1887

Abstract

Two-component signal transduction systems are essential for many bacteria to maintain homeostasis and adapt to environmental changes. Two-component signal transduction systems typically involve a membrane-bound histidine kinase that senses stimuli, autophosphorylates in the transmitter region and then transfers the phosphoryl group to the receiver domain of a cytoplasmic response regulator that mediates appropriate changes in bacterial physiology. Although usually found on distinct proteins, the transmitter and receiver modules are sometimes fused into a so-called hybrid histidine kinase (HyHK). Such structure results in multiple phosphate transfers that are believed to provide extra-fine-tuning mechanisms and more regulatory checkpoints than classical phosphotransfers. HyHK-based regulation may be crucial for finely tuning gene expression in a heterogeneous environment such as the rhizosphere, where intricate plant–bacteria interactions occur. In this review, we focus on roles fulfilled by bacterial HyHKs in plant-associated bacteria, providing recent findings on the mechanistic of their signalling properties. Recent insights into understanding additive regulatory properties fulfilled by the tethered receiver domain of HyHKs are also addressed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000370
2016-10-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/10/1715.html?itemId=/content/journal/micro/10.1099/mic.0.000370&mimeType=html&fmt=ahah

References

  1. Alexandre G., Greer S. E., Zhulin I. B..( 2000;). Energy taxis is the dominant behavior in Azospirillum brasilense. . J Bacteriol 182: 6042–6048. [CrossRef] [PubMed]
    [Google Scholar]
  2. Alexandre G., Greer-Phillips S., Zhulin I. B..( 2004;). Ecological role of energy taxis in microorganisms. . FEMS Microbiol Rev 28: 113–126. [CrossRef] [PubMed]
    [Google Scholar]
  3. An S. Q., Allan J. H., McCarthy Y., Febrer M., Dow J. M., Ryan R. P..( 2014;). The PAS domain-containing histidine kinase RpfS is a second sensor for the diffusible signal factor of Xanthomonas campestris. . Mol Microbiol 92: 586–597. [CrossRef] [PubMed]
    [Google Scholar]
  4. An S. Q., Febrer M., McCarthy Y., Tang D. J., Clissold L., Kaithakottil G., Swarbreck D., Tang J. L., Rogers J. et al.( 2013;). High-resolution transcriptional analysis of the regulatory influence of cell-to-cell signalling reveals novel genes that contribute to Xanthomonas phytopathogenesis. . Mol Microbiol 88: 1058–1069. [CrossRef] [PubMed]
    [Google Scholar]
  5. Andresen L., Kõiv V., Alamäe T., Mäe A..( 2007;). The Rcs phosphorelay modulates the expression of plant cell wall degrading enzymes and virulence in Pectobacterium carotovorum ssp. carotovorum. . FEMS Microbiol Lett 273: 229–238. [CrossRef] [PubMed]
    [Google Scholar]
  6. Andresen L., Sala E., Kõiv V., Mäe A..( 2010;). A role for the Rcs phosphorelay in regulating expression of plant cell wall degrading enzymes in Pectobacterium carotovorum subsp. carotovorum. . Microbiology 156: 1323–1334. [CrossRef] [PubMed]
    [Google Scholar]
  7. Appleby J. L., Parkinson J. S., Bourret R. B..( 1996;). Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. . Cell 86: 845–848. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bais H. P., Weir T. L., Perry L. G., Gilroy S., Vivanco J. M..( 2006;). The role of root exudates in rhizosphere interactions with plants and other organisms. . Annu Rev Plant Biol 57: 233–266. [CrossRef] [PubMed]
    [Google Scholar]
  9. Barber C. E., Tang J. L., Feng J. X., Pan M. Q., Wilson T. J., Slater H., Dow J. M., Williams P., Daniels M. J..( 1997;). A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. . Mol Microbiol 24: 555–566. [CrossRef] [PubMed]
    [Google Scholar]
  10. Biondi E. G., Skerker J. M., Arif M., Prasol M. S., Perchuk B. S., Laub M. T..( 2006;). A phosphorelay system controls stalk biogenesis during cell cycle progression in Caulobacter crescentus. . Mol Microbiol 59: 386–401. [CrossRef] [PubMed]
    [Google Scholar]
  11. Bobik C., Meilhoc E., Batut J..( 2006;). FixJ: a major regulator of the oxygen limitation response and late symbiotic functions of Sinorhizobium meliloti. . J Bacteriol 188: 4890–4902. [CrossRef] [PubMed]
    [Google Scholar]
  12. Boesten B., Priefer U. B..( 2004;). The C-terminal receiver domain of the Rhizobium leguminosarum bv. viciae FixL protein is required for free-living microaerobic induction of the fnrN promoter. . Microbiology 150: 3703–3713. [CrossRef] [PubMed]
    [Google Scholar]
  13. Bontemps-Gallo S., Madec E., Dondeyne J., Delrue B., Robbe-Masselot C., Vidal O., Prouvost A. F., Boussemart G., Bohin J. P., Lacroix J. M..( 2013;). Concentration of osmoregulated periplasmic glucans (OPGs) modulates the activation level of the RcsCD RcsB phosphorelay in the phytopathogen bacteria Dickeya dadantii. . Environ Microbiol 15: 881–894. [CrossRef] [PubMed]
    [Google Scholar]
  14. Borland S., Oudart A., Prigent-Combaret C., Brochier-Armanet C., Wisniewski-Dyé F..( 2015;). Genome-wide survey of two-component signal transduction systems in the plant growth-promoting bacterium Azospirillum. . BMC Genomics 16: 833. [CrossRef] [PubMed]
    [Google Scholar]
  15. Bouchart F., Boussemart G., Prouvost A. F., Cogez V., Madec E., Vidal O., Delrue B., Bohin J. P., Lacroix J. M..( 2010;). The virulence of a Dickeya dadantii 3937 mutant devoid of osmoregulated periplasmic glucans is restored by inactivation of the RcsCD-RcsB phosphorelay. . J Bacteriol 192: 3484–3490. [CrossRef] [PubMed]
    [Google Scholar]
  16. Brencic A., Winans S. C..( 2005;). Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. . Microbiol Mol Biol Rev 69: 155–194. [CrossRef] [PubMed]
    [Google Scholar]
  17. Buelow D. R., Raivio T. L..( 2010;). Three (and more) component regulatory systems – auxiliary regulators of bacterial histidine kinases. . Mol Microbiol 75: 547–566. [CrossRef] [PubMed]
    [Google Scholar]
  18. Burbulys D., Trach K. A., Hoch J. A..( 1991;). Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. . Cell 64: 545–552. [CrossRef] [PubMed]
    [Google Scholar]
  19. Burke A. K., Duong D. A., Jensen R. V., Stevens A. M..( 2015;). Analyzing the transcriptomes of two quorum-sensing controlled transcription factors, rcsa and lrha, important for pantoea stewartii virulence. . PLoS One 10:,e0145358. [CrossRef] [PubMed]
    [Google Scholar]
  20. Carlier A. L., von Bodman S. B..( 2006;). The rcsA promoter of Pantoea stewartii subsp. stewartii features a low-level constitutive promoter and an EsaR quorum-sensing-regulated promoter. . J Bacteriol 188: 4581–4584. [CrossRef] [PubMed]
    [Google Scholar]
  21. Castanié-Cornet M. P., Cam K., Jacq A..( 2006;). RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli. . J Bacteriol 188: 4264–4270. [CrossRef] [PubMed]
    [Google Scholar]
  22. Chang C. H., Zhu J., Winans S. C..( 1996;). Pleiotropic phenotypes caused by genetic ablation of the receiver module of the Agrobacterium tumefaciens VirA protein. . J Bacteriol 178: 4710–4716.[PubMed]
    [Google Scholar]
  23. Chatterjee S., Wistrom C., Lindow S. E..( 2008;). A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. . Proc Natl Acad Sci U S A 105: 2670–2675. [CrossRef] [PubMed]
    [Google Scholar]
  24. Cheng Z., He Y. W., Lim S. C., Qamra R., Walsh M. A., Zhang L. H., Song H..( 2010;). Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. . Structure 18: 1199–1209. [CrossRef] [PubMed]
    [Google Scholar]
  25. Clarke D. J..( 2010;). The Rcs phosphorelay: more than just a two-component pathway. . Future Microbiol 5: 1173–1184. [CrossRef] [PubMed]
    [Google Scholar]
  26. Couillerot O., Prigent-Combaret C., Caballero-Mellado J., Moënne-Loccoz Y..( 2009;). Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. . Lett Appl Microbiol 48: 505–512. [CrossRef] [PubMed]
    [Google Scholar]
  27. Cui Y., Tu R., Wu L., Hong Y., Chen S..( 2011;). A hybrid two-component system protein from Azospirillum brasilense Sp7 was involved in chemotaxis. . Microbiol Res 166: 458–467. [CrossRef] [PubMed]
    [Google Scholar]
  28. Da Re S., Schumacher J., Rousseau P., Fourment J., Ebel C., Kahn D..( 1999;). Phosphorylation-induced dimerization of the FixJ receiver domain. . Mol Microbiol 34: 504–511. [CrossRef] [PubMed]
    [Google Scholar]
  29. Defosse T. A., Sharma A., Mondal A. K., Dugé de Bernonville T., Latgé J. P., Calderone R., Giglioli-Guivarc'h N., Courdavault V., Clastre M., Papon N..( 2015;). Hybrid histidine kinases in pathogenic fungi. . Mol Microbiol 95: 914–924. [CrossRef] [PubMed]
    [Google Scholar]
  30. Dixon R., Kahn D..( 2004;). Genetic regulation of biological nitrogen fixation. . Nat Rev Microbiol 2: 621–631. [CrossRef] [PubMed]
    [Google Scholar]
  31. Drogue B., Combes-Meynet E., Moënne-Loccoz Y., Wisniewski-Dyé F., Prigent-Combaret C..( 2013;). Control of the cooperation between plant growth-promoting rhizobacteria and crops by rhizosphere signals. . In Molecular Microbial Ecology of the Rhizosphere, pp. 279–293. Edited by de Bruijn F. J.. Hoboken, NJ:: John Wiley & Sons, Inc;.[CrossRef]
    [Google Scholar]
  32. Drogue B., Doré H., Borland S., Wisniewski-Dyé F., Prigent-Combaret C..( 2012;). Which specificity in cooperation between phytostimulating rhizobacteria and plants?. Res Microbiol 163: 500–510. [CrossRef] [PubMed]
    [Google Scholar]
  33. Foussard M., Garnerone A. M., Ni F., Soupène E., Boistard P., Batut J..( 1997;). Negative autoregulation of the Rhizobium meliloti fixK gene is indirect and requires a newly identified regulator, FixT. . Mol Microbiol 25: 27–37. [CrossRef] [PubMed]
    [Google Scholar]
  34. Galperin M. Y..( 2005;). A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. . BMC Microbiol 5: 35. [CrossRef] [PubMed]
    [Google Scholar]
  35. Galperin M. Y..( 2010;). Diversity of structure and function of response regulator output domains. . Curr Opin Microbiol 13: 150–159. [CrossRef] [PubMed]
    [Google Scholar]
  36. Gao R., Stock A. M..( 2009;). Biological insights from structures of two-component proteins. . Annu Rev Microbiol 63: 133–154. [CrossRef] [PubMed]
    [Google Scholar]
  37. Gao R., Stock A. M..( 2010;). Molecular strategies for phosphorylation-mediated regulation of response regulator activity. . Curr Opin Microbiol 13: 160–167. [CrossRef] [PubMed]
    [Google Scholar]
  38. Garnerone A. M., Cabanes D., Foussard M., Boistard P., Batut J..( 1999;). Inhibition of the FixL sensor kinase by the FixT protein in Sinorhizobium meliloti. . J Biol Chem 274: 32500–32506. [CrossRef] [PubMed]
    [Google Scholar]
  39. Gooderham W. J., Hancock R. E..( 2009;). Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. . FEMS Microbiol Rev 33: 279–294. [CrossRef] [PubMed]
    [Google Scholar]
  40. Goodman A. L., Kulasekara B., Rietsch A., Boyd D., Smith R. S., Lory S..( 2004;). A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. . Dev Cell 7: 745–754. [CrossRef] [PubMed]
    [Google Scholar]
  41. Goodman A. L., Merighi M., Hyodo M., Ventre I., Filloux A., Lory S..( 2009;). Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. . Genes Dev 23: 249–259. [CrossRef] [PubMed]
    [Google Scholar]
  42. Gross H., Loper J. E..( 2009;). Genomics of secondary metabolite production by Pseudomonas spp. . Nat Prod Rep 26: 1408–1446. [CrossRef] [PubMed]
    [Google Scholar]
  43. Haas D., Défago G..( 2005;). Biological control of soil-borne pathogens by fluorescent pseudomonads. . Nat Rev Microbiol 3: 307–319. [CrossRef] [PubMed]
    [Google Scholar]
  44. Haas D., Keel C..( 2003;). Regulation of antibiotic production in root-colonizing Peudomonas spp. and relevance for biological control of plant disease. . Annu Rev Phytopathol 41: 117–153. [CrossRef] [PubMed]
    [Google Scholar]
  45. Hassan K. A., Johnson A., Shaffer B. T., Ren Q., Kidarsa T. A., Elbourne L. D., Hartney S., Duboy R., Goebel N. C. et al.( 2010;). Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. . Environ Microbiol 12: 899–915. [CrossRef] [PubMed]
    [Google Scholar]
  46. Hauryliuk V., Atkinson G. C., Murakami K. S., Tenson T., Gerdes K..( 2015;). Recent functional insights into the role of (p)ppGpp in bacterial physiology. . Nat Rev Microbiol 13: 298–309. [CrossRef] [PubMed]
    [Google Scholar]
  47. Hauwaerts D., Alexandre G., Das S. K., Vanderleyden J., Zhulin I. B..( 2002;). A major chemotaxis gene cluster in Azospirillum brasilense and relationships between chemotaxis operons in alpha-proteobacteria. . FEMS Microbiol Lett 208: 61–67.[PubMed]
    [Google Scholar]
  48. He K., Bauer C. E..( 2014;). Chemosensory signaling systems that control bacterial survival. . Trends Microbiol 22: 389–398. [CrossRef] [PubMed]
    [Google Scholar]
  49. He K., Dragnea V., Bauer C. E..( 2015;). Adenylate charge regulates sensor kinase CheS3 to control cyst formation in Rhodospirillum centenum. . MBio 6:,e0054615. [CrossRef] [PubMed]
    [Google Scholar]
  50. He K., Marden J. N., Quardokus E. M., Bauer C. E..( 2013;). Phosphate flow between hybrid histidine kinases CheA3 and CheS3 controls Rhodospirillum centenum cyst formation. . PLoS Genet 9:,e1004002. [CrossRef] [PubMed]
    [Google Scholar]
  51. He Y. W., Wang C., Zhou L., Song H., Dow J. M., Zhang L. H..( 2006;). Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. . J Biol Chem 281: 33414–33421. [CrossRef] [PubMed]
    [Google Scholar]
  52. Heeb S., Haas D..( 2001;). Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. . Mol Plant Microbe Interact 14: 1351–1363. [CrossRef] [PubMed]
    [Google Scholar]
  53. Heeb S., Blumer C., Haas D..( 2002;). Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. . J Bacteriol 184: 1046–1056. [CrossRef] [PubMed]
    [Google Scholar]
  54. Heeb S., Valverde C., Gigot-Bonnefoy C., Haas D..( 2005;). Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. . FEMS Microbiol Lett 243: 251–258. [CrossRef] [PubMed]
    [Google Scholar]
  55. Hentschel U., Steinert M., Hacker J..( 2000;). Common molecular mechanisms of symbiosis and pathogenesis. . Trends Microbiol 8: 226–231. [CrossRef] [PubMed]
    [Google Scholar]
  56. Hinsinger P., Gobran G. R., Gregory P. J., Wenzel W. W..( 2005;). Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. . New Phytol 168: 293–303. [CrossRef] [PubMed]
    [Google Scholar]
  57. Huang Y. H., Ferrières L., Clarke D. J..( 2006;). The role of the Rcs phosphorelay in Enterobacteriaceae. . Res Microbiol 157: 206–212. [CrossRef] [PubMed]
    [Google Scholar]
  58. Humair B., González N., Mossialos D., Reimmann C., Haas D..( 2009;). Temperature-responsive sensing regulates biocontrol factor expression in Pseudomonas fluorescens CHA0. . ISME J 3: 955–965. [CrossRef] [PubMed]
    [Google Scholar]
  59. Jones P., Binns D., McMenamin C., McAnulla C., Hunter S..( 2011;). The InterPro BioMart: federated query and web service access to the interPro resource. . Database 2011: bar033. [CrossRef] [PubMed]
    [Google Scholar]
  60. Jung K., Fried L., Behr S., Heermann R..( 2012;). Histidine kinases and response regulators in networks. . Curr Opin Microbiol 15: 118–124. [CrossRef] [PubMed]
    [Google Scholar]
  61. Kay E., Dubuis C., Haas D..( 2005;). Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Pro. . Natl Acad Sci USA 102: 17136–17141. [CrossRef]
    [Google Scholar]
  62. Kong W., Chen L., Zhao J., Shen T., Surette M. G., Shen L., Duan K..( 2013;). Hybrid sensor kinase PA1611 in Pseudomonas aeruginosa regulates transitions between acute and chronic infection through direct interaction with RetS. . Mol Microbiol 88: 784–797. [CrossRef] [PubMed]
    [Google Scholar]
  63. Kupferschmied P., Maurhofer M., Keel C..( 2013;). Promise for plant pest control: root-associated pseudomonads with insecticidal activities. . Front Plant Sci 4: 287. [CrossRef] [PubMed]
    [Google Scholar]
  64. Kupferschmied P., Péchy-Tarr M., Imperiali N., Maurhofer M., Keel C..( 2014;). Domain shuffling in a sensor protein contributed to the evolution of insect pathogenicity in plant-beneficial Pseudomonas protegens. . PLoS Pathog 10:,e1003964. [CrossRef] [PubMed]
    [Google Scholar]
  65. Kuzyakov Y., Xu X..( 2013;). Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. . New Phytol 198: 656–669. [CrossRef] [PubMed]
    [Google Scholar]
  66. Lapouge K., Schubert M., Allain F. H.-T., Haas D..( 2008;). Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. . Mol Microbiol 67: 241–253. [CrossRef] [PubMed]
    [Google Scholar]
  67. Laub M. T., Goulian M..( 2007;). Specificity in two-component signal transduction pathways. . Annu Rev Genet 41: 121–145. [CrossRef] [PubMed]
    [Google Scholar]
  68. Li H., Cui Y., Wu L., Tu R., Chen S..( 2011;). cDNA-AFLP analysis of differential gene expression related to cell chemotactic and encystment of Azospirillum brasilense. . Microbiol Res 166: 595–605. [CrossRef] [PubMed]
    [Google Scholar]
  69. Lopez-Guerrero M., Ormeno-Orrillo E., Rosenblueth M., Martinez-Romero J., Martinez-Romero E..( 2013;). Buffet hypothesis for microbial nutrition at the rhizosphere. . Funct Plant Ecol 4: 188. [CrossRef]
    [Google Scholar]
  70. Lu H., Patil P., Van Sluys M. A., White F. F., Ryan R. P., Dow J. M., Rabinowicz P., Salzberg S. L., Leach J. E. et al.( 2008;). Acquisition and evolution of plant pathogenesis-associated gene clusters and candidate determinants of tissue-specificity in xanthomonas. . PLoS One 3:,e3828. [CrossRef] [PubMed]
    [Google Scholar]
  71. Madec E., Bontemps-Gallo S., Lacroix J. M..( 2014;). Increased phosphorylation of the RcsB regulator of the RcsCDB phosphorelay in strains of Dickeya dadantii devoid of osmoregulated periplasmic glucans revealed by Phos-tag gel analysis. . Microbiology 160: 2763–2770. [CrossRef] [PubMed]
    [Google Scholar]
  72. Majdalani N., Gottesman S..( 2005;). The Rcs phosphorelay: a complex signal transduction system. . Annu Rev Microbiol 59: 379–405. [CrossRef] [PubMed]
    [Google Scholar]
  73. Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C. et al.( 2011;). CDD: a conserved domain database for the functional annotation of proteins. . Nucleic Acids Res 39: D225–D229. [CrossRef] [PubMed]
    [Google Scholar]
  74. Martínez-Granero F., Navazo A., Barahona E., Redondo-Nieto M., Rivilla R., Martín M..( 2012;). The Gac-Rsm and SadB signal transduction pathways converge on AlgU to downregulate motility in Pseudomonas fluorescens. . PLoS One 7:,e31765. [CrossRef] [PubMed]
    [Google Scholar]
  75. Masson-Boivin C., Giraud E., Perret X., Batut J..( 2009;). Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes?. Trends Microbiol 17: 458–466. [CrossRef] [PubMed]
    [Google Scholar]
  76. Mikkelsen H., Sivaneson M., Filloux A..( 2011;). Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. . Environ Microbiol 13: 1666–1681. [CrossRef] [PubMed]
    [Google Scholar]
  77. Minogue T. D., Carlier A. L., Koutsoudis M. D., von Bodman S. B..( 2005;). The cell density-dependent expression of stewartan exopolysaccharide in Pantoea stewartii ssp. stewartii is a function of EsaR-mediated repression of the rcsA gene. . Mol Microbiol 56: 189–203. [CrossRef] [PubMed]
    [Google Scholar]
  78. Mitrophanov A. Y., Groisman E. A..( 2008;). Signal integration in bacterial two-component regulatory systems. . Genes Dev 22: 2601–2611. [CrossRef] [PubMed]
    [Google Scholar]
  79. Mukhopadhyay A., Gao R., Lynn D. G..( 2004;). Integrating input from multiple signals: the VirA/VirG two-component system of Agrobacterium tumefaciens. . Chembiochem 5: 1535–1542. [CrossRef] [PubMed]
    [Google Scholar]
  80. Parkinson J. S., Hazelbauer G. L., Falke J. J..( 2015;). Signaling and sensory adaptation in Escherichia coli chemoreceptors: 2015 update. . Trends Microbiol 23: 257–266. [CrossRef] [PubMed]
    [Google Scholar]
  81. Preisig O., Anthamatten D., Hennecke H..( 1993;). Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. . Proc Natl Acad Sci U S A 90: 3309–3313. [CrossRef] [PubMed]
    [Google Scholar]
  82. Péchy-Tarr M., Borel N., Kupferschmied P., Turner V., Binggeli O., Radovanovic D., Maurhofer M., Keel C..( 2013;). Control and host-dependent activation of insect toxin expression in a root-associated biocontrol pseudomonad. . Environ Microbiol 15: 736–750. [CrossRef] [PubMed]
    [Google Scholar]
  83. Péchy-Tarr M., Bruck D. J., Maurhofer M., Fischer E., Vogne C., Henkels M. D., Donahue K. M., Grunder J., Loper J. E., Keel C..( 2008;). Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. . Environ Microbiol 10: 2368–2386. [CrossRef] [PubMed]
    [Google Scholar]
  84. Reimmann C., Valverde C., Kay E., Haas D..( 2005;). Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. . J Bacteriol 187: 276–285. [CrossRef] [PubMed]
    [Google Scholar]
  85. Rodrigue A., Quentin Y., Lazdunski A., Méjean V., Foglino M..( 2000;). Two-component systems in Pseudomonas aeruginosa: why so many?. Trends Microbiol 8: 498–504.[PubMed] [CrossRef]
    [Google Scholar]
  86. Ruffner B., Péchy-Tarr M., Höfte M., Bloemberg G., Grunder J., Keel C., Maurhofer M..( 2015;). Evolutionary patchwork of an insecticidal toxin shared between plant-associated pseudomonads and the insect pathogens Photorhabdus and Xenorhabdus. . BMC Genomics 16: 609. [CrossRef] [PubMed]
    [Google Scholar]
  87. Ruffner B., Péchy-Tarr M., Ryffel F., Hoegger P., Obrist C., Rindlisbacher A., Keel C., Maurhofer M..( 2013;). Oral insecticidal activity of plant-associated pseudomonads. . Environ Microbiol 15: 751–763. [CrossRef] [PubMed]
    [Google Scholar]
  88. Ryan R. P., Dow J. M..( 2011;). Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria. . Trends Microbiol 19: 145–152. [CrossRef] [PubMed]
    [Google Scholar]
  89. Ryan R. P., An S. Q., Allan J. H., McCarthy Y., Dow J. M..( 2015;). The DSF family of cell–cell signals: an expanding class of bacterial virulence regulators. . PLoS Pathog 11:,e1004986. [CrossRef] [PubMed]
    [Google Scholar]
  90. Ryan R. P., Fouhy Y., Lucey J. F., Crossman L. C., Spiro S., He Y. W., Zhang L. H., Heeb S., Cámara M. et al.( 2006;). Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. . Proc Natl Acad Sci U S A 103: 6712–6717. [CrossRef] [PubMed]
    [Google Scholar]
  91. Ryan R. P., McCarthy Y., Andrade M., Farah C. S., Armitage J. P., Dow J. M., Rade M..( 2010;). Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. . Proc Natl Acad Sci U S A 107: 5989–5994. [CrossRef] [PubMed]
    [Google Scholar]
  92. Ryan R. P., Vorhölter F. J., Potnis N., Jones J. B., Van Sluys M. A., Bogdanove A. J., Dow J. M..( 2011;). Pathogenomics of Xanthomonas: understanding bacterium-plant interactions. . Nat Rev Microbiol 9: 344–355. [CrossRef] [PubMed]
    [Google Scholar]
  93. Sall K. M., Casabona M. G., Bordi C., Huber P., de Bentzmann S., Attrée I., Elsen S..( 2014;). A gacS deletion in Pseudomonas aeruginosa cystic fibrosis isolate CHA shapes its virulence. . PLoS One 9:,e95936. [CrossRef] [PubMed]
    [Google Scholar]
  94. Scharf B. E., Hynes M. F., Alexandre G. M..( 2016;). Chemotaxis signaling systems in model beneficial plant-bacteria associations. . Plant Mol Biol 90: 549–559. [CrossRef] [PubMed]
    [Google Scholar]
  95. Schmöe K., Rogov V. V., Rogova N. Y., Löhr F., Güntert P., Bernhard F., Dötsch V..( 2011;). Structural insights into Rcs phosphotransfer: the newly identified RcsD-ABL domain enhances interaction with the response regulator RcsB. . Structure 19: 577–587. [CrossRef] [PubMed]
    [Google Scholar]
  96. Slater H., Alvarez-Morales A., Barber C. E., Daniels M. J., Dow J. M..( 2000;). A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. . Mol Microbiol 38: 986–1003. [CrossRef] [PubMed]
    [Google Scholar]
  97. Sousa E. H., Tuckerman J. R., Gondim A. C., Gonzalez G., Gilles-Gonzalez M. A..( 2013;). Signal transduction and phosphoryl transfer by a FixL hybrid kinase with low oxygen affinity: importance of the vicinal PAS domain and receiver aspartate. . Biochemistry 52: 456–465. [CrossRef] [PubMed]
    [Google Scholar]
  98. Stock A. M., Robinson V. L., Goudreau P. N..( 2000;). Two-component signal transduction. . Annu Rev Biochem 69: 183–215. [CrossRef] [PubMed]
    [Google Scholar]
  99. Stout V., Gottesman S..( 1990;). RcsB and RcsC: a two-component regulator of capsule synthesis in Escherichia coli. . J Bacteriol 172: 659–669.[PubMed]
    [Google Scholar]
  100. Takeuchi K., Kiefer P., Reimmann C., Keel C., Dubuis C., Rolli J., Vorholt J. A., Haas D..( 2009;). Small RNA-dependent expression of secondary metabolism is controlled by Krebs cycle function in Pseudomonas fluorescens. . J Biol Chem 284: 34976–34985. [CrossRef] [PubMed]
    [Google Scholar]
  101. Takeuchi K., Yamada K., Haas D..( 2012;). ppGpp controlled by the Gac/Rsm regulatory pathway sustains biocontrol activity in Pseudomonas fluorescens CHA0. . Mol Plant Microbe Interact 25: 1440–1449. [CrossRef] [PubMed]
    [Google Scholar]
  102. Terpolilli J. J., Hood G. A., Poole P. S..( 2012;). What determines the efficiency of N(2)-fixing Rhizobium-legume symbioses?. Adv Microb Physiol 60: 325–389. [CrossRef] [PubMed]
    [Google Scholar]
  103. Tu R., Cui Y., Chen S., Li J..( 2006;). PAS domain of the deduced Org35 protein mediates the interaction with NifA. . Chin Sci Bull 51: 1141–1144. [CrossRef]
    [Google Scholar]
  104. Ulrich L. E., Koonin E. V., Zhulin I. B..( 2005;). One-component systems dominate signal transduction in prokaryotes. . Trends Microbiol 13: 52–56. [CrossRef] [PubMed]
    [Google Scholar]
  105. Ventre I., Goodman A. L., Vallet-Gely I., Vasseur P., Soscia C., Molin S., Bleves S., Lazdunski A., Lory S., Filloux A..( 2006;). Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. . Proc Natl Acad Sci U S A 103: 171–176. [CrossRef] [PubMed]
    [Google Scholar]
  106. Vincent F., Round A., Reynaud A., Bordi C., Filloux A., Bourne Y..( 2010;). Distinct oligomeric forms of the Pseudomonas aeruginosa RetS sensor domain modulate accessibility to the ligand binding site. . Environ Microb 12: 1775–1786. [CrossRef] [PubMed]
    [Google Scholar]
  107. Wadhams G. H., Armitage J. P..( 2004;). Making sense of it all: bacterial chemotaxis. . Nat Rev Mol Cell Biol 5: 1024–1037. [CrossRef] [PubMed]
    [Google Scholar]
  108. Wang D., Korban S. S., Zhao Y..( 2009;). The Rcs phosphorelay system is essential for pathogenicity in Erwinia amylovora. . Mol Plant Pathol 10: 277–290. [CrossRef] [PubMed]
    [Google Scholar]
  109. Wang D., Korban S. S., Pusey P. L., Zhao Y..( 2011;). Characterization of the RcsC sensor kinase from Erwinia amylovora and other Enterobacteria. . Phytopathology 101: 710–717. [CrossRef] [PubMed]
    [Google Scholar]
  110. Wang D., Qi M., Calla B., Korban S. S., Clough S. J., Cock P. J., Sundin G. W., Toth I., Zhao Y..( 2012;). Genome-wide identification of genes regulated by the Rcs phosphorelay system in Erwinia amylovora. . Mol Plant Microbe Interact 25: 6–17. [CrossRef] [PubMed]
    [Google Scholar]
  111. Wang L. H., He Y., Gao Y., Wu J. E., Dong Y. H., He C., Wang S. X., Weng L. X., Xu J. L. et al.( 2004;). A bacterial cell-cell communication signal with cross-kingdom structural analogues. . Mol Microbiol 51: 903–912. [CrossRef] [PubMed]
    [Google Scholar]
  112. Wegener-Feldbrügge S., Søgaard-Andersen L..( 2009;). The atypical hybrid histidine protein kinase RodK in Myxococcus xanthus: spatial proximity supersedes kinetic preference in phosphotransfer reactions. . J Bacteriol 191: 1765–1776. [CrossRef] [PubMed]
    [Google Scholar]
  113. Whitworth D. E., Cock P. J..( 2008;). Two-component systems of the myxobacteria: structure, diversity and evolutionary relationships. . Microbiology 154: 360–372. [CrossRef] [PubMed]
    [Google Scholar]
  114. Wise A. A., Binns A. N..( 2016;). The receiver of the Agrobacterium tumefaciens VirA histidine kinase forms a stable interaction with VirG to activate virulence gene expression. . Front Microbiol 6: 1546. [CrossRef] [PubMed]
    [Google Scholar]
  115. Wise A. A., Fang F., Lin Y. H., He F., Lynn D. G., Binns A. N..( 2010;). The receiver domain of hybrid histidine kinase VirA: an enhancing factor for vir gene expression in Agrobacterium tumefaciens. . J Bacteriol 192: 1534–1542. [CrossRef] [PubMed]
    [Google Scholar]
  116. Wisniewski-Dyé F., Borziak K., Khalsa-Moyers G., Alexandre G., Sukharnikov L. O., Wuichet K., Hurst G. B., McDonald W. H., Robertson J. S. et al.( 2011;). Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. . PLoS Genet 7:,e1002430. [CrossRef] [PubMed]
    [Google Scholar]
  117. Wisniewski-Dyé F., Drogue B., Borland S., Prigent-Combaret C..( 2013;). Azospirillum–plant interaction: from root colonization to plant growth promotion. . In Beneficial Plant-Microbial Interactions: Ecology and Applications , pp. 237–279. Edited by Rodelas González M. B., González-López J.. Boca Raton, FL:: C. R. C. Press;.[CrossRef]
    [Google Scholar]
  118. Workentine M. L., Chang L., Ceri H., Turner R. J..( 2009;). The GacS-GacA two-component regulatory system of Pseudomonas fluorescens: a bacterial two-hybrid analysis. . FEMS Microbiol Lett 292: 50–56. [CrossRef] [PubMed]
    [Google Scholar]
  119. Wuichet K., Cantwell B. J., Zhulin I. B..( 2010;). Evolution and phyletic distribution of two-component signal transduction systems. . Curr Opin Microbiol 13: 219–225. [CrossRef] [PubMed]
    [Google Scholar]
  120. Zuber S., Carruthers F., Keel C., Mattart A., Blumer C., Pessi G., Gigot-Bonnefoy C., Schnider-Keel U., Heeb S. et al.( 2003;). GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of CHA0. . Mol Plant Microb Interact 16: 634–644.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000370
Loading
/content/journal/micro/10.1099/mic.0.000370
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error