A LOV protein modulates the physiological attributes of xanthomonas axonopodis pv. citri relevant for host plant colonization

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Kraiselburd, Ivana ^a   Alet, Analía I ^a   Tondo, María Laura ^a   Petrocelli, Silvana ^a   Daurelio, Lucas D ^a   Monzón, Jesica ^a   Ruiz, Oscar A ^b   Losi, Aba ^c   Orellano, Elena G ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

^c UNIVERSITY OF PARMA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EXOPOLYSACCHARIDE; LOV PROTEIN; PHYTOCHROME; UNCLASSIFIED DRUG; BACTERIAL POLYSACCHARIDE; PROTEIN HISTIDINE KINASE; PROTEIN KINASE; PROTEIN-HISTIDINE KINASE; RECOMBINANT PROTEIN;

ABIOTIC STRESS; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BIOFILM; BIOTIC STRESS; CANKER; CONTROLLED STUDY; ESCHERICHIA COLI; GENE SEQUENCE; GENETIC CODE; GRAM NEGATIVE BACTERIUM; INOCULATION; LOV GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOCHEMISTRY; PHOTORECEPTOR; PLANT PATHOGEN INTERACTION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SPECTROSCOPY; WILD TYPE; XANTHOMONAS AXONOPODIS; XANTHOMONAS CITRI; AMINO ACID SEQUENCE; BACTERIAL COUNT; BACTERIUM ADHERENCE; BIOLOGY; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; SWEET ORANGE;

BACTERIA (MICROORGANISMS); CITRUS; CITRUS SINENSIS; ESCHERICHIA COLI; NEGIBACTERIA; XANTHOMONAS; XANTHOMONAS AXONOPODIS PV. CITRI;

AMINO ACID SEQUENCE; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CITRUS SINENSIS; COLONY COUNT, MICROBIAL; COMPUTATIONAL BIOLOGY; GENE DELETION; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; MOVEMENT; PHOTOCHEMICAL PROCESSES; PLANT DISEASES; PLANT LEAVES; POLYSACCHARIDES, BACTERIAL; PROTEIN KINASES; RECOMBINANT PROTEINS; XANTHOMONAS AXONOPODIS;

EID: 84861845108     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038226     Document Type: Article

References (86)

1. Bechtold U, Karpinski S, Mullineaux PM, (2005) The influence of the light environment and photosynthesis on oxidative signalling responses in plant-biotrophic pathogen interactions. Plant Cell & Environment 28: 1046-1055.
2. Guo A, Reimers PJ, Leach JE, (1993) Effect of light on incompatible interactions between Xanthomonas oryzae pv oryzae and rice. Physiol Mol Plant Pathol 42: 413-425.
3. Griebel T, Zeier J, (2008) Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol 147: 790-801.
4. van der Horst MA, Key J, Hellingwerf KJ, (2007) Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too. Trends Microbiol 15: 554-562.
5. Gomelsky M, Hoff WD, (2011) Light helps bacteria make important lifestyle decisions. Trends Microbiol 19: 441-448.
6. Losi A, (2004) The bacterial counterparts of plant phototropins. Photochem Photobiol Sci 3: 566-574.
7. Swartz TE, Tseng TS, Frederickson MA, Paris G, Comerci DJ, et al. (2007) Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317: 1090-1093.
8. Crosson S, Rajagopal S, Moffat K, (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42: 2-10.
9. van der Horst MA, Hellingwerf KJ, (2004) Photoreceptor proteins, "star actors of modern times": a review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc Chem Res 37: 13-20.
10. Moglich A, Ayers RA, Moffat K, (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17: 1282-1294.
11. Galperin MY, Nikolskaya AN, Koonin EV, (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203: 11-21.
12. Christie JM, (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58: 21-45.
13. Salomon M, Christie JM, Knieb E, Lempert U, Briggs WR, (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. Biochemistry 39: 9401-9410.
14. Losi A, Gartner W, (2011) Old chromophores, new photoactivation paradigms, trendy applications: flavins in blue light-sensing photoreceptors(dagger). Photochem Photobiol 87: 491-510.
15. Herrou J, Crosson S, (2011) Function, structure and mechanism of bacterial photosensory LOV proteins. Nat Rev Microbiol 9: 713-723.
16. Losi A, (2007) Flavin-based Blue-Light photosensors: a photobiophysics update. Photochem Photobiol 83: 1283-1300.
17. Kottke T, Heberle J, Hehn D, Dick B, Hegemann P, (2003) Phot-LOV1: photocycle of a blue-light receptor domain from the green alga Chlamydomonas reinhardtii. Biophys J 84: 1192-1201.
18. Mussi MA, Gaddy JA, Cabruja M, Arivett BA, Viale AM, et al. (2010) The opportunistic human pathogen Acinetobacter baumannii senses and responds to light. J Bacteriol 192: 6336-6345.
19. Tschowri N, Busse S, Hengge R, (2009) The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli. Genes Dev 23: 522-534.
20. Ondrusch N, Kreft J, (2011) Blue and red light modulates SigB-dependent gene transcription, swimming motility and invasiveness in Listeria monocytogenes. PLoS One 6: e16151.
21. Avila-Perez M, Hellingwerf KJ, Kort R, (2006) Blue light activates the sigmaB-dependent stress response of Bacillus subtilis via YtvA. J Bacteriol 188: 6411-6414.
22. Gaidenko TA, Kim TJ, Weigel AL, Brody MS, Price CW, (2006) The blue-light receptor YtvA acts in the environmental stress signaling pathway of Bacillus subtilis. J Bacteriol 188: 6387-6395.
23. Purcell EB, Siegal-Gaskins D, Rawling DC, Fiebig A, Crosson S, (2007) A photosensory two-component system regulates bacterial cell attachment. Proc Natl Acad Sci U S A 104: 18241-18246.
24. Kanazawa T, Ren S, Maekawa M, Hasegawa K, Arisaka F, et al. (2010) Biochemical and physiological characterization of a BLUF protein-EAL protein complex involved in blue light-dependent degradation of cyclic diguanylate in the purple bacterium Rhodopseudomonas palustris. Biochemistry 49: 10647-10655.
25. Losi A, Gartner W, (2008) Bacterial bilin- and flavin-binding photoreceptors. Photochem Photobiol Sci 7: 1168-1178.
26. Idnurm A, Crosson S, (2009) The photobiology of microbial pathogenesis. PLoS Pathog 5: e1000470.
27. Cao Z, Buttani V, Losi A, Gartner W, (2008) A blue light inducible two-component signal transduction system in the plant pathogen Pseudomonas syringae pv. tomato. Biophys J 94: 897-905.
28. Oberpichler I, Rosen R, Rasouly A, Vugman M, Ron EZ, et al. (2008) Light affects motility and infectivity of Agrobacterium tumefaciens. Environ Microbiol 10: 2020-2029.
29. Brunings AM, Gabriel DW, (2003) Xanthomonas citri: breaking the surface. Mol Plant Pathol 4: 141-157.
30. Graham JH, Gottwald TR, Cubero J, Achor DS, (2004) Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Molecular Plant Pathology 5: 1-15.
31. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, et al. (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417: 459-463.
32. Van Sluys MA, Monteiro-Vitorello CB, Camargo LE, Menck CF, da Silva AC, et al. (2002) Comparative genomic analysis of plant-associated bacteria. Annu Rev Phytopathol 40: 169-189.
33. Huala E, Oeller PW, Liscum E, Han IS, Larsen E, et al. (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278: 2120-2123.
34. Harshey RM, (2003) Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57: 249-273.
35. Astua-Monge G, Freitas-Astua J, Bacocina G, Roncoletta J, Carvalho SA, et al. (2005) Expression profiling of virulence and pathogenicity genes of Xanthomonas axonopodis pv. citri. J Bacteriol 187: 1201-1205.
36. Sigrist CJ, Cerutti L, Hulo N, Gattiker A, Falquet L, et al. (2002) PROSITE: a documented database using patterns and profiles as motif descriptors. Brief Bioinform 3: 265-274.
37. Krauss U, Losi A, Gartner W, Jaeger KE, Eggert T, (2005) Initial characterization of a blue-light sensing, phototropin-related protein from Pseudomonas putida: a paradigm for an extended LOV construct. Phys Chem Chem Phys 7: 2804-2811.
38. Hendrischk AK, Moldt J, Fruhwirth SW, Klug G, (2009) Characterization of an unusual LOV domain protein in the alpha-proteobacterium Rhodobacter sphaeroides. Photochem Photobiol 85: 1254-1259.
39. Hofmann K, Stoffel W, (1993) TMbase- A database of membrane spanning proteins segments. Biol Chem Hoppe-Seyler 374: 166.
40. Semmler AB, Whitchurch CB, Mattick JS, (1999) A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology 145 (Pt 10): 2863-2873.
41. Mattick JS, (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56: 289-314.
42. Dunger G, Relling VM, Tondo ML, Barreras M, Ielpi L, et al. (2007) Xanthan is not essential for pathogenicity in citrus canker but contributes to Xanthomonas epiphytic survival. Arch Microbiol 188: 127-135.
43. Buttner D, Bonas U, (2010) Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev 34: 107-133.
44. Römling U, Bian Z, Hammar M, Sierralta WD, Normark S, (1998) Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180: 722-731.
45. Friedman L, Kolter R, (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51: 675-690.
46. Dow JM, Crossman L, Findlay K, He YQ, Feng JX, et al. (2003) Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A 100: 10995-11000.
47. 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: 1061-1069.
48. Koebnik R, Kruger A, Thieme F, Urban A, Bonas U, (2006) Specific binding of the Xanthomonas campestris pv. vesicatoria AraC-type transcriptional activator HrpX to plant-inducible promoter boxes. J Bacteriol 188: 7652-7660.
49. Qian W, Han ZJ, He C, (2008) Two-component signal transduction systems of Xanthomonas spp.: a lesson from genomics. Mol Plant Microbe Interact 21: 151-161.
50. Galperin MY, (2010) Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13: 150-159.
51. Swartz TE, Corchnoy SB, Christie JM, Lewis JW, Szundi I, et al. (2001) The photocycle of a flavin-binding domain of the blue light photoreceptor phototropin. J Biol Chem 276: 36493-36500.
52. Losi A, Quest B, Gartner W, (2003) Listening to the blue: the time-resolved thermodynamics of the bacterial blue-light receptor YtvA and its isolated LOV domain. Photochem Photobiol Sci 2: 759-766.
53. Losi A, Kottke T, Hegemann P, (2004) Recording of blue light-induced energy and volume changes within the wild-type and mutated phot-LOV1 domain from Chlamydomonas reinhardtii. Biophys J 86: 1051-1060.
54. Zoltowski BD, Vaccaro B, Crane BR, (2009) Mechanism-based tuning of a LOV domain photoreceptor. Nat Chem Biol 5: 827-834.
55. Raffelberg S, Mansurova M, Gartner W, Losi A, (2011) Modulation of the photocycle of a LOV domain photoreceptor by the hydrogen-bonding network. J Am Chem Soc 133: 5346-5356.
56. Song SH, Freddolino PL, Nash AI, Carroll EC, Schulten K, et al. (2011) Modulating LOV domain photodynamics with a residue alteration outside the chromophore binding site. Biochemistry 50: 2411-2423.
57. Gottig N, Garavaglia BS, Garofalo CG, Orellano EG, Ottado J, (2009) A filamentous hemagglutinin-like protein of Xanthomonas axonopodis pv. citri, the phytopathogen responsible for citrus canker, is involved in bacterial virulence. PLoS One 4: e4358.
58. Macnab RM, (2003) How bacteria assemble flagella. Annu Rev Microbiol 57: 77-100.
59. Rigano LA, Siciliano F, Enrique R, Sendin L, Filippone P, et al. (2007) Biofilm formation, epiphytic fitness, and canker development in Xanthomonas axonopodis pv. citri. Mol Plant Microbe Interact 20: 1222-1230.
60. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM, (1995) Microbial biofilms. Annu Rev Microbiol 49: 711-745.
61. Stoodley P, Sauer K, Davies DG, Costerton JW, (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56: 187-209.
62. Branda SS, Vik S, Friedman L, Kolter R, (2005) Biofilms: the matrix revisited. Trends Microbiol 13: 20-26.
63. Karatan E, Watnick P, (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73: 310-347.
64. Malamud F, Torres PS, Roeschlin R, Rigano LA, Enrique R, et al. (2011) The Xanthomonas axonopodis pv. citri flagellum is required for mature biofilm and canker development. Microbiology 157: 819-829.
65. Crossman L, Dow JM, (2004) Biofilm formation and dispersal in Xanthomonas campestris. Microbes Infect 6: 623-629.
66. Li J, Wang N, (2011) Genome-wide mutagenesis of Xanthomonas axonopodis pv. citri reveals novel genetic determinants and regulation mechanisms of biofilm formation. PLoS One 6: e21804.
67. Purcell EB, Boutte CC, Crosson S, (2008) Two-component signaling systems and cell cycle control in Caulobacter crescentus. Adv Exp Med Biol 631: 122-130.
68. Gerlach RG, Hensel M, (2007) Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 297: 401-415.
69. O'Toole GA, Kolter R, (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
70. O'Toole GA, Kolter R, (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28: 449-461.
71. Soto GE, Hultgren SJ, (1999) Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol 181: 1059-1071.
72. Lemon KP, Higgins DE, Kolter R, (2007) Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189: 4418-4424.
73. Tondo ML, Petrocelli S, Ottado J, Orellano EG, (2010) The monofunctional catalase KatE of Xanthomonas axonopodis pv. citri is required for full virulence in citrus plants. PLoS One 5: e10803.
74. Green J, Paget MS, (2004) Bacterial redox sensors. Nat Rev Microbiol 2: 954-966.
75. Hellingwerf KJ, Hoff WD, Crielaard W, (1996) Photobiology of microorganisms: how photosensors catch a photon to initialize signalling. Mol Microbiol 21: 683-693.
76. Gottig N, Garavaglia BS, Daurelio LD, Valentine A, Gehring C, et al. (2008) Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide-like protein to modify host homeostasis. Proc Natl Acad Sci U S A 105: 18631-18636.
77. Purcell EB, McDonald CA, Palfey BA, Crosson S, (2010) An analysis of the solution structure and signaling mechanism of LovK, a sensor histidine kinase integrating light and redox signals. Biochemistry 49: 6761-6770.
78. Daurelio LD, Tondo ML, Dunger G, Gottig N, Ottado J, et al. (2009) Hypersensitive response. In: Narwal SS, Catalán AN, Sampietro DA, Vattuone MA, Polyticka B, editors. Book on Plant Bioassays Section II. Plant-microorganisms interactions. Houston Studium Press, LLC pp. 187-206.
79. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular cloning. a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
80. Losi A, Ternelli E, Gartner W, (2004) Tryptophan fluorescence in the Bacillus subtilis phototropin-related protein YtvA as a marker of interdomain interaction. Photochem Photobiol 80: 150-153.
81. Kearns DB, Losick R, (2004) Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 49: 581-590.
82. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
83. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
84. Simon R, Priefer U, Pühler A, (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1, 784-791.
85. Reece KS, Phillips GJ, (1995) New plasmids carrying antibiotic-resistance cassettes. Gene 165: 141-142.
86. Katzen F, Becker A, Ielmini MV, Oddo CG, Ielpi L, (1999) New mobilizable vectors suitable for gene replacement in gram-negative bacteria and their use in mapping of the 3' end of the Xanthomonas campestris pv. campestris gum operon. Appl Environ Microbiol 65: 278-282.