[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.5423/PPJ.OA.06.2017.0115

Hydrogen Cyanide Produced by Pseudomonas chlororaphis O6 Exhibits Nematicidal Activity against Meloidogyne hapla

Kang, Beom Ryong (Institute of Environmentally-Friendly Agriculture, Chonnam National University)
Anderson, Anne J. (Department of Biology, Utah State University)
Kim, Young Cheol (Institute of Environmentally-Friendly Agriculture, Chonnam National University)

Publication Information

The Plant Pathology Journal / v.34, no.1, 2018 , pp. 35-43 More about this Journal

Abstract

Root-knot nematodes (Meloidogyne spp.) are parasites that attack many field crops and orchard trees, and affect both the quantity and quality of the products. A root-colonizing bacterium, Pseudomonas chlororaphis O6, possesses beneficial traits including strong nematicidal activity. To determine the molecular mechanisms involved in the nematicidal activity of P. chlororaphis O6, we constructed two mutants; one lacking hydrogen cyanide production, and a second lacking an insecticidal toxin, FitD. Root drenching with wild-type P. chlororaphis O6 cells caused juvenile mortality in vitro and in planta. Efficacy was not altered in the fitD mutant compared to the wild-type but was reduced in both bioassays for the mutant lacking hydrogen cyanide production. The reduced number of galls on tomato plants caused by the wild-type strain was comparable to that of a standard chemical nematicide. These findings suggest that hydrogen cyanide-producing root colonizers, such as P. chlororaphis O6, could be formulated as "green" nematicides that are compatible with many crops and offer agricultural sustainability.

Keywords

biological control; FitD insecticidal protein; hydrogen cyanide; nematicide; root-knot nematode;

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Times Cited By KSCI : 2 (Citation Analysis)

Reference
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1	Flury, P., Aellen, N., Ruffner, B., Pechy-Tarr, M., Fataar, S., Metla, Z., Dominguez-Ferreras, A., Bloemberg, G., Frey, J., Goesmann, A., Raaijmakers, J. M., Duffy, B., Hofte, M., Blom, J., Smits, T. H., Keel, C. and Maurhofer, M. 2016. Insect pathogenicity in plant-beneficial pseudomonads: phylogenetic distribution and comparative genomics. ISME J. 10: 2527-2542. DOI
2	Guibault, G. G. and Kramer, D. N. 1966. Ultra sensitive, specific method for cyanide using p-nitrobenzaldehyde and o-dinitrobenzene. Anal. Chem. 38:834-836. DOI
3	Han, S. H., Lee, S. J., Moon, J. H., Park, K. H., Yang, K. Y., Cho, B. H., Kim, K. Y., Kim, Y. W., Lee, M. C., Anderson, A. J. and Kim, Y. C. 2006. GacS-dependent production of 2R, 3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Mol. Plant-Microbe Interact. 19:924-930. DOI
4	Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J. and Schweizer, H. P. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86. DOI
5	Jang, J. Y., Choi, Y. H., Shin, T. S., Kim, T. H., Shin, K.-S., Park, H. W., Kim, Y. H., Kim, H., Choi, G. J. and Jang, K. S. 2016. Biological control of Meloidogyne incognita by Aspergillus niger F22 producing oxalic acid. PLoS One 11:e0156230. DOI
6	Kamilova, F., Kravchenko, L. V., Shaposhnikov, A. I., Azarova, T., Makarova, N. and Lugtenberg, B. 2006. Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol. Plant-Microbe Interact. 19:250-256. DOI
7	Lesuffleur, F., Paynel, F., Bataille, M.-P., Le Deunff, E. and Cliquet, J.-B. 2007. Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant Soil 294:235-246. DOI
8	Loper, J. E., Hassan, K. A., Mavrodi, D. V., Davis, E. W., Lim, C. K., Shaffer, B. T., Elbourne, L. D. H., Stockwell, V. O., Hartney, S. L., Breakwell, K., Henkels, M. D., Tetu, S. G., Rangel, L. I., Kidarsa, T. A., Wilson, N. L., de Mortel, J. E. V., Song, C. X., Blumhagen, R., Radune, D., Hostetler, J. B., Brinkac, L. M., Durkin, A. S., Kluepfel, D. A., Wechter, W. P., Anderson, A. J., Kim, Y. C., Pierson, L. S., Pierson, E. A., Lindow, S. E., Kobayashi, D. Y., Raaijmakers, J. M., Weller, D. M., Thomashow, L. S., Allen, A. E. and Paulsen, I. T. 2012. Comparative genomics of plant-associated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. 8:e1002784. DOI
9	McCarter, J. 2009. Molecular approaches toward resistance to plant-parasitic nematodes. In: Cell biology of plant nematode parasitism, pp. 239-267. Springer.
10	Meyer, S. L. F., Halbrendt, J. M., Carta, L. K., Skantar, A. M., Liu, T., Abdelnabby, H. M. E. and Vinyard, B. T. 2009. Toxicity of 2,4-diacetylphloroglucinol (DAPG) to plant-parasitic and bacterial-feeding nematodes. J. Nematol. 41:274-280.
11	Miller, C. D., Kim, Y. C. and Anderson, A. J. 1997. Cloning and mutational analysis of the gene for the stationary-phase inducible catalase (catC) from Pseudomonas putida. J. Bacteriol. 179:5241-5245. DOI
12	Nandi, M., Selin, C., Brassinga, A. K. C., Belmonte, M. F., Fernando, W. D., Loewen, P. C. and De Kievit, T. R. 2015. Pyrrolnitrin and hydrogen cyanide production by Pseudomonas chlororaphis strain PA23 exhibits nematicidal and repellent activity against Caenorhabditis elegans. PLoS One 10:e0123184. DOI
13	Anderson, A. J., Kang, B. R. and Kim, Y. C. 2017. The Gac/Rsm signaling pathway of a biocontrol bacterium, Pseudomonas chlororaphis O6. Res. Plant Dis. 23:212-227. DOI
14	Kang, B. R., Han, S.-H., Zdor, R. E., Anderson, A. J., Spencer, M., Yang, K. Y., Kim, Y. H., Lee, M. C., Cho, B. H. and Kim, Y. C. 2007. Inhibition of seed germination and induction of systemic disease resistance by Pseudomonas chlororaphis O6 requires phenazine production regulated by the global regulator, gacS. J. Microbiol. Biotech. 17:586-593.
15	Kerry, B. R. 2000. Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu. Rev. Phytopathol. 38:423-441. DOI
16	Kim, D.-G. and Lee, J.-H. 2008. Economic threshold of Meloidogyne incognita for greenhouse grown cucumber in Korea. Res. Plant Dis. 14:117-121. DOI
17	Abawi, G. S. and Widmer, T. L. 2000. Impact of soil health management practices on soilborne pathogens, nematodes and root diseases of vegetable crops. Appl. Soil Ecol. 15:37-47. DOI
18	Akhtar, M. and Malik, A. 2000. Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresour. Technol. 74:35-47. DOI
19	Anderson, A. J. and Kim, Y. C. 2018. Biopesticides produced by plant-probiotic Pseudomonas chlororaphis isolates. Crop Prot. 105:62-69. DOI
20	Kim, D. G. 2001. Occurrence of root-knot nematodes on fruit vegetables under greenhouse conditions in Korea. Res. Plant Dis. 7:69-79.
21	Kim, D. G., Choi, D. R. and Lee, S. B. 2001. Effects of control methods on yields of oriental melon in fields infested with Meloidogyne arenaria. Res. Plant Dis. 7:42-48.
22	Kim, M. S., Cho, S. M., Kang, E. Y., Im, Y. J., Hwangbo, H., Kim, Y. C., Ryu, C. M., Yang, K. Y., Chung, G. C. and Cho, B. H. 2008. Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root colonization. Mol. Plant-Microbe Interact. 21:1643-1653. DOI
23	King, E. O., Ward, M. and Raney, D. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab. Clin. Med. 44:301-307.
24	Lapouge, K., Schubert, M., Allain, F. H. and Haas, D. 2008. Gac/Rsm signal transduction pathway of ${\gamma}$ -proteobacteria: from RNA recognition to regulation of social behavior. Mol. Microbiol. 67:241-253.
25	Lee, J. H., Ma, K. C., Ko, S. J., Kang, B. R., Kim, I. S. and Kim, Y. C. 2011. Nematicidal activity of a nonpathogenic biocontrol bacterium, Pseudomonas chlororaphis O6. Curr. Microbiol. 62:746-751. DOI
26	Pessi, G. and Haas, D. 2000. Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J. Bacteriol. 182:6940-6949. DOI
27	Park, J. Y., Kang, B. R., Ryu, C.-M., Anderson, A. J. and Kim, Y. C. 2018. Polyamine is a critical determinant of Pseudomonas chlororaphis O6 for GacS-depedent bacterial cell growth and biocontrol activity. Mol. Plant Pathol. doi: 10.1111/mpp.12610 (in press). DOI
28	Park, J. Y., Oh, S. A., Anderson, A. J., Neiswender, J., Kim, J. C. and Kim, Y. C. 2011. Production of the antifungal compounds phenazine and pyrrolnitrin from Pseudomonas chlororaphis O6 is differentially regulated by glucose. Lett. Appl. Microbiol. 52:532-537. DOI
29	Pechy-Tarr, M., Bruck, D. J., Maurhofer, M., Fischer, E., Vogne, C., Henkels, M. D., Donahue, K. M., Grunder, J., Loper, J. E. and Keel, C. 2008. Molecular analysis of a novel gene cluster encoding an insect toxin in plant-associated strains of Pseudomonas fluorescens. Environ. Microbiol. 10:2368-2386. DOI
30	Rangel, L. I., Henkels, M. D., Shaffer, B. T., Walker, F. L., Davis II, E. W., Stockwell, V. O., Bruck, D., Taylor, B. J. and Loper, J. E. 2016. Characterization of toxin complex gene clusters and insect toxicity of bacteria representing four subgroups of Pseudomonas fluorescens. PLoS One 11:e0161120. DOI
31	Fischer, H., Meyer, A., Fischer, K. and Kuzyakov, Y. 2007. Carbohydrate and amino acid composition of dissolved organic matter leached from soil. Soil Biol. Biochem. 39:2926-2935. DOI
32	Cho, M. R., Lee, B. C., Kim, D. S., Jeon, H. Y., Yiem, M. S. and Lee, J. O. 2000. Distribution of plant-parasitic nematodes in fruit vegetable production areas in Korea and identification of root-knot nematodes by enzyme phenotypes. Korean J. Appl. Entomol. 39:123-129.
33	Cho, S. M., Kang, B. R., Han, S. H., Anderson, A. J., Park, J. Y., Lee, Y. H., Cho, B. H., Yang, K. Y., Ryu, C. M. and Kim, Y. C. 2008. 2R,3R-butanediol, a bacterial volatile produced by Pseudomonas chlororaphis O6, is involved in induction of systemic tolerance to drought in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 21:1067-1075. DOI
34	Choi, Y. E. and Choo, H. Y. 1978. A study on the root-knot nematodes (Meloidogyne spp.) affecting economic crops in Korea. Korean J. Appl. Entomol. 17:89-98.
35	Spencer, M., Ryu, C. M., Yang, K. Y., Kim, Y. C., Kloepper, J. W. and Anderson, A. J. 2003. Induced defence in tobacco by Pseudomonas chlororaphis strain O6 involves at least the ethylene pathway. Physiol. Mol. Plant Pathol. 63:27-34. DOI
36	Rich, J. R., Brito, J. A., Kaur, R. and Ferrell, J. A. 2009. Weed species as hosts of Meloidogyne: a review. Nematropica 39:157-185.
37	Rijavec, T. and Lapanje, A. 2016. Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front. Microbiol. 7:1785.
38	Rodriguez-Kabana, R., Morgan-Jones, G. and Chet, I. 1987. Biological control of nematodes: Soil amendments and microbial antagonists. Plant Soil 100:237-247. DOI
39	Sambrook, J. 2001. Sambrook, J., Fritsch, E. F. and Maniatis, T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, NY, USA.
40	Siddiqui, I. A. and Shaukat, S. S. 2003. Suppression of root-knot disease by Pseudomonas fluorescens CHA0 in tomato: importance of bacterial secondary metabolite, 2,4-diacetylpholoroglucinol. Soil Biol. Biochem. 35:1615-1623. DOI
41	Wright, M., Adams, J., Yang, K., McManus, P., Jacobson, A., Gade, A., McLean, J., Britt, D. and Anderson, A. 2016. A root-colonizing pseudomonad lessens stress responses in wheat imposed by CuO nanoparticles. PLoS One 11:e0164635. DOI
42	Tripathi, R. K. and Gottlieb, D. 1969. Mechanism of action of the antifungal antibiotic pyrrolnitrin. J. Bacteriol. 100:310-318.
43	Wissing, F. 1974. Cyanide formation from oxidation of glycine of Pseudomonas species. J. Bacteriol. 117:1289-1294.
44	Wong, D. T. and Airall, J. M. 1970. The mode of action of antifungal agents: effect of pyrrolnitrin on mitochondrial electron transport. J. Antibiot. 23:55-62. DOI
45	Zdor, R. E. 2015. Bacterial cyanogenesis: impact on biotic interactions. J. Appl. Microbiol. 118:267-274. DOI