1932

Abstract

species complex (RSSC) strains are devastating plant pathogens distributed worldwide. The primary cell density–dependent gene expression system in RSSC strains is quorum sensing (QS). It regulates the expression of about 30% of all genes, including those related to cellular activity, primary and secondary metabolism, pathogenicity, and more. The regulatory elements encoded by the operon and gene play vital roles. RSSC strains use methyl 3-hydroxymyristate (3-OH MAME) or methyl 3-hydroxypalmitate (3-OH PAME) as the QS signal. Each type of RSSC strain has specificity in generating and receiving its QS signal, but their signaling pathways might not differ significantly. In this review, I describe the genetic and biochemical factors involved in QS signal input and the regulatory network and summarize control of the QS system, new cell–cell communications, and QS-dependent interactions with soil fungi.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-032521-030537
2023-09-15
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/77/1/annurev-micro-032521-030537.html?itemId=/content/journals/10.1146/annurev-micro-032521-030537&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Achari GA, Ramesh R. 2015. Characterization of bacteria degrading 3-hydroxy palmitic acid methyl ester (3OH-PAME), a quorum sensing molecule of Ralstonia solanacearum. Lett. Appl. Microbiol. 60:447–55
    [Google Scholar]
  2. 2.
    Aldon D, Brito B, Boucher C, Genin S. 2000. A bacterial sensor of plant cell contact controls the transcriptional induction of Ralstonia solanacearum pathogenicity genes. EMBO J. 19:2304–14
    [Google Scholar]
  3. 3.
    Allen C, Prior P, Hayward AC, eds. 2005. Bacterial Wilt Disease and the Ralstonia solanacearum Species Complex St. Paul, MN: APS
    [Google Scholar]
  4. 4.
    Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C et al. 2008. Genome sequence of the β-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res. 18:1472–83
    [Google Scholar]
  5. 5.
    Araud-Razou I, Vasse J, Montrozier H, Etchebar C, Trigalet A. 1998. Detection and visualization of the major acidic exopolysaccharide of Ralstonia solanacearum and its role in tomato root infection and vascular colonization. Eur. J. Plant Pathol. 104:795–809
    [Google Scholar]
  6. 6.
    Arlat M, Gijsegem FV, Huet JC, Pernollet JC, Boucher CA. 1994. PopAl, a protein which induces a hypersensitivity-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J. 13:543–53
    [Google Scholar]
  7. 7.
    Baldeweg F, Kage H, Schieferdecker S, Allen A, Hoffmeister D, Nett M. 2017. Structure of ralsolamycin, the interkingdom morphogen from the crop plant pathogen Ralstonia solanacearum. Org. Lett. 19:4868–71
    [Google Scholar]
  8. 8.
    Baroukh C, Zemouri M, Genin S. 2021. Trophic preferences of the pathogen Ralstonia solanacearum and consequences on its growth in xylem sap. MicrobiologyOpen 11:e1240
    [Google Scholar]
  9. 9.
    Bridges AA, Prentice JA, Wingreen NS, Bassler BL. 2022. Signal transduction network principles underlying bacterial collective behaviors. Annu. Rev. Microbiol. 76:235–57
    [Google Scholar]
  10. 10.
    Brumbley SM, Carney BF, Denny TP. 1993. Phenotype conversion in Pseudomonas solanacearum due to spontaneous inactivation of PhcA, a putative LysR transcriptional regulator. J. Bacteriol. 175:5477–87
    [Google Scholar]
  11. 11.
    Buddenhagen I, Kelman A. 1964. Biological and physiological aspects of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 2:203–30
    [Google Scholar]
  12. 12.
    Busby PE, Newcombe G, Neat AS, Averill C. 2022. Facilitating reforestation through the plant microbiome: perspectives from the phyllosphere. Annu. Rev. Phytopathol. 60:337–56
    [Google Scholar]
  13. 13.
    Buschiazzo A, Trajtenberg F. 2019. Two-component sensing and regulation: How do histidine kinases talk with response regulators at the molecular level?. Annu. Rev. Microbiol. 73:507–28
    [Google Scholar]
  14. 14.
    Chang Q, Wang W, Regev-Yochay G, Lipsitch M, Hanage WP. 2015. Antibiotics in agriculture and the risk to human health: How worried should we be?. Evol. Appl. 8:240–47
    [Google Scholar]
  15. 15.
    Chen M, Zhang W, Han L, Ru X, Cao Y et al. 2022. A CysB regulator positively regulates cysteine synthesis, expression of type III secretion system genes, and pathogenicity in Ralstonia solanacearum. Mol. Plant Pathol. 23:679–92
    [Google Scholar]
  16. 16.
    Clough SJ, Lee KE, Schell MA, Denny TP. 1997. A two-component system in Ralstonia (Pseudomonas) solanacearum modulates production of PhcA-regulated virulence factors in response to 3-hydroxypalmitic acid methyl ester. J. Bacteriol. 179:3639–48
    [Google Scholar]
  17. 17.
    Clough SJ, Schell MA, Denny TP. 1994. Evidence for involvement of a volatile extracellular factor in Pseudomonas solanacearum virulence gene expression. Mol. Plant-Microbe Interact. 7:621–30
    [Google Scholar]
  18. 18.
    Cunnac S, Occhialini A, Barberis P, Boucher C, Genin S. 2004. Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: identification of novel effector proteins translocated to plant host cells through the type III secretion system. Mol. Microbiol. 53:115–28
    [Google Scholar]
  19. 19.
    da Silva DP, Matwichuk ML, Townsend DO, Reichhardt C, Lamba D et al. 2019. The Pseudomonas aeruginosa lectin LecB binds to the exopolysaccharide Psl and stabilizes the biofilm matrix. Nat. Commun. 10:2183
    [Google Scholar]
  20. 20.
    Davenport PW, Griffin JL, Welch M. 2015. Quorum sensing is accompanied by global metabolic changes in the opportunistic human pathogen Pseudomonas aeruginosa. J. Bacteriol. 197:2072–82
    [Google Scholar]
  21. 21.
    de Pedro-Jové R, Puigvert M, Sebastià P, Macho AP, Monteiro JS et al. 2021. Dynamic expression of Ralstonia solanacearum virulence factors and metabolism-controlling genes during plant infection. BMC Genom. 22:170
    [Google Scholar]
  22. 22.
    Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH. 2001. Quenching quorum-sensing dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–17
    [Google Scholar]
  23. 23.
    Dong YH, Xu JL, Li XZ, Zhang LH. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. PNAS 97:3526–31
    [Google Scholar]
  24. 24.
    Fatima U, Senthil-Kumar M. 2015. Plant and pathogen nutrient acquisition strategies. Front. Plant Sci. 6:750
    [Google Scholar]
  25. 25.
    Flavier AB, Clough SJ, Schell MA, Denny TP. 1997. Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol. Microbiol. 26:251–59
    [Google Scholar]
  26. 26.
    Flavier AB, Ganova-Raeva LM, Schell MA, Denny TP. 1997. Hierarchical autoinduction in Ralstonia solanacearum: control of acyl-homoserine lactone production by a novel autoregulatory system responsive to 3-hydroxypalmitic acid methyl ester. J. Bacteriol. 179:7089–97
    [Google Scholar]
  27. 27.
    Galloway WRJD, Hodgkinson JT, Bowden SD, Welch M, Spring DR. 2011. Quorum sensing in Gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem. Rev. 111:28–67
    [Google Scholar]
  28. 28.
    Geng R, Cheng L, Cao C, Liu Z, Liu D et al. 2022. Comprehensive analysis reveals the genetic and pathogenic diversity of Ralstonia solanacearum species complex and benefits its taxonomic classification. Front. Microbiol. 13:854792
    [Google Scholar]
  29. 29.
    Genin S, Denny TP. 2012. Pathogenomics of the Ralstonia solanacearum species complex. Annu. Rev. Phytopathol. 50:67–89
    [Google Scholar]
  30. 30.
    Genin S, Gough CL, Zischek C, Boucher CA. 1992. Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol. Microbiol. 6:3065–76
    [Google Scholar]
  31. 31.
    Goo E, Majerczyk CD, An JH, Chandler JR, Seo YS et al. 2012. Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress. PNAS 109:19775–80
    [Google Scholar]
  32. 32.
    Grandclément C, Tannières M, Moréra S, Dessaux Y, Faure D. 2016. Quorum quenching: role in nature and applied developments. FEMS Microbiol. Rev. 40:86–116
    [Google Scholar]
  33. 33.
    Grimster NP, Stump B, Fotsing JR, Weide T, Talley TT et al. 2012. Generation of candidate ligands for nicotinic acetylcholine receptors via in situ click chemistry with a soluble acetylcholine binding protein template. J. Am. Chem. Soc. 134:673240
    [Google Scholar]
  34. 34.
    Han SW, Yoshikuni Y. 2022. Microbiome engineering for sustainable agriculture: using synthetic biology to enhance nitrogen metabolism in plant-associated microbes. Curr. Opin. Microbiol. 68:102172
    [Google Scholar]
  35. 35.
    Hayashi K, Kai K, Mori Y, Ishikawa S, Ujita Y et al. 2019. Contribution of a lectin, LecM, to the quorum sensing signalling pathway of Ralstonia solanacearum strain OE1-1. Mol. Plant Pathol. 20:334–45
    [Google Scholar]
  36. 36.
    Hayashi K, Senuma W, Kai K, Kiba A, Ohnishi K, Hikichi Y. 2019. Major exopolysaccharide, EPS I, is associated with the feedback loop in the quorum sensing of Ralstonia solanacearum strain OE1-1. Mol. Plant Pathol. 20:1740–47
    [Google Scholar]
  37. 37.
    Hayward AC. 1991. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu. Rev. Phytopathol. 29:65–87
    [Google Scholar]
  38. 38.
    Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL. 2007. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450:883–86
    [Google Scholar]
  39. 39.
    Hikichi Y, Yoshimochi T, Tsujimoto S, Shinohara R, Nakaho K et al. 2007. Global regulation of pathogenicity mechanism of Ralstonia solanacearum. Plant Biotechnol. 24:149–54
    [Google Scholar]
  40. 40.
    Hirakawa H, Tomita H. 2013. Interference of bacterial cell-to-cell communication: A new concept of antimicrobial chemotherapy breaks antibiotic resistance. Front. Microbiol. 4:114
    [Google Scholar]
  41. 41.
    Jacobs JM, Babujee L, Meng F, Milling A, Allen C. 2012. The in planta transcriptome of Ralstonia solanacearum: conserved physiological and virulence strategies during bacterial wilt of tomato. mBio 3:e00114–12
    [Google Scholar]
  42. 42.
    Jing J, Cong WF, Bezemer TM. 2022. Legacies at work: plant-soil-microbiome interactions underpinning agricultural sustainability. Trends Plant Sci. 27:781–92
    [Google Scholar]
  43. 43.
    Joshi JR, Khazanov N, Charkowski A, Faigenboim A, Senderowitz H, Yedidia I. 2021. Interkingdom signaling interference: the effect of plant-derived small molecules on quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 59:153–90
    [Google Scholar]
  44. 44.
    Kai K, Ohnishi H, Kiba A, Ohnishi K, Hikichi Y. 2016. Studies on the biosynthesis of ralfuranones in Ralstonia solanacearum. Biosci. Biotechnol. Biochem. 80:440–44
    [Google Scholar]
  45. 45.
    Kai K, Ohnishi H, Mori Y, Kiba A, Ohnishi K, Hikichi Y. 2014. Involvement of ralfuranone production in the virulence of Ralstonia solanacearum OE1-1. ChemBioChem 15:2590–97
    [Google Scholar]
  46. 46.
    Kai K, Ohnishi H, Shimatani M, Ishikawa S, Mori Y et al. 2015. Methyl 3-hydroxymyristate, a diffusible signal mediating phc quorum sensing in Ralstonia solanacearum. ChemBioChem 16:2309–18
    [Google Scholar]
  47. 47.
    Khalid S, Baccile JA, Spraker JE, Tannous J, Imran M et al. 2018. NRPS-derived isoquinolines and lipopetides mediate antagonism between plant pathogenic fungi and bacteria. ACS Chem. Biol. 13:17179
    [Google Scholar]
  48. 48.
    Khokhani D, Lowe-Power TM, Tran TM, Allen C. 2017. A single regulator mediates strategic switching between attachment/spread and growth/virulence in the plant pathogen Ralstonia solanacearum. mBio 8:e00895–17
    [Google Scholar]
  49. 49.
    Kitamura S, Zheng Q, Woehl JL, Solania A, Chen E et al. 2020. Sulfur(VI) fluoride exchange (SuFEx)-enabled high-throughput medicinal chemistry. J. Am. Chem. Soc. 142:10899904
    [Google Scholar]
  50. 50.
    Kumar S, Ahmad K, Behera SK, Nagrale DT, Chaurasia A et al. 2022. Biocomputational assessment of natural compounds as a potent inhibitor to quorum sensors in Ralstonia solanacearum. Molecules 27:3034
    [Google Scholar]
  51. 51.
    Lee J, Zhang L. 2015. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell 6:26–41
    [Google Scholar]
  52. 52.
    Lee MH, Khan R, Tao W, Choi K, Lee SY et al. 2018. Soil metagenome-derived 3-hydroxypalmitic acid methyl ester hydrolases suppress extracellular polysaccharide production in Ralstonia solanacearum. J. Biotechnol. 270:30–38
    [Google Scholar]
  53. 53.
    Li P, Cao X, Zhang L, Lv M, Zhang LH. 2022. PhcA and PhcR regulate ralsolamycin biosynthesis oppositely in Ralstonia solanacearum. Front. Plant Sci. 13:903310
    [Google Scholar]
  54. 54.
    Li P, Yin W, Yan J, Chen Y, Fu S et al. 2017. Modulation of inter-kingdom communication by PhcBSR quorum sensing system in Ralstonia solanacearum phylotype I strain GMI1000. Front. Microbiol. 8:1172
    [Google Scholar]
  55. 55.
    Lipsitch M, Singer RS, Levin BR. 2002. Antibiotics in agriculture: When is it time to close the barn door?. PNAS 99:5752–54
    [Google Scholar]
  56. 56.
    Liu F, Hu M, Zhang Z, Xue Y, Chen S, Hu A, Zhang LH, Zhou J. 2022. Dickeya manipulates multiple quorum sensing systems to control virulence and collective behaviors. Front. Plant Sci. 13:838125
    [Google Scholar]
  57. 57.
    Lowe-Power TM, Khokhani D, Allen C. 2018. How Ralstonia solanacearum exploits and thrives in the flowing plant xylem environment. Trends Microbiol. 26:929–41
    [Google Scholar]
  58. 58.
    McGarvey JA, Denny TP, Schell MA. 1999. Spatial-temporal and quantitative analysis of growth and EPS I production by Ralstonia solanacearum in resistant and susceptible tomato cultivars. Phytopathology 89:1233–39
    [Google Scholar]
  59. 59.
    Miller MB, Bassler BL. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165–99
    [Google Scholar]
  60. 60.
    Mori Y, Ishikawa S, Ohnishi SM, Morikawa Y, Hayashi K et al. 2018. Involvement of ralfuranones in the quorum sensing signalling pathway and virulence of Ralstonia solanacearum strain OE1-1. Mol. Plant Pathol. 19:454–63
    [Google Scholar]
  61. 61.
    Murai Y, Mori S, Konno H, Hikichi Y, Kai K. 2017. Ralstonins A and B, lipopeptides with chlamydospore-inducing and phytotoxic activities from the plant pathogen Ralstoniasolanacearum. Org. Lett. 19:417578
    [Google Scholar]
  62. 62.
    Neiditch MB, Federle MJ, Pompeani AJ, Kelly RC, Swem DL et al. 2006. Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing. Cell 126:1095–108
    [Google Scholar]
  63. 63.
    Papenfort K, Bassler BL. 2016. Quorum sensing signal-response systems in Gram-negative bacteria. Nat. Rev. Microbiol. 14:576–88
    [Google Scholar]
  64. 64.
    Pauly J, Nett M, Hoffmeister D. 2014. Ralfuranone is produced by an alternative aryl-substituted γ-lactone biosynthetic route in Ralstonia solanacearum. J. Nat. Prod. 77:1967–71
    [Google Scholar]
  65. 65.
    Pauly J, Spiteller D, Linz J, Jacobs J, Allen C et al. 2013. Ralfuranone thioether production by the plant pathogen Ralstonia solanacearum. ChemBioChem 14:2169–78
    [Google Scholar]
  66. 66.
    Peeters N, Guidot A, Vailleau F, Valls M. 2013. Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol. Plant Pathol. 14:651–62
    [Google Scholar]
  67. 67.
    Perrier A, Barlet X, Peyraud R, Rengel D, Guidot A, Genin S. 2018. Comparative transcriptomic studies identify specific expression patterns of virulence factors under the control of the master regulator PhcA in the Ralstonia solanacearum species complex. Microb. Pathog. 116:273–78
    [Google Scholar]
  68. 68.
    Peyraud R, Cottret L, Marmiesse L, Gouzy J, Genin S. 2016. A resource allocation trade-off between virulence and proliferation drives metabolic versatility in the plant pathogen Ralstonia solanacearum. PLOS Pathog. 12:e1005939
    [Google Scholar]
  69. 69.
    Praneenararat T, Geske GD, Blackwell HE. 2009. Efficient synthesis and evaluation of quorum-sensing modulators using small molecule macroarrays. Org. Lett. 11:4600–3
    [Google Scholar]
  70. 70.
    Safni I, Cleenwerck I, Vos PD, Fegan M, Sly L, Kappler U. 2014. Polyphasic taxonomic revision of the Ralstonia solanacearum species complex: proposal to emend the descriptions of Ralstonia solanacearum and Ralstonia syzygii and reclassify current R. syzygii strains as Ralstonia syzygii subsp. syzygii subsp. nov., R. solanacearum phylotype IV strains as Ralstonia syzygii subsp. indonesiensis subsp. nov., banana blood disease bacterium strains as Ralstonia syzygii subsp. celebesensis subsp. nov. and R. solanacearum phylotype I and III strains as Ralstonia pseudosolanacearum sp. nov. Int. J. Syst. Evol. Microbiol. 64:3087–103
    [Google Scholar]
  71. 71.
    Saile E, McGarvey JA, Schell MA, Denny TP. 1997. Role of extracellular polysaccharide and endoglucanase in root invasion and colonization of tomato plants by Ralstonia solanacearum. Phytopathology 87:1184–96
    [Google Scholar]
  72. 72.
    Schell MA. 2000. Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annu. Rev. Phytopathol. 38:263–92
    [Google Scholar]
  73. 73.
    Schneider P, Jacobs JM, Neres J, Aldrich CC, Allen A et al. 2009. The global virulence regulators VsrAD and PhcA control secondary metabolism in the plant pathogen Ralstonia solanacearum. ChemBioChem 10:2730–32
    [Google Scholar]
  74. 74.
    Seed PC, Passdor L, Iglewski BH. 1995. Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. J. Bacteriol. 177:654–59
    [Google Scholar]
  75. 75.
    Senuma W, Takemura C, Hayashi K, Ishikawa S, Kiba A et al. 2020. The putative sensor histidine kinase PhcK is required for the full expression of phcA encoding the global transcriptional regulator to drive the quorum-sensing circuit of Ralstonia solanacearum strain OE1-1. Mol. Plant Pathol. 21:1591–605
    [Google Scholar]
  76. 76.
    Shaw PD, Ping G, Daly SL, Cha C, Cronan JE Jr. et al. 1997. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. PNAS 94:6036–41
    [Google Scholar]
  77. 77.
    Shinohara M, Nakajima N, Uehara Y. 2007. Purification and characterization of a novel esterase (β-hydroxypalmitate methyl ester hydrolase) and prevention of the expression of virulence by Ralstonia solanacearum. J. Appl. Microbiol. 103:152–62
    [Google Scholar]
  78. 78.
    Song S, Sun X, Guo Q, Cui B, Zhu Y et al. 2022. An anthranilic acid-responsive transcriptional regulator controls the physiology and pathogenicity of Ralstonia solanacearum. PLOS Pathog. 18:e1010562
    [Google Scholar]
  79. 79.
    Song S, Yin W, Sun X, Cui B, Huang L et al. 2020. Anthranilic acid from Ralstonia solanacearum plays dual roles in intraspecies signalling and inter-kingdom communication. ISME J. 14:2248–60
    [Google Scholar]
  80. 80.
    Spraker JE, Sanchez LM, Lowe TM, Dorrestein PC, Keller NP. 2016. Ralstonia solanacearum lipopeptide induces chlamydospore development in fungi and facilitates bacterial entry into fungal tissues. ISME J. 10:2317–30
    [Google Scholar]
  81. 81.
    Spraker JE, Wiemann P, Baccile JA, Venkatesh N, Schumacher J et al. 2018. Conserved responses in a war of small molecules between a plant-pathogenic bacterium and fungi. mBio 9:e00820–18
    [Google Scholar]
  82. 82.
    Stanley D, Batacan R Jr., Bajagai YS. 2002. Rapid growth of antimicrobial resistance: The role of agriculture in the problem and the solutions. Appl. Microbiol. Biotechnol. 106:6953–62
    [Google Scholar]
  83. 83.
    Stock AM, Robinson VL, Goudreau PN. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183–215
    [Google Scholar]
  84. 84.
    Takemura C, Senuma W, Hayashi K, Minami A, Terazawa Y et al. 2021. PhcQ mainly contributes to the regulation of quorum sensing-dependent genes, in which PhcR is partially involved, in Ralstonia pseudosolanacearum strain OE1-1. Mol Plant Pathol. 22:1538–52
    [Google Scholar]
  85. 85.
    Tang M, Bouchez O, Cruveiller S, Masson-Boivin C, Capela D. 2020. Modulation of quorum sensing as an adaptation to nodule cell infection during experimental evolution of legume symbionts. mBio 11:e03129–19
    [Google Scholar]
  86. 86.
    Tsumori C, Matsuo S, Murai Y, Kai K. 2022. Quorum sensing-dependent invasion of Ralstonia solanacearum into Fusarium oxysporum chlamydospores. bioRxiv 2022.11.03.515128, Nov. 4
  87. 87.
    Ujita Y, Sakata M, Yoshihara A, Hikichi Y, Kai K. 2019. Signal production and response specificity in the phc quorum sensing systems of Ralstonia solanacearum species complex. ACS Chem. Biol. 14:224351
    [Google Scholar]
  88. 88.
    Valls M, Genin S, Boucher C. 2006. Integrated regulation of the Type III secretion system and other virulence determinants in Ralstonia solanacearum. PLOS Pathog. 2:e82
    [Google Scholar]
  89. 89.
    Vasse J, Genin S, Frey P, Boucher C, Brito B. 2000. The hrpB and hrpG regulatory genes of Ralstonia solanacearum are required for different stages of the tomato root infection process. Mol. Plant Microbe Interact. 13:259–67
    [Google Scholar]
  90. 90.
    Vella P, Rudraraju RS, Lundbäck T, Axelsson H, Almqvist H et al. 2021. A FabG inhibitor targeting an allosteric binding site inhibits several orthologs from Gram-negative ESKAPE pathogens. Bioorg. Med. Chem. 30:115898
    [Google Scholar]
  91. 91.
    Venkatesh N, Greco C, Drott MT, Koss MJ, Ludwikoski I et al. 2022. Bacterial hitchhikers derive benefits from fungal housing. Curr. Biol. 32:1523–33
    [Google Scholar]
  92. 92.
    Wackler B, Schneider P, Jacobs JM, Pauly J, Allen C et al. 2011. Ralfuranone biosynthesis in Ralstonia solanacearum suggests functional divergence in the quinone synthetase family of enzymes. Chem. Biol. 18:354–60
    [Google Scholar]
  93. 93.
    Wakimoto T, Nakagishi S, Matsukawa N, Tani S, Kai K. 2020. A unique combination of two different quorum sensing systems in the β-rhizobium Cupriavidus taiwanensis. J. Nat. Prod. 83:1876–84
    [Google Scholar]
  94. 94.
    Wang LH, He Y, Gao Y, Wu JE, Dong YH et al. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol. Microbiol. 51:903–12
    [Google Scholar]
  95. 95.
    Waseem M, Williams JQL, Thangavel A, StillID PC, Ymele-Leki P. 2019. A structural analog of ralfuranones and flavipesins promotes biofilm formation by Vibrio cholerae. PLOS ONE 14:e0215273
    [Google Scholar]
  96. 96.
    Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21:319–46
    [Google Scholar]
  97. 97.
    Withers H, Swift S, Williams P. 2001. Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr. Opin. Microbiol. 4:186–93
    [Google Scholar]
  98. 98.
    Yan J, Li P, Wang X, Zhu M, Shi H et al. 2022. RasI/R quorum sensing system controls the virulence of Ralstonia solanacearum strain EP1. Appl. Environ. Microbiol. 88:e0032522
    [Google Scholar]
  99. 99.
    Ye P, Li X, Cui B, Song S, Shen F et al. 2022. Proline utilization A controls bacterial pathogenicity by sensing its substrate and cofactors. Commun. Biol. 5:496
    [Google Scholar]
  100. 100.
    Yoshihara A, Shimatani M, Sakata M, Takemura C, Senuma W et al. 2020. Quorum sensing inhibition attenuates the virulence of the plant pathogen Ralstonia solanacearum species complex. ACS Chem. Biol. 15:305059
    [Google Scholar]
  101. 101.
    Yoshimochi T, Zhang Y, Kiba A, Hikichi Y, Ohnishi K. 2009. Expression of hrpG and activation of response regulator HrpG are controlled by distinct signal cascades in Ralstonia solanacearum. J. Gen. Plant Pathol. 75:196–204
    [Google Scholar]
  102. 102.
    Zhou L, Yu Y, Chen X, Diab AA, Ruan L et al. 2015. The multiple DSF-family QS signals are synthesized from carbohydrate and branched-chain amino acids via the FAS elongation cycle. Sci. Rep. 5:13294
    [Google Scholar]
  103. 103.
    Zuluaga AP, Puigvert M, Valls M. 2013. Novel plant inputs influencing Ralstonia solanacearum during infection. Front. Microbiol. 4:349
    [Google Scholar]
/content/journals/10.1146/annurev-micro-032521-030537
Loading
/content/journals/10.1146/annurev-micro-032521-030537
Loading

Data & Media loading...

  • Article Type: Review Article
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