Chemotactic signal transduction and phosphate metabolism as adaptive strategies during citrus canker induction by Xanthomonas citri

Functional and Integrative Genomics

Volumn 15, Issue 2, 2015, Pages 197-210

  Moreira, Leandro Marcio ^a   Facincani, Agda Paula ^b   Ferreira, Cristiano Barbalho ^b   Ferreira, Rafael Marine ^b   Ferro, Maria Inês Tiraboshi ^b   Gozzo, Fabio Cesar ^c   de Oliveira, Julio Cezar Franco ^d   Ferro, Jesus Aparecido ^b   Soares, Márcia Regina ^e  

^a FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c UNIVERSITY OF CAMPINAS   (Brazil)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Chemotaxis signal transduction; Phosphate metabolism; Two component systems PhoBR and PhoPQ; Virulence; Xanthomonas adaptation

Indexed keywords

ARTICLE; BACTERIAL VIRULENCE; BINDING SITE; CANKER; CHEMOTAXIS; CITRUS CANKER; CONTROLLED STUDY; DISEASE ASSOCIATION; GENE CONTROL; MCP GENE; NONHUMAN; PHOSPHATE METABOLISM; PLANT GENE; PLANT PATHOGEN INTERACTION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEOMICS; PST GENE; PSTB GENE; SIGNAL TRANSDUCTION; XAC GENE; XANTHOMONAS CITRI; ADAPTATION; CITRUS; FLAGELLUM; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; REGULON; XANTHOMONAS;

BACTERIAL PROTEIN; PHOB PROTEIN, BACTERIA; PHOP PROTEIN, BACTERIA; PHOSPHATE; TRANSCRIPTION FACTOR;

ADAPTATION, BIOLOGICAL; BACTERIAL PROTEINS; BINDING SITES; CHEMOTAXIS; CITRUS; FLAGELLA; MUTATION; PHOSPHATES; PLANT DISEASES; REGULON; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; XANTHOMONAS;

EID: 84925521293     PISSN: 1438793X     EISSN: 14387948     Source Type: Journal    
DOI: 10.1007/s10142-014-0414-z     Document Type: Article

References (46)

1. Agusti G, Astola O, Rodriguez-Guell E, Julian E, Luquin M (2008) Surface spreading motility shown by a group of phylogenetically related, rapidly growing pigmented mycobacteria suggests that motility is a common property of mycobacterial species but is restricted to smooth colonies. J Bacteriol 190(20):6894–6902. doi:10.1128/Jb.00572-08
2. Ames P, Parkinson JS (1994) Constitutively signaling fragments of Tsr, the Escherichia coli Serine chemoreceptor. J Bacteriol 176(20):6340–6348
3. Antunez-Lamas M, Cabrera-Ordonez E, Lopez-Solanilla E, Raposo R, Trelles-Salazar O, Rodriguez-Moreno A, Rodriguez-Palenzuela P (2009) Role of motility and chemotaxis in the pathogenesis of Dickeya dadantii 3937 (ex Erwinia chrysanthemi 3937). Microbiology 155(Pt 2):434–442. doi:10.1099/mic. 0.022244-0
4. Bains M, Fernandez L, Hancock RE (2012) Phosphate starvation promotes swarming motility and cytotoxicity of Pseudomonas aeruginosa. Appl Environ Microbiol 78(18):6762–6768. doi:10.1128/AEM. 01015-12
5. Bateman A, Birney E, Durbin R, Eddy SR, Howe KL, Sonnhammer EL (2000) The Pfam protein families database. Nucleic Acids Res 28(1):263–266. doi:10.1093/nar/28.1.263
6. Berg HC (1991) Bacterial motility: handedness and symmetry. Ciba Found Symp 162:58–69
7. Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58(15–16):4019–4026. doi:10.1093/jxb/erm298
8. Branda SS, Vik A, Friedman L, Kolter R (2005) Biofilms: the matrix revisited. Trends Microbiol 13(1):20–26. doi:10.1016/j.tim.2004.11.006
9. Broek AV, Vanderleyden J (1995) The role of bacterial motility, chemotaxis, and attachment in bacteria plant interactions. Mol Plant-Microbe Interact 8(6):800–810. doi:10.1094/Mpmi-8-0800
10. Chagnot C, Zorgani MA, Astruc T, Desvaux M (2013) Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol 4:303. doi:10.3389/fmicb.2013.00303
11. Cox GB, Rosenberg H, Downie JA, Silver S (1981) Genetic analysis of mutants affected in the Pst inorganic phosphate transport system. J Bacteriol 148(1):1–9
12. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, Quaggio RB, Monteiro-Vitorello CB, Van Sluys MA, Almeida NF, Alves LM, do Amaral AM, Bertolini MC, Camargo LE, Camarotte G, Cannavan F, Cardozo J, Chambergo F, Ciapina LP, Cicarelli RM, Coutinho LL, Cursino-Santos JR, El-Dorry H, Faria JB, Ferreira AJ, Ferreira RC, Ferro MI, Formighieri EF, Franco MC, Greggio CC, Gruber A, Katsuyama AM, Kishi LT, Leite RP, Lemos EG, Lemos MV, Locali EC, Machado MA, Madeira AM, Martinez-Rossi NM, Martins EC, Meidanis J, Menck CF, Miyaki CY, Moon DH, Moreira LM, Novo MT, Okura VK, Oliveira MC, Oliveira VR, Pereira HA, Rossi A, Sena JA, Silva C, de Souza RF, Spinola LA, Takita MA, Tamura RE, Teixeira EC, Tezza RI, Trindade dos Santos M, Truffi D, Tsai SM, White FF, Setubal JC, Kitajima JP (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417(6887):459–463. doi:10.1038/417459a
13. Danhorn T, Hentzer M, Givskov M, Parsek MR, Fuqua C (2004) Phosphorus limitation enhances biofilm formation of the plant pathogen Agrobacterium tumefaciens through the PhoR-PhoB regulatory system. J Bacteriol 186(14):4492–4501. doi:10.1128/JB.186.14.4492-4501.2004
14. de Jong A, Pietersma H, Cordes M, Kuipers OP, Kok J (2012) PePPER: a webserver for prediction of prokaryote promoter elements and regulons. BMC Genomics 13:299. doi:10.1186/1471-2164-13-299
15. Eisenbach M (1996) Control of bacterial chemotaxis. Mol Microbiol 20(5):903–910. doi:10.1111/j.1365-2958.1996.tb02531.x
16. Facincani AP, Moreira LM, Soares MR, Ferreira CB, Ferreira RM, Ferro MIT, Ferro JA, Gozzo FC, de Oliveira JCF (2013) Comparative proteomic analysis reveals that T3SS, Tfp, and xanthan gum are key factors in initial stages of Citrus sinensis infection by Xanthomonas citri subsp. citri. Funct Integr Genomics 14(1):205–217. doi:10.1007/s10142-013-0340-5
17. Falke JJ, Bass RB, Butler SL, Chervitz SA, Danielson MA (1997) The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu Rev Cell Dev Biol 13:457–512. doi:10.1146/annurev.cellbio.13.1.457
18. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18(3):265–276. doi:10.1046/j.1365-313X.1999.00265.x
19. Gerardo NM, Jacobs SR, Currie CR, Mueller UG (2006) Ancient host-pathogen associations maintained by specificity of chemotaxis and antibiosis. PLoS Biol 4(8):e235. doi:10.1371/journal.pbio.0040235
20. Gristwood T, Fineran PC, Everson L, Williamson NR, Salmond GP (2009) The PhoBR two-component system regulates antibiotic biosynthesis in Serratia in response to phosphate. BMC Microbiol 9:112. doi:10.1186/1471-2180-9-112
21. Harshey RM (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57:249–273. doi:10.1146/annurev.micro.57.030502.091014
22. Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30
23. Kearns DB (2010) A field guide to bacterial swarming motility. Nat Rev Microbiol 8(9):634–644. doi:10.1038/nrmicro2405
24. Kim SK, Makino K, Amemura M, Shinagawa H, Nakata A (1993) Molecular analysis of the Phoh gene, belonging to the phosphate regulon in Escherichia coli. J Bacteriol 175(5):1316–1324
25. Laia ML, Moreira LM, Dezajacomo J, Brigati JB, Ferreira CB, Ferro MI, Silva AC, Ferro JA, Oliveira JC (2009) New genes of Xanthomonas citri subsp. citri involved in pathogenesis and adaptation revealed by a transposon-based mutant library. BMC Microbiol 9:12. doi:10.1186/1471-2180-9-12
26. Lamarche MG, Wanner BL, Crepin S, Harel J (2008) The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol Rev 32(3):461–473. doi:10.1111/j.1574-6976.2008.00101.x
27. Lux R, Shi WY (2004) Chemotaxis-guided movements in bacteria. Crit Rev Oral Biol Med 15(4):207–220. doi:10.1177/154411130401500404
28. Malamud F, Torres PS, Roeschlin R, Rigano LA, Enrique R, Bonomi HR, Castagnaro AP, Marano MR, Vojnov AA (2011) The Xanthomonas axonopodis pv. citri flagellum is required for mature biofilm and canker development. Microbiol-Sgm 157:819–829. doi:10.1099/Mic. 0.044255-0
29. Merritt PM, Danhorn T, Fuqua C (2007) Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189(22):8005–8014. doi:10.1128/JB.00566-07
30. Mhedbi-Hajri N, Darrasse A, Pigne S, Durand K, Fouteau S, Barbe V, Manceau C, Lemaire C, Jacques MA (2011) Sensing and adhesion are adaptive functions in the plant pathogenic xanthomonads. BMC Evol Biol 11
31. Moreira LM, de Souza RF, Almeida NF Jr, Setubal JC, Oliveira JC, Furlan LR, Ferro JA, da Silva AC (2004) Comparative genomics analyses of citrus-associated bacteria. Annu Rev Phytopathol 42:163–184. doi:10.1146/annurev.phyto.42.040803.140310
32. Nadell CD, Xavier JB, Levin SA, Foster KR (2008) The evolution of quorum sensing in bacterial biofilms. PLoS Biol 6(1):e14. doi:10.1371/journal.pbio.0060014
33. Naito K, Taguchi F, Suzuki T, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2008) Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol Plant-Microbe Interact 21(9):1165–1174. doi:10.1094/Mpmi-21-9-1165
34. Olsen JE, Hoegh-Andersen KH, Casadesus J, Rosenkranzt J, Chadfield MS, Thomsen LE (2013) The role of flagella and chemotaxis genes in host pathogen interaction of the host adapted Salmonella enterica serovar Dublin compared to the broad host range serovar S. Typhimurium BMC Microbiol 13:67. doi:10.1186/1471-2180-13-67
35. Peters NK, Verma DPS (1990) Phenolic-compounds as regulators of gene-expression in plant-microbe interactions. Mol Plant-Microbe Interact 3(1):4–8. doi:10.1094/Mpmi-3-004
36. Rosenberg H, Gerdes RG, Chegwidden K (1977) Two systems for the uptake of phosphate in Escherichia coli. J Bacteriol 131(2):505–511
37. Rosenberg H, Russell LM, Jacomb PA, Chegwidden K (1982) Phosphate exchange in the pit transport system in Escherichia coli. J Bacteriol 149(1):123–130
38. Soares MR, Facincani AP, Ferreira RM, Moreira LM, de Oliveira JCF, Ferro JA, Ferro MIT, Meneghini R, Gozzo FC (2010) Proteome of the phytopathogen Xanthomonas citri subsp citri: a global expression profile. Proteome Sci 8:55. doi:10.1186/1477-5956-8-55
39. Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141(2):373–378. doi:10.1104/pp. 106.079467
40. Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, Michiels J (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16(10):496–506. doi:10.1016/j.tim.2008.07.004
41. Wang K, Kang L, Anand A, Lazarovits G, Mysore KS (2007) Monitoring in planta bacterial infection at both cellular and whole-plant levels using the green fluorescent protein variant GFPuv. New Phytol 174:212–223. doi:10.1111/j.1469-8137.2007.01999.x
42. Wanner BL (1993) Gene-regulation by phosphate in enteric bacteria. J Cell Biochem 51(1):47–54. doi:10.1002/jcb.240510110
43. Wengelnik K, Marie C, Russel M, Bonas U (1996) Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction ofthe hypersensitive reaction. J Bacteriol 178(4):1061–1069
44. Willsky GR, Malamy MH (1980) Characterization of two genetically separable inorganic phosphate transport systems in Escherichia coli. J Bacteriol 144(1):356–365
45. Xu J, Kim J, Danhorn T, Merritt PM, Fuqua C (2012) Phosphorus limitation increases attachment in Agrobacterium tumefaciens and reveals a conditional functional redundancy in adhesin biosynthesis. Res Microbiol 163(9–10):674–684. doi:10.1016/j.resmic.2012.10.013
46. Yang TC, Leu YW, Chang-Chien HC, Hu RM (2009) Flagellar biogenesis of Xanthomonas campestris requires the alternative sigma factors RpoN2 and FliA and is temporally regulated by FlhA, FlhB, and FlgM. J Bacteriol 191(7):2266–2275. doi:10.1128/Jb.01152-08