Functional characterization of copA gene encoding multicopper oxidase in xanthomonas campestris pv. campestris

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 17, 2011, Pages 9290-9302

  Hsiao, Yi Min ^a   Liu, Yu Fan ^b   Lee, Pei Yu ^a   Hsu, Pei Chi ^a   Tseng, Szu Yu ^a   Pan, Yu Chien ^a  

^a CENTRAL TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Multicopper oxidase; reporter assay; site directed mutagenesis; Xanthomonas

Indexed keywords

ALANINE SUBSTITUTION; BLACK ROT; CATABOLITE REPRESSION; CAUSATIVE AGENTS; COPPER BINDING; COPPER RESISTANCE GENES; COPPER TOLERANCE; FUNCTIONAL CHARACTERIZATION; MULTICOPPER OXIDASE; MUTATIONAL ANALYSIS; NITROGEN STARVATION; OSMOLARITY; OXIDASE ACTIVITY; OXYGEN LIMITATION; REPORTER ASSAY; SITE DIRECTED MUTAGENESIS; XANTHOMONAS; XANTHOMONAS CAMPESTRIS;

AMINO ACIDS; ASSAYS; BACTERICIDES; DISEASE CONTROL; ENCODING (SYMBOLS); GENE ENCODING; PLANTS (BOTANY); TRANSCRIPTION;

COPPER;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; COPA PROTEIN, BACTERIA; COPPER; COPPER OXIDASE; OXIDOREDUCTASE;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BRASSICACEAE; CHEMISTRY; ENZYMOLOGY; GENETICS; MICROBIOLOGY; MOLECULAR GENETICS; PLANT DISEASE; SITE DIRECTED MUTAGENESIS; XANTHOMONAS CAMPESTRIS;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BRASSICACEAE; COPPER; DRUG RESISTANCE, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OXIDOREDUCTASES; PLANT DISEASES; XANTHOMONAS CAMPESTRIS;

BRASSICA OLERACEA VAR. CAPITATA; NEGIBACTERIA; XANTHOMONAS; XANTHOMONAS CAMPESTRIS; XANTHOMONAS CAMPESTRIS PV. CAMPESTRIS;

EID: 80052578301     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf2024006     Document Type: Article

References (58)

1. Voloudakis, A. E.; Reignier, T. M.; Cooksey, D. A. Regulation of resistance to copper in Xanthomonas axonopodis pv. vesicatoria Appl. Environ. Microbiol. 2005, 71 (2) 782-789 (Pubitemid 40223563)
2. Cooksey, D. A.; Azad, H. R.; Cha, J. S.; Lim, C. K. Copper resistance gene homologs in pathogenic and saprophytic bacterial species from tomato Appl. Environ. Microbiol. 1990, 56 (2) 431-435 (Pubitemid 20055317)
3. Cooksey, D. A. Characterization of a copper resistance plasmid conserved in copper-resistant strains of Pseudomonas syringae pv. tomato Appl. Environ. Microbiol. 1987, 53 (2) 454-456 (Pubitemid 17004635)
4. Sundin, G. W.; Jones, A. L.; Fulbright, D. W. Copper resistance in Pseudomonas syringae pv. syringae from cherry orchards and its associated transfer in vitro and in planta with a plasmid Phytopathology 1989, 79, 861-865
5. Bender, C. L.; Cooksey, D. A. Indigenous plasmids in Pseudomonas syringae pv. tomato: conjugative transfer and role in copper resistance J. Bacteriol. 1986, 165 (2) 534-541 (Pubitemid 16060526)
6. Bender, C. L.; Malvick, D. K.; Conway, K. E.; George, S.; Pratt, P. Characterization of pXV10A, a copper resistance plasmid in Xanthomonas campestris pv. vesicatoria Appl. Environ. Microbiol. 1990, 56 (1) 170-175 (Pubitemid 20031198)
7. Lee, Y. A.; Hendson, M.; Panopoulos, N. J.; Schroth, M. N. Molecular cloning, chromosomal mapping, and sequence analysis of copper resistance genes from Xanthomonas campestris pv. juglandis: homology with small blue copper proteins and multicopper oxidase J. Bacteriol. 1994, 176 (1) 173-188 (Pubitemid 24014937)
8. Bender, C. L.; Cooksey, D. A. Molecular cloning of copper resistance genes from Pseudomonas syringae pv. tomato J. Bacteriol. 1987, 169 (2) 470-474 (Pubitemid 17010848)
9. Mellano, M. A.; Cooksey, D. A. Induction of the copper resistance operon from Pseudomonas syringae J. Bacteriol. 1988, 170 (9) 4399-4401
10. Mellano, M. A.; Cooksey, D. A. Nucleotide sequence and organization of copper resistance genes from Pseudomonas syringae pv. tomato J. Bacteriol. 1988, 170 (6) 2879-2883
11. Mills, S. D.; Jasalavich, C. A.; Cooksey, D. A. A two-component regulatory system required for copper-inducible expression of the copper resistance operon of Pseudomonas syringae J. Bacteriol. 1993, 175 (6) 1656-1664 (Pubitemid 23084127)
12. Teixeira, E. C.; Franco de Oliveira, J. C.; Marques Novo, M. T.; Bertolini, M. C. The copper resistance operon copAB from Xanthomonas axonopodis pathovar citri: gene inactivation results in copper sensitivity Microbiology 2008, 154 (Pt 2) 402-412 (Pubitemid 351292294)
13. da Silva, A. C.; Ferro, J. A.; Reinach, F. C.; Farah, C. S.; Furlan, L. R.; Quaggio, R. B.; Monteiro-Vitorello, C. B.; Van Sluys, M. A.; Almeida, N. F.; Alves, L. M.; do Amaral, A. M.; Bertolini, M. C.; Camargo, L. E.; Camarotte, G.; Cannavan, F.; Cardozo, J.; Chambergo, F.; Ciapina, L. P.; Cicarelli, R. M.; Coutinho, L. L.; Cursino-Santos, J. R.; El-Dorry, H.; Faria, J. B.; Ferreira, A. J.; Ferreira, R. C.; Ferro, M. I.; Formighieri, E. F.; Franco, M. C.; Greggio, C. C.; Gruber, A.; Katsuyama, A. M.; Kishi, L. T.; Leite, R. P.; Lemos, E. G.; Lemos, M. V.; Locali, E. C.; Machado, M. A.; Madeira, A. M.; Martinez-Rossi, N. M.; Martins, E. C.; Meidanis, J.; Menck, C. F.; Miyaki, C. Y.; Moon, D. H.; Moreira, L. M.; Novo, M. T.; Okura, V. K.; Oliveira, M. C.; Oliveira, V. R.; Pereira, H. A.; Rossi, A.; Sena, J. A.; Silva, C.; de Souza, R. F.; Spinola, L. A.; Takita, M. A.; Tamura, R. E.; Teixeira, E. C.; Tezza, R. I.; Trindade dos Santos, M.; Truffi, D.; Tsai, S. M.; White, F. F.; Setubal, J. C.; Kitajima, J. P. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities Nature 2002, 417 (6887) 459-463 (Pubitemid 34563540)
14. Behlau, F.; Canteros, B. I.; Minsavage, G. V.; Jones, J. B.; Graham, J. H. Molecular characterization of copper resistance genes from Xanthomonas citri subsp. citri and Xanthomonas alfalfae subsp. citrumelonis Appl. Environ. Microbiol. 2011, 77, 4089-4096
15. Voloudakis, A. E.; Bender, C. L.; Cooksey, D. A. Similarity between copper resistance genes from Xanthomonas campestris and Pseudomonas syringae Appl. Environ. Microbiol. 1993, 59 (5) 1627-1634 (Pubitemid 23141181)
16. Williams, P. H. Black rot: A continuing threat to world crucifers Plant Dis. 1980, 64 (8) 736-742
17. Miller, J. H. Experiments in Molecular Genetics; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1972.
18. Wengelnik, K.; Marie, C.; Russel, M.; Bonas, U. Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive reaction J. Bacteriol. 1996, 178 (4) 1061-1069 (Pubitemid 26048022)
19. Fu, J. F.; Tseng, Y. H. Construction of lactose-utilizing Xanthomonas campestris and production of xanthan gum from whey Appl. Environ. Microbiol. 1990, 56 (4) 919-923
20. Hsiao, Y. M.; Zheng, M. H.; Hu, R. M.; Yang, T. C.; Tseng, Y. H. Regulation of the pehA gene encoding the major polygalacturonase of Xanthomonas campestris by Clp and RpfF Microbiology 2008, 154 (Pt 3) 705-713
21. Jittawuttipoka, T.; Sallabhan, R.; Vattanaviboon, P.; Fuangthong, M.; Mongkolsuk, S. Mutations of ferric uptake regulator (fur) impair iron homeostasis, growth, oxidative stress survival, and virulence of Xanthomonas campestris pv. campestris Arch. Microbiol. 2010, 192 (5) 331-339
22. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular Cloning: A Laboratory Manual, 2 nd ed.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1989.
23. Hsiao, Y. M.; Liao, H. Y.; Lee, M. C.; Yang, T. C.; Tseng, Y. H. Clp upregulates transcription of engA gene encoding a virulence factor in Xanthomonas campestris by direct binding to the upstream tandem Clp sites FEBS Lett. 2005, 579 (17) 3525-3533
24. Sanger, F.; Nicklen, S.; Coulson, A. R. DNA sequencing with chain-terminating inhibitors Proc. Natl. Acad. Sci. U.S.A. 1977, 74 (12) 5463-5467
25. Wang, T. W.; Tseng, Y. H. Electrotransformation of Xanthomonas campestris by RF DNA of filamentous phageLf Lett. Appl. Microbiol. 1992, 14 (2) 65-68
26. Vieira, J.; Messing, J. New pUC-derived cloning vectors with different selectable markers and DNA replication origins Gene 1991, 100, 189-194
27. Schweizer, H. D. Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis Biotechniques 1993, 15 (5) 831-834
28. Keen, N. T.; Tamaki, S.; Kobayashi, D.; Trollinger, D. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria Gene 1988, 70 (1) 191-197 (Pubitemid 18263496)
29. Hsiao, Y. M.; Liu, Y. F.; Fang, M. C.; Song, W. L. XCC2731, a GGDEF domain protein in Xanthomonas campestris, is involved in bacterial attachment and is positively regulated by Clp. Microbiol Res 2011, in press.
30. Tang, J. L.; Liu, Y. N.; Barber, C. E.; Dow, J. M.; Wootton, J. C.; Daniels, M. J. Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris Mol. Gen. Genet. 1991, 226 (3) 409-417
31. Huston, W. M.; Naylor, J.; Cianciotto, N. P.; Jennings, M. P.; McEwan, A. G. Functional analysis of the multi-copper oxidase from Legionella pneumophila Microbes Infect. 2008, 10 (5) 497-503
32. Solano, F.; Lucas-Elio, P.; Lopez-Serrano, D.; Fernandez, E.; Sanchez-Amat, A. Dimethoxyphenol oxidase activity of different microbial blue multicopper proteins FEMS Microbiol. Lett. 2001, 204 (1) 175-181 (Pubitemid 33000053)
33. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
34. Lee, T. C.; Chen, S. T.; Lee, M. C.; Chang, C. M.; Chen, C. H.; Weng, S. F.; Tseng, Y. H. The early stages of filamentous phage Lf infection require the host transcription factor, Clp J. Mol. Microbiol. Biotechnol. 2001, 3 (3) 471-481
35. Vorholter, F. J.; Schneiker, S.; Goesmann, A.; Krause, L.; Bekel, T.; Kaiser, O.; Linke, B.; Patschkowski, T.; Ruckert, C.; Schmid, J.; Sidhu, V. K.; Sieber, V.; Tauch, A.; Watt, S. A.; Weisshaar, B.; Becker, A.; Niehaus, K.; Puhler, A. The genome of Xanthomonas campestris pv. campestris B100 and its use for the reconstruction of metabolic pathways involved in xanthan biosynthesis J. Biotechnol. 2008, 134 (1-2) 33-45
36. Qian, W.; Jia, Y.; Ren, S. X.; He, Y. Q.; Feng, J. X.; Lu, L. F.; Sun, Q.; Ying, G.; Tang, D. J.; Tang, H.; Wu, W.; Hao, P.; Wang, L.; Jiang, B. L.; Zeng, S.; Gu, W. Y.; Lu, G.; Rong, L.; Tian, Y.; Yao, Z.; Fu, G.; Chen, B.; Fang, R.; Qiang, B.; Chen, Z.; Zhao, G. P.; Tang, J. L.; He, C. Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris Genome Res. 2005, 15 (6) 757-767 (Pubitemid 41003099)
37. Yang, B. Y.; Tseng, Y. H. Production of exopolysaccharide and levels of protease and pectinase activity in pathogenic and non-pathogenic strains of Xanthomonas campestris pv. campestris Bot. Bull. Acad. Sin. 1988, 29, 93-99
38. Chan, J. W.; Goodwin, P. H. The molecular genetics of virulence of Xanthomonas campestris Biotechnol. Adv. 1999, 17 (6) 489-508 (Pubitemid 30044516)
39. Dow, J. M.; Daniels, M. J. Pathogenicity determinants and global regulation of pathogenicity of Xanthomonas campestris pv. campestris Curr. Top. Microbiol. Immunol. 1994, 192, 29-41 (Pubitemid 24344400)
40. Ryan, R. P.; Fouhy, Y.; Lucey, J. F.; Jiang, B. L.; He, Y. Q.; Feng, J. X.; Tang, J. L.; Dow, J. M. Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris Mol. Microbiol. 2007, 63 (2) 429-442 (Pubitemid 46058930)
41. Messerschmidt, A.; Rossi, A.; Ladenstein, R.; Huber, R.; Bolognesi, M.; Gatti, G.; Marchesini, A.; Petruzzelli, R.; Finazzi-Agro, A. X-ray crystal structure of the blue oxidase ascorbate oxidase from zucchini. Analysis of the polypeptide fold and a model of the copper sites and ligands J. Mol. Biol. 1989, 206 (3) 513-529
42. Messerschmidt, A.; Ladenstein, R.; Huber, R.; Bolognesi, M.; Avigliano, L.; Petruzzelli, R.; Rossi, A.; Finazzi-Agro, A. Refined crystal structure of ascorbate oxidase at 1.9 A resolution J. Mol. Biol. 1992, 224 (1) 179-205
43. Taylor, A. B.; Stoj, C. S.; Ziegler, L.; Kosman, D. J.; Hart, P. J. The copper-iron connection in biology: structure of the metallo-oxidase Fet3p Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (43) 15459-15464 (Pubitemid 41528079)
44. Roberts, S. A.; Weichsel, A.; Grass, G.; Thakali, K.; Hazzard, J. T.; Tollin, G.; Rensing, C.; Montfort, W. R. Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (5) 2766-2771 (Pubitemid 34240535)
45. Ueki, Y.; Inoue, M.; Kurose, S.; Kataoka, K.; Sakurai, T. Mutations at Asp112 adjacent to the trinuclear Cu center in CueO as the proton donor in the four-electron reduction of dioxygen FEBS Lett. 2006, 580 (17) 4069-4072 (Pubitemid 44037572)
46. Sanchez-Sutil, M. C.; Gomez-Santos, N.; Moraleda-Munoz, A.; Martins, L. O.; Perez, J.; Munoz-Dorado, J. Differential expression of the three multicopper oxidases from Myxococcus xanthus J. Bacteriol. 2007, 189 (13) 4887-4898 (Pubitemid 47025601)
47. Sakurai, T.; Kataoka, K. Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase Chem. Rec. 2007, 7 (4) 220-229
48. Sakurai, T.; Kataoka, K. Structure and function of type I copper in multicopper oxidases Cell. Mol. Life Sci. 2007, 64 (19-20) 2642-2656 (Pubitemid 350035609)
49. Giardina, P.; Faraco, V.; Pezzella, C.; Piscitelli, A.; Vanhulle, S.; Sannia, G. Laccases: a never-ending story Cell. Mol. Life Sci. 2010, 67 (3) 369-385
50. Katzen, F.; Becker, A.; Zorreguieta, A.; Puhler, A.; Ielpi, L. Promoter analysis of the Xanthomonas campestris pv. campestris gum operon directing biosynthesis of the xanthan polysaccharide J. Bacteriol. 1996, 178 (14) 4313-4318 (Pubitemid 26240918)
51. He, Y. W.; Xu, M.; Lin, K.; Ng, Y. J.; Wen, C. M.; Wang, L. H.; Liu, Z. D.; Zhang, H. B.; Dong, Y. H.; Dow, J. M.; Zhang, L. H. Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell-cell communication-dependent genes and functions Mol. Microbiol. 2006, 59 (2) 610-622
52. He, Y. W.; Ng, A. Y.; Xu, M.; Lin, K.; Wang, L. H.; Dong, Y. H.; Zhang, L. H. Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network Mol. Microbiol. 2007, 64 (2) 281-292 (Pubitemid 46632629)
53. Tseng, Y. H.; Choy, K. T.; Hung, C. H.; Lin, N. T.; Liu, J. Y.; Lou, C. H.; Yang, B. Y.; Wen, F. S.; Weng, S. F.; Wu, J. R. Chromosome map of Xanthomonas campestris pv. campestris 17 with locations of genes involved in xanthan gum synthesis and yellow pigmentation J. Bacteriol. 1999, 181 (1) 117-125
54. Thieme, F.; Koebnik, R.; Bekel, T.; Berger, C.; Boch, J.; Buttner, D.; Caldana, C.; Gaigalat, L.; Goesmann, A.; Kay, S.; Kirchner, O.; Lanz, C.; Linke, B.; McHardy, A. C.; Meyer, F.; Mittenhuber, G.; Nies, D. H.; Niesbach-Klosgen, U.; Patschkowski, T.; Ruckert, C.; Rupp, O.; Schneiker, S.; Schuster, S. C.; Vorholter, F. J.; Weber, E.; Puhler, A.; Bonas, U.; Bartels, D.; Kaiser, O. Insights into genome plasticity and pathogenicity of the plant pathogenic bacterium Xanthomonas campestris pv. vesicatoria revealed by the complete genome sequence J. Bacteriol. 2005, 187 (21) 7254-7266 (Pubitemid 41507782)
55. Lee, B. M.; Park, Y. J.; Park, D. S.; Kang, H. W.; Kim, J. G.; Song, E. S.; Park, I. C.; Yoon, U. H.; Hahn, J. H.; Koo, B. S.; Lee, G. B.; Kim, H.; Park, H. S.; Yoon, K. O.; Kim, J. H.; Jung, C. H.; Koh, N. H.; Seo, J. S.; Go, S. J. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice Nucleic Acids Res. 2005, 33 (2) 577-586 (Pubitemid 40360987)
56. Messerschmidt, A.; Luecke, H.; Huber, R. X-ray structures and mechanistic implications of three functional derivatives of ascorbate oxidase from zucchini. Reduced, peroxide and azide forms J. Mol. Biol. 1993, 230 (3) 997-1014 (Pubitemid 23159940)
57. Blackburn, N. J.; Ralle, M.; Hassett, R.; Kosman, D. J. Spectroscopic analysis of the trinuclear cluster in the Fet3 protein from yeast, a multinuclear copper oxidase Biochemistry 2000, 39 (9) 2316-2324 (Pubitemid 30130081)
58. Hanahan, D. Studies on transformation of Escherichia coli with plasmids J. Mol. Biol. 1983, 166 (4) 557-580 (Pubitemid 13027898)