
Transcriptome and Proteome Analysis ofBacillus subtilisGene Expression Modulated by Amino Acid Availability
Mäder, U., Homuth, G., Scharf, C., Büttner, K., Bode, R., & Hecker, M. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.15.4288-4295.2002 · Cited by 72
Self-citation
Comparative transcriptomic analysis of Porphyromonas gingivalisbiofilm and planktonic cells
Lo, A. W. H., Seers, C. A., Boyce, J. D., Dashper, S. G., Slakeski, N., Lissel, J. P., & Reynolds, E. C. (2009) · BMC Microbiology · doi:10.1186/1471-2180-9-18 · Cited by 71
The Evolution of gene regulation research in Lactococcus lactis
Kok, J., van Gijtenbeek, L. A., de Jong, A., van der Meulen, S. B., Solopova, A., & Kuipers, O. P. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux028 · Cited by 70
Approaches for the quantification of protein concentration ratios
Moritz, B., & Meyer, H. E. (2003) · PROTEOMICS · doi:10.1002/pmic.200300581 · Cited by 69
A proteomic view of cell physiology of Bacillus licheniformis
Voigt, B., Schweder, T., Becher, D., Ehrenreich, A., Gottschalk, G., Feesche, J., Maurer, K., & Hecker, M. (2004) · PROTEOMICS · doi:10.1002/pmic.200300684 · Cited by 68
Self-citation
A Defect in Menadione Biosynthesis Induces Global Changes in Gene Expression in Staphylococcus aureus
Köhler, C., von Eiff, C., Liebeke, M., McNamara, P. J., Lalk, M., Proctor, R. A., Hecker, M., & Engelmann, S. (2008) · Journal of Bacteriology · doi:10.1128/jb.00505-08 · Cited by 65
Self-citation
Degradation of ppGpp by Nudix Pyrophosphatase Modulates the Transition of Growth Phase in the Bacterium Thermus thermophilus
Ooga, T., Ohashi, Y., Kuramitsu, S., Koyama, Y., Tomita, M., Soga, T., & Masui, R. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m900582200 · Cited by 66
Transcriptome Analysis of Sorbic Acid-Stressed Bacillus subtilis Reveals a Nutrient Limitation Response and Indicates Plasma Membrane Remodeling
Beek, A. T., Keijser, B. J. F., Boorsma, A., Zakrzewska, A., Orij, R., Smits, G. J., & Brul, S. (2007) · Journal of Bacteriology · doi:10.1128/jb.01516-07 · Cited by 66
Transcriptional Organization and Posttranscriptional Regulation of the Bacillus subtilis Branched-Chain Amino Acid Biosynthesis Genes
Mäder, U., Hennig, S., Hecker, M., & Homuth, G. (2004) · Journal of Bacteriology · doi:10.1128/jb.186.8.2240-2252.2004 · Cited by 66
Self-citation
Genome-wide mRNA profiling in glucose starved Bacillus subtilis cells
Koburger, T., Weibezahn, J., Bernhardt, J., Homuth, G., & Hecker, M. (2005) · Molecular Genetics and Genomics · doi:10.1007/s00438-005-1119-8 · Cited by 65
Self-citation

Authors: Eymann, C., Homuth, G., Scharf, C., & Hecker, M.
Affiliations: Universität Greifswald (DE)
Corresponding author: Hecker, Michael
ORCID: Eymann, Christine
Homuth, Georg
Scharf, Christian
Venue: Journal of Bacteriology
Publisher: American Society for Microbiology
Published: 2002-05
Volume: 184
Issue: 9
Pages: 2500-2520
ISSN: 0021-9193 (ISSN-L)
1098-5530
DOI: 10.1128/jb.184.9.2500-2520.2002
PMC: PMC134987
OpenAlex: W2161630640
Cited by: 306
References: 96
Citations by year: 2026: 10 · 2025: 8 · 2024: 3 · 2023: 5 · 2022: 5 · 2021: 6 · 2020: 16 · 2019: 2 · 2018: 9 · 2017: 12 · 2016: 5 · 2015: 9 · 2014: 12 · 2013: 7 · 2012: 12
FWCI: 12.77
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Journal of Bacteriology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Fonds der Chemischen Industrie
Deutsche Forschungsgemeinschaft
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Molecular Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
Keywords: stringent response, Bacillus subtilis, RelA, (p)ppGpp, protein synthesis regulation, transcriptome, proteome, gene expression profiling, ribosome biogenesis, glycolytic enzymes
MeSH terms: Bacillus subtilis, Bacterial Proteins, Guanosine Tetraphosphate, Ligases, RNA, Messenger, Transcription, Genetic, Protein Biosynthesis, Valine, Electrophoresis, Gel, Two-Dimensional, Gene Expression, Gene Expression Regulation, Bacterial, DNA, Complementary, Regulon, Oligonucleotide Array Sequence Analysis, Proteome

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks