The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
권호 표지
DOI QR코드

DOI QR Code

Identification of a Gene Encoding Adenylate Kinase Involved in Antifungal Activity Expression of the Biocontrol Strain Burkholderia pyrrocinia CH-67

  • Lee, Kwang Youll (Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute) ;
  • Kong, Hyun-Gi (Department of Applied Biology, Dong-A University) ;
  • Lee, Seon-Woo (Department of Applied Biology, Dong-A University)
  • Received : 2012.08.16
  • Accepted : 2012.09.25
  • Published : 2012.12.01
Download PDF
⟨ Previous Next ⟩

Abstract

Burkholderia pyrrocinia CH-67 is a biocontrol bacterium with strong antifungal activity against several plant pathogenic fungi. Transposon mutagenesis was performed to identify the genes responsible for the antifungal activity of B. pyrrocinia CH-67. Of the 2,500 mutants tested using the Fulvia fulva spore screening method, a mutant deficient in antifungal activity, M208, was selected. DNA sequence analysis of the transposon-inserted region revealed that a gene encoding an adenylate kinase-related kinase was disrupted in M208. Antifungal activity was restored in M208 when a full-length adenylate kinase gene with its promoter was introduced in trans. The deduced amino acid sequence of adenylate kinase from CH-67 was 80% identical to that of B. cenocepacia MCO-3. Adenosine diphosphate supplementation or high levels of adenosine triphosphate and adenosine monophosphate together restored antifungal activity in M208, suggesting that adenylate kinase of B. pyrrocinia CH-67 is involved in antifungal activity expression.

Keywords

References

  1. Andrews, J. H. 1992. Biological control in the phyllosphere. Annu. Rev. Phytopathol. 30:603-635. https://doi.org/10.1146/annurev.py.30.090192.003131
  2. Asaka, O. and Shoda, M. 1996. Biocontrol of Rhizoctonia solani damping-off of tomato with Bacillus subtilis RB14. Appl. Environ. Microbiol. 62:4081-4085.
  3. Becker, J. O. and Schwinn, F. J. 1993. Control of soil-borne pathogens with living bacteria and fungi: status and outlook. Pestic. Sci. 37:355-363. https://doi.org/10.1002/ps.2780370408
  4. Burkholder, W. H. 1950. Sour skin, a bacterial rot of onion bulbs. Phytopathology 40:115-118.
  5. Chiarini, L., Bevivino, A., Dalmastri, C., Tabacchioni, S. and Visca, P. 2006. Burkholderia cepacia complex species: health hazards and biotechnological potential. Trends Microbiol. 14:277-286. https://doi.org/10.1016/j.tim.2006.04.006
  6. Dennis, J. J. and Zylstra, G. J. 1998. Plasposons: modular selfcloning mini-transposon derivatives for the rapid genetic analysis of gram-negative bacterial genomes. Appl. Environ. Microbiol. 64:2710-2715.
  7. Dowling, D. N. and O'Gara, F. 1994. Metabolites of Pseudomonas involved in the biocontrol of plant disease. Trends Biotechnol. 12:133-141. https://doi.org/10.1016/0167-7799(94)90091-4
  8. Ehling-Schulz, M., Vukov, N., Schulz, A., Shaheen, R., Andersson, M., Martlbauer, E. and Scherer, S. 2005. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Appl. Environ. Microbiol. 71:105-113. https://doi.org/10.1128/AEM.71.1.105-113.2005
  9. El-Banna, N. and Winkelmann, G. 1998. Pyrrolnitrin from Burkholderia cepacia: antibiotic activity against fungi and novel activities against Streptomyces. J. Appl. Microbiol. 85:69-78. https://doi.org/10.1046/j.1365-2672.1998.00473.x
  10. Farr, D. F., Bills, G. F., Chamuris, G. P. and Rossman, A. Y. 1989. Fungi on Plants and Plant Products in the United States. American Phytopathological Society, St. Paul, Minn, USA
  11. Fenton, A. M., Stephens, P. M., Crowley, J., O'Callaghan, M. and O'Gara, F. 1992. Exploitation of gene(s) involved in 2,4- diacetylphloroglucinol biosynthesis to confer a new biocontrol capability to a Pseudomonas strain. Appl. Environ. Microbiol. 58:3873-3878.
  12. Figurski, D. H. and Helinski, D. R. 1979. Replication of an origin containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652. https://doi.org/10.1073/pnas.76.4.1648
  13. Glaser, M., Nulty, W. and Vagelos, P. R. 1975. Role of adenylate kinase in the regulation of macromolecular biosynthesis in a putative mutant of Escherichia coli defective in membrane phospholipid biosynthesis. J. Bacteriol. 123:128-136.
  14. Goelz, S. E. and Cronan, J. E. Jr. 1982. Adenylate kinase of Escherichia coli: evidence for a functional interaction in phospholipid synthesis. Biochemistry 21:189-195. https://doi.org/10.1021/bi00530a032
  15. Gu, G., Smith, L., Wang, N., Wang, H. and Lu, S.-E. 2009. Biosynthesis of an antifungal oligopeptide in Burkholderia contaminans strain MS14. Biochem. Biophys. Res. Commun. 380:328-332. https://doi.org/10.1016/j.bbrc.2009.01.073
  16. Gu, G., Smith, L., Liu, A. and Lu, S.-E. 2011. Genetic and biochemical map for the biosynthesis of occidiofungin, an antifungal produced by Burkholderia contaminans strain MS14. Appl. Environ. Microbiol. 77:6189-6198. https://doi.org/10.1128/AEM.00377-11
  17. Handelsman, J. and Stabb, E. V. 1996. Biocontrol of soilborn plant pathogens. Plant Cell 8:1855-1869. https://doi.org/10.1105/tpc.8.10.1855
  18. Hill, D. S., Stein, J. I., Torkewitz, N. R., Morse, A. M., Howell, C. R., Pachlatko, J. P., Becker, J. O. and Ligon, J. M. 1994. Cloning of genes involved in the synthesis of pyrrolnitrin from Pseudomonas fluorescens and role of pyrrolnitrin synthesis in biological control of plant disease. Appl. Environ. Microbiol. 60:78-85.
  19. Hoffman, L. M., Jendrisak, J. J., Meis, R. J., Goryshin, I. Y. and Reznikof, S. W. 2000. Transposome insertional mutagenesis and direct sequencing of microbial genomes. Genetica. 108:19-24. https://doi.org/10.1023/A:1004083307819
  20. Holmes, A., Govan, J. and Goldstein, R. 1998. Agricultural use of Burkholderia (Pseudomonas) cepacia: a threat to human health? Emerg. Infect. Dis. 4:221-227. https://doi.org/10.3201/eid0402.980209
  21. Horecka, J. and Jigami, Y. 2000. Identifying tagged transposon insertion sites in yeast by direct genomic sequencing. Yeast 16:967-970. https://doi.org/10.1002/1097-0061(200007)16:10<967::AID-YEA597>3.0.CO;2-G
  22. Howell, C. R. and Stipanovic, R. D. 1980. Suppression of Pythium ultimum induced damping-off of cotton seedlings by Pseudomonas fluorescens and its antibiotic pyoluteorin. Phytopathology 70:712-715. https://doi.org/10.1094/Phyto-70-712
  23. Huss, R. J. and Glaser, M. 1983. Identification and purification of an adenylate kinase-associated protein that influences the thermolability of adenylate kinase from a temperature-sensitive adk mutant of Escherichia coli. J. Biol. Chem. 258:13370- 13376.
  24. Janisiewicz, W. J. and Roitman, J. 1988. Biological control of blue mold and gray mold on apple and pear with Pseudomonas cepacia. Phytopathology 78:1697-1700. https://doi.org/10.1094/Phyto-78-1697
  25. Jayaswal, R. K., Fernandez, M., Upadhyay, R. S., Visintin, L., Kurz, M., Webb, J. and Rinehart, K. 1993. Antagonism of Pseudomonas cepacia against phytopathogenic fungi. Curr. Microbiol. 26:17-22. https://doi.org/10.1007/BF01577237
  26. Keel, C., Schnider, U., Maurhofer, M., Voisard, C., Laville, J., Burger, U., Wirthner, P., Haas, D. and Défago, G. 1992. Suppression of root diseases by Pseudomonas fluorescens CHA0: importance of the bacterial secondary metabolite 2,4-diacetylphloroglucinol. Mol. Plant-Microbe Interact. 5:4-13. https://doi.org/10.1094/MPMI-5-004
  27. Keen, N. T., Tamaki, S., Kobayashi, D. and Trollinger, D. 1988. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191-197. https://doi.org/10.1016/0378-1119(88)90117-5
  28. King, E. B. and Parke, J. L. 1993. Biocontrol of Aphanomyces root rot and Pythium damping-off by Pseudomonas cepacia AMMD on four pea cultivars. Plant Dis. 77:1185-1188. https://doi.org/10.1094/PD-77-1185
  29. Kraus, J. and Loper, J. E. 1995. Characterization of a genomic region required for production of the antibiotic pyoluteorin by the biological control agent Pseudomonas fluorescens Pf-5. Appl. Environ. Microbiol. 61:849-854.
  30. Lee, C. H., Kim, S., Hyun, B., Suh, J. W., Yon, C., Kim, C., Lim, Y. and Kim, C. 1994. Cepacidine A, a novel antifungal antibiotic produced by Pseudomonas cepacia. J. Antibiot. 47:1402- 1418. https://doi.org/10.7164/antibiotics.47.1402
  31. Lee, H., Vazquez-Laslop, N., Klyachko, K. A. and Neyfakh, A. A. 2003. Isolation of antibiotic hyper susceptibility mutants of Acinetobacter spp. by selection for DNA release. Antimicrob. Agents Chemother. 47:1267-1274. https://doi.org/10.1128/AAC.47.4.1267-1274.2003
  32. Lee, K. Y., Kong, H. G., Choi, K. H., Lee, S.-W. and Moon, B. J. 2011. Isolation and identification of Burkholderia pyrrocinia CH-67 to control tomato leaf mold and damping-off on crisphead lettuce and tomato. Plant Pathology J. 27:59-67. https://doi.org/10.5423/PPJ.2011.27.1.059
  33. Loper, J. E., Henkels, M. D., Shaffer, B. T., Valeriote, F. A. and Gross, H. 2008. Isolation and identification of rhizoxin analogs from Pseudomonas fluorescens Pf-5 by using a genomic mining strategy. Appl. Environ. Microbiol. 74:3085-3093. https://doi.org/10.1128/AEM.02848-07
  34. Lu, S.-E., Noval, J., Austin, F. W., Gu, G., Ellis, D., Kirk, M., Wilson- Stanford, S., Tonelli, M. and Smith, L. 2009. Occidiofungin, a unique antifungal glycopeptides produced by a strain of Burkholderia contaminans. Biochemistry 48:8312-8321. https://doi.org/10.1021/bi900814c
  35. Mahenthiralingam, E., Urban, T. A. and Goldberg, J. B. 2005. The multifarious, multireplicon Burkholderia cepacia complex. Nat. Rev. Microbiol. 3:144-156. https://doi.org/10.1038/nrmicro1085
  36. Mao, W., Lumsden, R. D., Lewis, J. A. and Hebbar, P. K. 1998. Seed treatment using pre-infiltration and biocontrol agents to reduce damping-off of corn caused by species of Pythium and Fusarium. Plant Dis. 82:294-299. https://doi.org/10.1094/PDIS.1998.82.3.294
  37. Mavrodi, D. V., Blankenfeldt, W. and Thomashow, L. S. 2006. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu. Rev. Phytopathol. 44:417-445. https://doi.org/10.1146/annurev.phyto.44.013106.145710
  38. McLoughlin, T. J., Quinn, J. P., Bettermann, A. and Bookland, R. 1992. Pseudomonas cepacia suppression of sunflower wilt fungus and role of antifungal compounds in controlling the disease. Appl. Environ. Microbiol. 58:1760-1763.
  39. Meyers, E., Bisacchi, G. S., Dean, L., Liu, W. C., Minassian, B., Slusarchyk, D. S., Sykes, R. B., Tanaka, S. K. and Trejo, W. 1987. Xylocandin: a new complex of antifungal peptides. I. Taxonomy, isolation and biological activity. J. Antibiot. 40: 1515-1519. https://doi.org/10.7164/antibiotics.40.1515
  40. Munier-Lehmann, H., Chenal-Francisque, V., Ionescu, M., Chrisova, P., Foulon, J., Carniel, E. and Bârzu, O. 2003. Relationship between bacterial virulence and nucleotide metabolism: a mutation in the adenylate kinase gene renders Yersinia pestis avirulent. Biochem. J. 373:515-522. https://doi.org/10.1042/BJ20030284
  41. Ongena, M. and Jacques, P. 2008. Bacillus lipopeptides: versatile weapons for plant disease control. Trends Microbiol. 16:115- 125. https://doi.org/10.1016/j.tim.2007.12.009
  42. Parke, J. L., Rand, R. E., Joy, A. E. and King, E. B. 1991. Biological control of Pythium-damping off and Aphanomyces root rot of peas by application of Pseudomonas cepacia or Pseudomonas fluorescens to seed. Plant Dis. 75:987-992. https://doi.org/10.1094/PD-75-0987
  43. Parker, J. L. and Gurian-Sherman, D. 2001. Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu. Rev. Phytopathol. 39:225-258. https://doi.org/10.1146/annurev.phyto.39.1.225
  44. Roberts, D. P., Lohrke, S. M., Meyer, S. L. F., Buyer, J. S., Bowers, J. H., Baker, C. J., Li, W., De Souza, J. T., Lewis, J. A. and Chung, S. 2005. Biocontrol agents applied individually and in combination for suppression of soilborn diseases of cucumber. Crop Prot. 24:141-155. https://doi.org/10.1016/j.cropro.2004.07.004
  45. Romero-Tabarez, M., Jansen, R., Sylla, M., Luensdorf, H., Huessler, S., Santosa, D. A., Timmis, K. N. and Molinari, G. 2006. 7-O-Malonyl macrolactin A, a new macrolactin antibiotic from Bacillus subtilis active against methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococci and a small-colony variant of Burkholderia cepacia. Antimicrob. Agents Chemother. 50:1701-1709. https://doi.org/10.1128/AAC.50.5.1701-1709.2006
  46. Rondon, M. R., Ballering, K. S. and Thomas, M. G. 2004. Identification and analysis of a siderophore biosynthetic gene cluster from Agrobacterium tumefaciens C58. Microbiology 150: 3857-3866. https://doi.org/10.1099/mic.0.27319-0
  47. Ruffin, D. C., Van Santen, V. L., Zhang, Y., Voelker, L. L., Panangala, V. S. and Dybvig, K. 2000. Transposon mutagenesis of Mycoplasma gallisepticum by conjugation with Enterococcus faecalis and determination of insertion site by direct genomic sequencing. Plasmid 44:191-195. https://doi.org/10.1006/plas.2000.1485
  48. Sambrook, J., Fritsch, E. F. and Maniatis, T. 1989. Molecular cloning; a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
  49. Santos, A. V., Dillon, R. J., Dillon, V. M., Reynolds, S. E. and Samuels, R. I. 2004. Ocurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol. Lett. 239:319- 323. https://doi.org/10.1016/j.femsle.2004.09.005
  50. Simon, R., Priefer, U. and Pühler, A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/Technology 1:784-795. https://doi.org/10.1038/nbt1183-784
  51. Sokol, P. A., Lewis, C. J. and Dennis, J. J. 1992. Isolation of a novel siderophore from Pseudomonas cepacia. J. Med. Microbiol. 36:184-189. https://doi.org/10.1099/00222615-36-3-184

Cited by

  1. Draft Genome Sequence of Burkholderia pyrrocinia Lyc2, a Biological Control Strain That Can Suppress Multiple Plant Microbial Pathogens vol.2, pp.5, 2014, https://doi.org/10.1128/genomeA.00991-14
  2. Molecular Docking Evaluation of (E)-5-arylidene-2-thioxothiazolidin-4-one Derivatives as Selective Bacterial Adenylate Kinase Inhibitors vol.23, pp.5, 2018, https://doi.org/10.3390/molecules23051076