DOI QR코드

DOI QR Code

An Effective and Practical Strategy for Biocontrol of Plant Diseases Using On-Site Mass Cultivation of Chitin-Degrading Bacteria

키틴분해세균의 현장 대량 배양방법을 이용한 효과적인 식물병의 생물적 방제 전략

  • Kim, Young-Cheol (Institute of Environmentally-Friendly Agriculture, Chonnam National University) ;
  • Kang, Beom Ryong (Institute of Environmentally-Friendly Agriculture, Chonnam National University) ;
  • Kim, Yong Hwan (Department of Crop Science and Biotechnology, Dankook University) ;
  • Park, Seur Kee (Department of Plant Medicine, Sunchon National University)
  • 김영철 (전남대학교 친환경농업연구소) ;
  • 강범용 (전남대학교 친환경농업연구소) ;
  • 김용환 (단국대학교 식량생명공학과) ;
  • 박서기 (순천대학교 식물의학과)
  • Received : 2017.02.08
  • Accepted : 2017.02.21
  • Published : 2017.03.31

Abstract

Recent worldwide demand for organic and sustainable agriculture products is driving the development of formulations of biopesticides effective in the field. Biopesticides have the benefit of environmentally-friendly qualities. However, biocontrol approaches largely have been ineffective in controlling plant pests in field conditions. Previously, we developed a cost-effective biocontrol formulation containing chitin and chitinase-producing biocontrol bacteria with field efficacy. This formulated product has successfully suppressed various plant diseases in the field conditions. In this review, we focus on ecological aspects and the potential mechanisms underpinning the success of chitinase-producing bacteria. In addition, we discuss the possibility on-site cultivation of the formulated products to further strengthen the approach as being farmer friendly and successful.

유기농 및 지속 가능한 농산물에 대한 최근의 전 세계적인 수요는 농가 현장에서 사용 가능한 생물 농약의 개발 및 활용에 대한 요구가 증대되고 있다. 그러나 대부분의 생물학적 방제 방법은 실제 현장 조건에서 식물병 방제 스펙트럼이 제한적이고 효능이 높지 않다. 본 연구팀은 키틴분해 미생물과 키틴을 활용하여 적은 비용으로 방제효과가 우수한 키틴 기반 제형을 개발했다. 이 제형은 포장 조건에서 다양한 식물병을 성공적으로 방제하였다. 본 리뷰에서는 성공적인 포장 연구와 관련하여 이 제형에 함유되어 있는 키틴분해미생물들의 생태학적 측면과 생물적 방제 기작에 대해 기술하였다. 또한 현장에서 키틴분해미생물의 현장 대량 배양과 효과적인 생물학적 방제 방법을 사용하여 농민 친화적인 수단으로 확대 할 수 있는 생물적 방제 방법과 전략의 가능성에 대해 논의했다.

Keywords

References

  1. Aballay, E., Ordenes, P., Martensson, A. and Persson, P. 2013. Effects of rhizobacteria on parasitism by Meloidogyne ethiopica on grapevines. Eur. J. Plant Pathol. 135: 137-145. https://doi.org/10.1007/s10658-012-0073-7
  2. Abiala, M. A., Odebode, A. C., Hsu, S. F. and Blackwood, C. B. 2015. Phytobeneficial properties of bacteria isolated from the rhizosphere of maize in southwestern Nigerian soils. Appl. Environ. Microbiol. 81: 4736-4743. https://doi.org/10.1128/AEM.00570-15
  3. Aggarwal, C., Paul, S., Tripathi, V., Paul, B. and Khan, M. A. 2015. Chitinase producing Serratia marcescens for biocontrol of Spodoptera litura (Fab) and studies on its chitinolytic activities. Ann. Agric. Res. 36: 132-137.
  4. Ahmed, A. S., Ezziyyani, M., Sanchez, C. P. and Candela, M. E. 2003. Effect of chitin on biological control activity of Bacillus spp. and Trichoderma harzianum against root rot disease in pepper (Capsicum annuum) plants. Eur. J. Plant Pathol. 109: 633-637. https://doi.org/10.1023/A:1024734216814
  5. Akocak, P. B., Churey, J. J. and Worobo, R. W. 2015. Antagonistic effect of chitinolytic Pseudomonas and Bacillus on growth of fungal hyphae and spores of aflatoxigenic Aspergillus flavus. Food Biosci. 10: 48-58. https://doi.org/10.1016/j.fbio.2015.01.005
  6. Akutsu, K., Hirata, A., Yamamoto, M., Hirayae, K., Okuyama, S. and Hibi, T. 1993. Growth inhibition of Botrytis spp. by Serratia marcescens B2 isolated from tomato phylloplane. Ann. Phytopathol. Soc. Jpn. 59: 18-25. https://doi.org/10.3186/jjphytopath.59.18
  7. Azizah, S. N., Mubarik, N. R. and Sudirman, L. I. 2015. Potential of chitinolytic Bacillus amyloliquefaciens SAHA 12.07 and Serratia marcescens KAHN 15.12 as biocontrol agents of Ganoderma boninense. Res. J. Microbiol. 10: 452-465. https://doi.org/10.3923/jm.2015.452.465
  8. Barber, M. S., Bertram, R. E. and Ride, J. P. 1989. Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol. Mol. Plant Pathol. 34: 3-12. https://doi.org/10.1016/0885-5765(89)90012-X
  9. Barreto, E. S., Torres, A. R., Barreto, M. R., Vasconcelos, A. T., Astolfi-Filho, S. and Hungria, M. 2008. Diversity in antifungal activity of strains of Chromobacterium violaceum from the Brazilian Amazon. J. Ind. Microbiol. Biotechnol. 35: 783-790. https://doi.org/10.1007/s10295-008-0331-z
  10. Belair, G. and Tremblay, N. 1995. The influence of chitin-urea amendments applied to an organic soil on a Meloidogyne hapla population and on the growth of greenhouse tomato. Phytoprotection 76: 75-80. https://doi.org/10.7202/706087ar
  11. Bell, A. A., Hubbard, J. C., Liu, L., Davis, R. M. and Subbarao, K. V. 1998. Effects of chitin and chitosan on the incidence and severity of Fusarium yellows of celery. Plant Dis. 82: 322-328. https://doi.org/10.1094/PDIS.1998.82.3.322
  12. Benhamou, N., Gagne, S., Le Quere, D. and Dehbi, L. 2000. Bacterial-mediated induced resistance in cucumber: beneficial effect of the endophytic bacterium Serratia plymuthica on the protection against infection by Pythium ultimum. Phytopathology 90: 45-56. https://doi.org/10.1094/PHYTO.2000.90.1.45
  13. Bottjer, K. P., Bone, L. W. and Gill, S. S. 1985. Nematoda: susceptibility of the egg to Bacillus thuringiensis toxins. Exp. Parasitol. 60: 239-244. https://doi.org/10.1016/0014-4894(85)90027-X
  14. Brazilian National Genome Project Consortium. 2003. The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability. Proc. Natl. Acad. Sci. U. S. A. 100: 11660-11665. https://doi.org/10.1073/pnas.1832124100
  15. Brzezinska, M. S., Jankiewicz, U., Burkowska, A. and Walczak, M. 2014. Chitinolytic microorganisms and their possible application in environmental protection. Curr. Microbiol. 68: 71-81. https://doi.org/10.1007/s00284-013-0440-4
  16. Chen, J., Moore, W. H., Yuen, G. Y., Kobayashi, D. and Caswell-Chen, E. P. 2006. Influence of Lysobacter enzymogenes strain C3 on nematodes. J. Nematol. 38: 233-239.
  17. Chernin, L. S., Winson, M. K., Thompson, J. M., Haran, S., Bycroft, B. W., Chet, I., Williams, P. and Stewart, G. S. 1998. Chitinolytic activity in Chromobacterium violaceum: substrate analysis and regulation by quorum sensing. J. Bacteriol. 180: 4435-4441.
  18. Chernov, T. I., Zhelezova, A. D., Manucharova, N. A. and Zvyagintsev, D. G. 2013. Monitoring of the chitinolytic microbial complex of the phylloplane. Biol. Bull. 40: 527-532. https://doi.org/10.1134/S1062359013060034
  19. Cretoiu, M. S., Korthals, G. W., Visser, J. H. M. and van Elsas, J. D. 2013. Chitin amendment increases soil suppressiveness toward plant pathogens and modulates the actinobacterial and oxalobacteraceal communities in an experimental agricultural field. Appl. Environ. Microbiol. 79: 5291-5301. https://doi.org/10.1128/AEM.01361-13
  20. Cronin, D., Moenne-Loccoz, Y., Dunne, C. and O'gara, F. 1997. In-hibition of egg hatch of the potato cyst nematode Globodera rostochiensis by chitinase-producing bacteria. Eur. J. Plant Pathol. 103: 433-440. https://doi.org/10.1023/A:1008662729757
  21. da Silva Melo, P., Maria, S. S., Vidal, B. C., Haun, M. and Duran, N. 2000. Violacein cytotoxicity and induction of apoptosis in V79 cells. In Vitro Cell Dev. Biol. Anim. 36: 539-543. https://doi.org/10.1290/1071-2690(2000)036<0539:VCAIOA>2.0.CO;2
  22. D'Addabbo, T. 1995. The nematicidal effect of organic amendments: a review of the literature, 1982-1994. Nematol. Medit. 23: 299-305.
  23. Dandurishvili, N., Toklikishvili, N., Ovadis, M., Eliashvili, P., Giorgobiani, N., Keshelava, R., Tediashvili, M., Vainstein, A., Khmel, I., Szegedi, E. and Chernin, L. 2011. Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants. J. Appl. Microbiol. 110: 341-352. https://doi.org/10.1111/j.1365-2672.2010.04891.x
  24. de Boer, M., Bom, P., Kindt, F., Keurentjes, J. J., van der Sluis, I., van Loon, L. C. and Bakker, P. A. 2003. Control of Fusarium wilt of radish by combining Pseudomonas putida strains that have different disease-suppressive mechanisms. Phytopathology 93: 626-632. https://doi.org/10.1094/PHYTO.2003.93.5.626
  25. de Bruijn, I., Cheng, X., de Jager, V., Exposito, R. G., Watrous, J., Patel, N., Postma, J., Dorrestein, P. C., Kobayashi, D. and Raaijmakers, J. M. 2015. Comparative genomics and metabolic profiling of the genus Lysobacter. BMC Genomics 16: 991. https://doi.org/10.1186/s12864-015-2191-z
  26. De Souza, A. O., Girello-Aily, D. C., Sato, D. N. and Duran, N. 1999. In vitro activity of violacein against Mycobacterium tuberculosis H37RA. Rev. Inst. Adolfo Lutz 58: 59-62.
  27. De Vleesschauwer, D. and Hofte, M. 2007. Using Serratia plymuthica to control fungal pathogens of plants. CAB Rev.: Perspect. Agric., Vet. Sci., Nutr. Nat. Resour. 2: 046.
  28. Divatar, M., Ahmed, S. and Lingappa, K. 2016. Isolation and screening of soil microbes for extracellular chitinase activity. J. Adv. Sci. Res. 7: 10-14.
  29. Domenech, J., Reddy, M. S., Kloepper, J. W., Ramos, B. and Gutierrez-Manero, J. 2006. Combined application of the biological product LS213 with Bacillus, Pseudomonas or Chryseobacterium for growth promotion and biological control of soil-borne diseases in pepper and tomato. BioControl 51: 245-258. https://doi.org/10.1007/s10526-005-2940-z
  30. Duran, N., Antonio, R. V., Haun, M. and Pilli, R. A. 1994. Biosynthesis of a trypanocide by Chromobacterium violaceum. World J. Microbiol. Biotechnol. 10: 686-690. https://doi.org/10.1007/BF00327960
  31. El-Tarabily, K. A., Sykes, M. L., Kurtboke, I. D., Hardy, G. E. S. J., Barbosa, A. M. and Dekker, R. F. H. 1996. Synergistic effects of a cellulase-producing Micromonospora carbonacea and an antibiotic-producing Streptomyces violascens on the suppression of Phytophthora cinnamomi root rot of Banksia grandis. Can. J. Bot. 74: 618-624. https://doi.org/10.1139/b96-078
  32. Folman, L. B., De Klein, M. J. E. M., Postma, J. and Van Veen, J. A. 2004. Production of antifungal compounds by Lysobacter enzymogenes isolate 3.1 T8 under different conditions in relation to its efficacy as a biocontrol agent of Pythium aphanidermatum in cucumber. Biol. Control 31: 145-154. https://doi.org/10.1016/j.biocontrol.2004.03.008
  33. Folman, L. B., Postma, J. and van Veen, J. A. 2003. Characterisation of Lysobacter enzymogenes (Christensen and Cook 1978) strain 3.1 T8, a powerful antagonist of fungal diseases of cucumber. Microbiol. Res. 158: 107-115. https://doi.org/10.1078/0944-5013-00185
  34. Frankowski, J., Lorito, M., Scala, F., Schmid, R., Berg, G. and Bahl, H. 2001. Purification and properties of two chitinolytic enzymes of Serratia plymuthica HRO-C48. Arch. Microbiol. 176: 421-426. https://doi.org/10.1007/s002030100347
  35. Ghasemi, S., Ahmadian, G., Jelodar, N. B., Rahimian, H., Ghandili, S., Dehestani, A. and Shariati, P. 2010. Antifungal chitinases from Bacillus pumilus SG2: preliminary report. World J. Microbiol. Biotechnol. 26: 1437-1443. https://doi.org/10.1007/s11274-010-0318-6
  36. Giesler, L. J. and Yuen, G. Y. 1998. Evaluation of Stenotrophomonas maltophilia strain C3 for biocontrol of brown patch disease. Crop Prot. 17: 509-513. https://doi.org/10.1016/S0261-2194(98)00049-0
  37. Giotis, C., Markelou, E., Theodoropoulou, A., Toufexi, E., Hodson, R., Shotton, P., Shiel, R., Cooper, J. and Leifert, C. 2009. Effect of soil amendments and biological control agents (BCAs) on soilborne root diseases caused by Pyrenochaeta lycopersici and Verticillium albo-atrum in organic greenhouse tomato production systems. Eur. J. Plant Pathol. 123: 387-400. https://doi.org/10.1007/s10658-008-9376-0
  38. Godoy, G., Rodriguez-Kabana, R., Shelby, R. A. and Morgan-Jones, G. 1983. Chitin amendments for control of Meloidogyne arenaria in infested soil. II. Effects on microbial population. Nematropica 13: 63-74.
  39. Ha, W. J., Kim, Y. C., Jung, H. and Park, S. K. 2014. Control of the root-knot nematode (Meloidogyne spp.) on cucumber by a liquid bio-formulation containing chitinolytic bacteria, chitin and their products. Res. Plant Dis. 20: 112-118. (In Korean) https://doi.org/10.5423/RPD.2014.20.2.112
  40. Halder, S. K., Maity, C., Jana, A., Das, A., Paul, T., Mohapatra, P. K. D., Pati, B. R. and Mondal, K. C. 2013. Proficient biodegradation of shrimp shell waste by Aeromonas hydrophila SBK1 for the concomitant production of antifungal chitinase and antioxidant chitosaccharides. Int. Biodeterior. Biodegrad. 79: 88-97. https://doi.org/10.1016/j.ibiod.2013.01.011
  41. Hallmann, J., Rodriguez-Kabana, R. and Kloepper, J. W. 1999. Chitin-mediated changes in bacterial communities of the soil, rhizosphere and within roots of cotton in relation to nematode control. Soil Biol. Biochem. 31: 551-560. https://doi.org/10.1016/S0038-0717(98)00146-1
  42. Hammami, I., Siala, R., Jridi, M., Ktari, N., Nasri, M. and Triki, M. A. 2013. Partial purification and characterization of chiIO8, a novel antifungal chitinase produced by Bacillus cereus IO8. J. Appl. Microbiol. 115: 358-366. https://doi.org/10.1111/jam.12242
  43. Han, T., Cho, M. Y., Lee, Y. S., Park, Y. S., Park, R. D., Nam, Y. and Kim, K. Y. 2010. Biocontrol of pepper diseases by Lysobacter enzymogenes LE429 and neem oil. Korean J. Soil Sci. Fert. 43: 490-497.
  44. Hayward, A. C., Fegan, N., Fegan, M. and Stirling, G. 2010. Stenotrophomonas and Lysobacter: ubiquitous plant-associated gamma-proteobacteria of developing significance in applied microbiology. J. Appl. Microbiol. 108: 756-770. https://doi.org/10.1111/j.1365-2672.2009.04471.x
  45. Hellberg, J. E., Matilla, M. A. and Salmond, G. P. 2015. The broadspectrum antibiotic, zeamine, kills the nematode worm Caenorhabditis elegans. Front. Microbiol. 6: 137.
  46. Hodgson, J. J., Arif, B. M. and Krell, P. J. 2013. Role of interactions between Autographa californica multiple nucleopolyhedrovirus procathepsin and chitinase chitin-binding or active-site domains in viral cathepsin processing. J. Virol. 87: 3471-3483. https://doi.org/10.1128/JVI.01937-12
  47. Hong, S. H., Anees, M. and Kim, K. Y. 2013. Biocontrol of Meloidogyne incognita inciting disease in tomato by using a mixed compost inoculated with Paenibacillus ehimensis RS820. Bio-control Sci. Technol. 23: 1024-1039. https://doi.org/10.1080/09583157.2013.811468
  48. Insunza, V., Alstrom, S. and Eriksson, K. B. 2002. Root bacteria from nematicidal plants and their biocontrol potential against trichodorid nematodes in potato. Plant Soil 241: 271-278. https://doi.org/10.1023/A:1016159902759
  49. Jabrane, A., Sabri, A., Compere, P., Jacques, P., Vandenberghe, I., Van Beeumen, J. and Thonart, P. 2002. Characterization of serracin P, a phage-tail-like bacteriocin, and its activity against Erwinia amylovora, the fire blight pathogen. Appl. Environ. Microbiol. 68: 5704-5710. https://doi.org/10.1128/AEM.68.11.5704-5710.2002
  50. Jankiewicz, U. and Brzezinska, M. S. 2015. Purification, characteristics and identification of chitinases synthesized by the bacterium Serratia plymuthica MP44 antagonistic against phytopathogenic fungi. Appl. Biochem. Microbiol. 51: 560-565. https://doi.org/10.1134/S0003683815050105
  51. Jeong, M. H., Yang, S. Y., Lee, Y. S., Ahn, Y. S., Park, Y. S., Han, H. R. and Kim, K. Y. 2015. Selection and characterization of Bacillus licheniformis MH48 for the biocontrol of pine wood nematode (Bursaphelenchus xylophilus). J. Korean For. Soc. 104: 512-518. (In Korean) https://doi.org/10.14578/jkfs.2015.104.3.512
  52. Jochum, C. C., Osborne, L. E. and Yuen, G. 2006. Fusarium head blight biological control with Lysobacter enzymogenes strain C3. Biol. Control 39: 336-344. https://doi.org/10.1016/j.biocontrol.2006.05.004
  53. Jung, W. J., Jung, S. J., An, K. N., Jin, Y. L., Park, R. D., Kim, K. Y., Shon, B. K. and Kim, T. H. 2002. Effect of chitinase-producing Paenibacillus illinoisensis KJA-424 on egg hatching of root-knot nematode (Meloidogyne incognita). J. Microbiol. Biotechnol. 12: 865-871.
  54. Kalbe, C., Marten, P. and Berg, G. 1996. Strains of the genus Serratia as beneficial rhizobacteria of oilseed rape with antifungal properties. Microbiol. Res. 151: 433-439. https://doi.org/10.1016/S0944-5013(96)80014-0
  55. Kamensky, M., Ovadis, M., Chet, I. and Chernin, L. 2003. Soil-borne strain IC14 of Serratia plymuthica with multiple mechanisms of antifungal activity provides biocontrol of Botrytis cinerea and Sclerotinia sclerotiorum diseases. Soil Biol. Biochem. 35: 323-331. https://doi.org/10.1016/S0038-0717(02)00283-3
  56. Khan, Z., Kim, S. G., Jeon, Y. H., Khan, H. U., Son, S. H. and Kim, Y. H. 2008. A plant growth promoting rhizobacterium, Paenibacillus polymyxa strain GBR-1, suppresses root-knot nematode. Bioresour. Technol. 99: 3016-3023. https://doi.org/10.1016/j.biortech.2007.06.031
  57. Kielak, A. M., Cretoiu, M. S., Semenov, A. V., Sorensen, S. J. and van Elsas, J. D. 2013. Bacterial chitinolytic communities respond to chitin and pH alteration in soil. Appl. Environ. Microbiol. 79: 263-272. https://doi.org/10.1128/AEM.02546-12
  58. Kilic-Ekici, O. and Yuen, G. Y. 2003. Induced resistance as a mechanism of biological control by Lysobacter enzymogenes strain C3. Phytopathology 93: 1103-1110. https://doi.org/10.1094/PHYTO.2003.93.9.1103
  59. Kilic-Ekici, O. and Yuen, G. Y. 2004. Comparison of strains of Lysobacter enzymogenes and PGPR for induction of resistance against Bipolaris sorokiniana in tall fescue. Biol. Control 30: 446-455. https://doi.org/10.1016/j.biocontrol.2004.01.014
  60. Kim, H. J., Choi, H. S., Yang, S. Y., Kim, I. S., Yamaguchi, T., Sohng, J. K., Park, S. K., Kim, J. C., Lee, C. H., Gardener, B. M. and Kim, Y. C. 2014. Both extracellular chitinase and a new cyclic lipopeptide, chromobactomycin, contribute to the biocontrol activity of Chromobacterium sp. C61. Mol. Plant Pathol. 15: 122-132. https://doi.org/10.1111/mpp.12070
  61. Kim, H. J., Park, J. Y., Han, S. H., Lee, J. H., Rong, X., Gardener, B. B. M., Park, S. K. and Kim, Y. C. 2011. Draft genome sequence of the biocontrol bacterium Chromobacterium sp. strain C-61. J. Bacteriol. 193: 6803-6804. https://doi.org/10.1128/JB.06191-11
  62. Kim, I. S., Yang, S. Y., Park, S. K. and Kim, Y. C. 2017. Quorum sensing is a key regulator for the antifungal and biocontrol activity of chitinase-producing Chromobacterium sp. C61. Mol. Plant Pathol. 18: 134-140. https://doi.org/10.1111/mpp.12379
  63. Kim, Y. C., Jung, H., Kim, K. Y. and Park, S. K. 2008. An effective biocontrol bioformulation against Phytophthora blight of pepper using growth mixtures of combined chitinolytic bacteria under different field conditions. Eur. J. Plant Pathol. 120: 373-382. https://doi.org/10.1007/s10658-007-9227-4
  64. Kim, Y. C., Lee, J. H., Bae, Y. S., Sohn, B. K. and Park, S. K. 2010. Development of effective environmentally-friendly approaches to control Alternaria blight and anthracnose diseases of Korean ginseng. Eur. J. Plant Pathol. 127: 443-450. https://doi.org/10.1007/s10658-010-9610-4
  65. Kishore, G. K. and Pande, S. 2007. Chitin-supplemented foliar application of chitinolytic Bacillus cereus reduces severity of Botrytis gray mold disease in chickpea under controlled conditions. Lett. Appl. Microbiol. 44: 98-105. https://doi.org/10.1111/j.1472-765X.2006.02022.x
  66. Kishore, G. K., Pande, S. and Podile, A. R. 2005a. Biological control of late leaf spot of peanut (Arachis hypogaea) with chitinolytic bacteria. Phytopathology 95: 1157-1165. https://doi.org/10.1094/PHYTO-95-1157
  67. Kishore, G. K., Pande, S. and Podile, A. R. 2005b. Chitin-supplemented foliar application of Serratia marcescens GPS 5 improves control of late leaf spot disease of groundnut by activating defence-related enzymes. J. Phytopathol. 153: 169-173. https://doi.org/10.1111/j.1439-0434.2005.00951.x
  68. Kobayashi, D. Y., Reedy, R. M., Palumbo, J. D., Zhou, J. M. and Yuen, G. Y. 2005. A clp gene homologue belonging to the Crp gene family globally regulates lytic enzyme production, antimicrobial activity, and biological control activity expressed by Lysobacter enzymogenes strain C3. Appl. Environ. Microbiol. 71: 261-269. https://doi.org/10.1128/AEM.71.1.261-269.2005
  69. Kobayashi, D. Y. and Yuen, G. Y. 2005. The role of clp-regulated factors in antagonism against Magnaporthe poae and biological control of summer patch disease of Kentucky bluegrass by Lysobacter enzymogenes C3. Can. J. Microbiol. 51: 719-723. https://doi.org/10.1139/w05-056
  70. Kurze, S., Bahl, H., Dahl, R. and Berg, G. 2001. Biological control of fungal strawberry diseases by Serratia plymuthica HRO-C48. Plant Dis. 85: 529-534. https://doi.org/10.1094/PDIS.2001.85.5.529
  71. Ladner, D. C., Tchounwou, P. B. and Lawrence, G. W. 2008. Evaluation of the effect of ecologic on root knot nematode, Meloidogyne incognita, and tomato plant, Lycopersicon esculenum. Int. J. Environ. Res. Pub. Health 5: 104-110. https://doi.org/10.3390/ijerph5020104
  72. Lee, Y. S. and Kim, K. Y. 2016. Antagonistic potential of Bacillus pumilus L1 against root-knot nematode, Meloidogyne arenaria. J. Phytopathol. 164: 29-39. https://doi.org/10.1111/jph.12421
  73. Lee, Y. S., Park, Y. S., Kim, S. B. and Kim, K. Y. 2013. Biological control of root-knot nematode by Lysobacter capsici YS1215. Korean J. Soil Sci. Fert. 46: 105-111. (In Korean) https://doi.org/10.7745/KJSSF.2013.46.2.105
  74. Leon, L. L., Miranda, C. C., De Souza, A. O. and Duran, N. 2001. Antileishmanial activity of the violacein extracted from Chromobacterium violaceum. J. Antimicrob. Chemother. 48: 449-450. https://doi.org/10.1093/jac/48.3.449
  75. Levenfors, J. J., Hedman, R., Thaning, C., Gerhardson, B. and Welch, C. J. 2004. Broad-spectrum antifungal metabolites produced by the soil bacterium Serratia plymuthica A 153. Soil Biol. Biochem. 36: 677-685. https://doi.org/10.1016/j.soilbio.2003.12.008
  76. Li, S., Jochum, C. C., Yu, F., Zaleta-Rivera, K., Du, L., Harris, S. D. and Yuen, G. Y. 2008. An antibiotic complex from Lysobacter enzymogenes strain C3: antimicrobial activity and role in plant disease control. Phytopathology 98: 695-701. https://doi.org/10.1094/PHYTO-98-6-0695
  77. Liopa-Tsakalidi, A., Chalikiopoulos, D., and Papasavvas, A. 2010. Effect of chitin on growth and chlorophyll content of two medicinal plants. J. Med. Plants Res. 4: 499-508.
  78. Liu, D., Cai, J., Xie, C. C., Liu, C. and Chen, Y. H. 2010. Purification and partial characterization of a 36-kDa chitinase from Bacillus thuringiensis subsp. colmeri, and its biocontrol potential. Enzyme Microb. Technol. 46: 252-256. https://doi.org/10.1016/j.enzmictec.2009.10.007
  79. Liu, M., Cai, Q. X., Liu, H. Z., Zhang, B. H., Yan, J. P. and Yuan, Z. M. 2002. Chitinolytic activities in Bacillus thuringiensis and their synergistic effects on larvicidal activity. J. Appl. Microbiol. 93: 374-379. https://doi.org/10.1046/j.1365-2672.2002.01693.x
  80. Manjula, K. and Podile, A. R. 2001. Chitin-supplemented formulations improve biocontrol and plant growth promoting efficiency of Bacillus subtilis AF 1. Can. J. Microbiol. 47: 618-625. https://doi.org/10.1139/w01-057
  81. Matilla, M. A., Drew, A., Udaondo, Z., Krell, T. and Salmond, G. P. 2016a. Genome sequence of Serratia plymuthica A153, a model rhizobacterium for the investigation of the synthesis and regulation of haterumalides, zeamine, and andrimid. Genome Announc. 4: e00373-16.
  82. Matilla, M. A., Nogellova, V., Morel, B., Krell, T. and Salmond, G. P. 2016b. Biosynthesis of the acetyl-CoA carboxylase-inhibiting antibiotic, andrimid, in Serratia is regulated by Hfq and the LysR-type transcriptional regulator, AdmX. Environ. Microbiol. 18: 3635-3650. https://doi.org/10.1111/1462-2920.13241
  83. Mian, I. H., Godoy, G., Shelby, R. A., Rodriguez-Kabana, R. and Morgan-Jones, G. 1982. Chitin amendments for control of Meloidogyne arenaria in infested soil. Nematropica 12: 71-84.
  84. Michaels, R. and Corpe, W. A. 1965. Cyanide formation by Chromobacterium violaceum. J. Bacteriol. 89: 106-112.
  85. Muller, H., Westendorf, C., Leitner, E., Chernin, L., Riedel, K., Schmidt, S., Eberl, L. and Berg, G. 2009. Quorum-sensing effects in the antagonistic rhizosphere bacterium Serratia plymuthica HRO-C48. FEMS Microbiol. Ecol. 67: 468-478. https://doi.org/10.1111/j.1574-6941.2008.00635.x
  86. Muymas, P., Pichyangkura, R., Wiriyakitnateekul, W., Wangsomboondee, T., Chadchawan, S. and Seraypheap, K. 2015. Effects of chitin-rich residues on growth and postharvest quality of lettuce. Biol. Agric. Hortic. 31: 108-117. https://doi.org/10.1080/01448765.2014.974669
  87. Nagpure, A., Choudhary, B. and Gupta, R. K. 2014. Chitinases: in agriculture and human healthcare. Crit. Rev. Biotechnol. 34: 215-232. https://doi.org/10.3109/07388551.2013.790874
  88. Narasimhan, A. and Shivakumar, S. 2012. Optimization of chitinase produced by a biocontrol strain of Bacillus subtilis using Plackett-Burman design. Eur. J. Exp. Biol. 2: 861-865.
  89. Nguyen, X. H., Naing, K. W., Lee, Y. S., Jung, W. J., Anees, M. and Kim, K. Y. 2013. Antagonistic potential of Paenibacillus elgii HOA73 against the root-knot nematode, Meloidogyne incognita. Nematology 15: 991-1000. https://doi.org/10.1163/15685411-00002737
  90. Niu, Q., Huang, X., Zhang, L., Li, Y., Li, J., Yang, J. and Zhang, K. 2006. A neutral protease from Bacillus nematocida, another potential virulence factor in the infection against nematodes. Arch. Microbiol. 185: 439-448. https://doi.org/10.1007/s00203-006-0112-x
  91. Otsu, Y., Matsuda, Y., Shimizu, H., Ueki, H., Mori, H., Fujiwara, K., Nakajima, T., Miwa, A., Nonomura, T., Sakuratani, Y., Tosa, Y., Mayama, S. and Toyoda, H. 2003. Biological control of phytophagous ladybird beetles Epilachna vigintioctopunctata (Col., Coccinellidae) by chitinolytic phylloplane bacteria Alcaligenes paradoxus entrapped in alginate beads. J. Appl. Entomol. 127: 441-446. https://doi.org/10.1046/j.1439-0418.2003.00773.x
  92. Pal, K. K. and Gardener, B. M. 2006. Biological control of plant pathogens. Plant Health Instr. 2: 1117-1142.
  93. Palumbo, J. D., Yuen, G. Y., Jochum, C. C., Tatum, K. and Kobayashi, D. Y. 2005. Mutagenesis of beta -1, 3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward Bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology 95: 701-707. https://doi.org/10.1094/PHYTO-95-0701
  94. Park, S. K. and Kim, K. C. 1991. Pathogenicities of pathogens and disease complex associated with wilt of hot pepper plants cropped in plastic house. Korean J. Plant Pathol. 7: 28-36.
  95. Park, S. K., Lee, H. Y. and Kim, K. C. 1995. Antagonistic effect of chitinolytic bacteria on soilborne plant pathogens. Korean J. Plant Pathol. 11: 47-52.
  96. Park, S. K., Lee, M. C. and Harman, G. E. 2005. The biocontrol activity of Chromobacterium sp. strain C-61 against Rhizoctonia solani depends on the productive ability of chitinase. Plant Pathol. J. 21: 275-282. https://doi.org/10.5423/PPJ.2005.21.3.275
  97. Parker, W. L., Rathnum, M. L., Johnson, J. H., Wells, J. S., Prinipe, P. A. and Sykes, R. B. 1988. Aerocyanidin, a new antibiotic produced by Chromobacterium violaceum. J. Antibiot. 41: 454-460. https://doi.org/10.7164/antibiotics.41.454
  98. Postma, J. and Schilder, M. T. 2015. Enhancement of soil suppressiveness against Rhizoctonia solani in sugar beet by organic amendments. Appl. Soil Ecol. 94: 72-79. https://doi.org/10.1016/j.apsoil.2015.05.002
  99. Qian, G. L., Hu, B. S., Jiang, Y. H. and Liu, F. Q. 2009. Identification and characterization of Lysobacter enzymogenes as a biological control agent against some fungal pathogens. Agric. Sci. Chin. 8: 68-75. https://doi.org/10.1016/S1671-2927(09)60010-9
  100. Radwan, M. A., Farrag, S. A. A., Abu-Elamayem, M. M. and Ahmed, N. S. 2012. Extraction, characterization, and nematicidal activity of chitin and chitosan derived from shrimp shell wastes. Biol. Fert. Soils 48: 463-468. https://doi.org/10.1007/s00374-011-0632-7
  101. Rajkumar, M., Lee, K. J. and Freitas, H. 2008. Effects of chitin and salicylic acid on biological control activity of Pseudomonas spp. against damping off of pepper. S. Afr. J. Bot. 74: 268-273. https://doi.org/10.1016/j.sajb.2007.11.014
  102. Ramamoorthy, V., Viswanathan, R., Raguchander, T., Prakasam, V. and Samiyappan, R. 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Prot. 20: 1-11. https://doi.org/10.1016/S0261-2194(00)00056-9
  103. Rathore, A. S. and Gupta, R. D. 2015. Chitinases from bacteria to human: properties, applications, and future perspectives. Enzyme Res. 2015: 791907.
  104. Regev, A., Keller, M., Strizhov, N., Sneh, B., Prudovsky, E., Chet, I., Ginzberg, I., Koncz-Kalman, Z., Koncz, C., Schell, J. and Zilberstein, A. 1996. Synergistic activity of a Bacillus thuringiensis delta-endotoxin and a bacterial endochitinase against Spodoptera littoralis larvae. Appl. Environ. Microbiol. 62: 3581-3586.
  105. Rettori, D. and Duran, N. 1998. Production, extraction and purificationof violacein: an antibiotic pigment produced by Chromobacterium violaceum. World J. Microbiol. Biotechnol. 14: 685-688. https://doi.org/10.1023/A:1008809504504
  106. Reyes-Ramirez, A., Escudero-Abarca, B. I., Aguilar-Uscanga, G., Hayward-Jones, P. M. and Barboza-Corona, J. E. 2004. Antifungal activity of Bacillus thuringiensis chitinase and its potential for the biocontrol of phytopathogenic fungi in soybean seeds. J. Food Sci. 69: M131-M134.
  107. Rodriguez-Kabana, R. 1986. Organic and inorganic nitrogen amendments to soil as nematode suppressants. J. Nematol. 18: 129-134.
  108. Rodriguez-Kabana, R., Morgan-Jones, G. and Gintis, B. O. 1984. Effects of chitin amendments to soil on Heterodera glycines, microbial populations, and colonization of cysts by fungi. Nematropica 14: 10-25.
  109. Sarathchandra, S. U., Watson, R. N., Cox, N. R., di Menna, M. E., Brown, J. A., Burch, G. and Neville, F. J. 1996. Effects of chitin amendment of soil on microorganisms, nematodes, and growth of white clover (Trifolium repens L.) and perennial ryegrass (Lolium perenne L.). Biol. Fert. Soils 22: 221-226. https://doi.org/10.1007/BF00382516
  110. Sato, I., Yoshida, S., Iwamoto, Y., Aino, M., Hyakumachi, M., Shimizu, M., Takahashi, H., Ando, S. and Tsushima, S. 2014. Suppressive potential of Paenibacillus strains isolated from the tomato phyllosphere against Fusarium crown and root rot of tomato. Microbes Environ. 29: 168-177. https://doi.org/10.1264/jsme2.ME13172
  111. Seo, C. C., Jung, H. C. and Park, S. K. 2007. Control of powdery mildew of pepper using culture solutions of chitinolytic bacteria, Chromobacterium sp. and Lysobacter enzymogenes. Res. Plant Dis. 13: 40-44. (In Korean) https://doi.org/10.5423/RPD.2007.13.1.040
  112. Shanmugam, V., Thakur, H. and Gupta, S. 2013. Use of chitinolytic Bacillus atrophaeus strain S2BC-2 antagonistic to Fusarium spp. for control of rhizome rot of ginger. Ann. Microbiol. 63: 989-996. https://doi.org/10.1007/s13213-012-0552-2
  113. Sharp, R. G. 2013. A review of the applications of chitin and its derivatives in agriculture to modify plant-microbial interactions and improve crop yields. Agronomy 3: 757-793. https://doi.org/10.3390/agronomy3040757
  114. Shibuya, N. and Minami, E. 2001. Oligosaccharide signalling for defence responses in plant. Physiol. Mol. Plant Pathol. 59: 223-233. https://doi.org/10.1006/pmpp.2001.0364
  115. Singh, A. K., Singh, A. and Joshi, P. 2016. Combined application of chitinolytic bacterium Paenibacillus sp. D1 with low doses of chemical pesticides for better control of Helicoverpa armigera. Int. J. Pest Manag. 62: 222-227. https://doi.org/10.1080/09670874.2016.1167267
  116. Singh, G., Bhalla, A., Bhatti, J. S., Chandel, S., Rajput, A., Abdullah, A., Andrabi, W. and Kaur, P. 2014. Potential of chitinases as a biopesticide against agriculturally harmful fungi and insects. Res. Rev.: J. Microbiol. Biotechnol. 3: 27-32.
  117. Singh, P. D., Liu, W. C., Gougoutas, J. Z., Malley, M. F., Porubcan, M. A., Trejo, W. H., Wells, J. S. and Sykes, R. B. 1988. Aerocavin, a new antibiotic produced by Chromobacterium violaceum. J. Antibiot. 41: 446-453. https://doi.org/10.7164/antibiotics.41.446
  118. Singh, P. P., Shin, Y. C., Park, C. S. and Chung, Y. R. 1999. Biological control of fusarium wilt of cucumber by chitinolytic bacteria. Phytopathology 89: 92-99. https://doi.org/10.1094/PHYTO.1999.89.1.92
  119. Slimene, I. B., Tabbene, O., Gharbi, D., Mnasri, B., Schmitter, J. M., Urdaci, M. C. and Limam, F. 2015. Isolation of a chitinolytic Bacillus licheniformis S213 strain exerting a biological control against Phoma medicaginis infection. Appl. Biochem. Biotechnol. 175: 3494-3506. https://doi.org/10.1007/s12010-015-1520-7
  120. Sneh, B., Schuster, S. and Gross, S. 1983. Improvement of the insecticidal activity of Bacillus thuringiensis var. entomocidus on larvae of Spodoptera littoralis (Lepidoptera, Noctuidae) by addition of chitinolytic bacteria, a phagostimulant and a UVprotectant. J. Appl. Entomol. 96: 77-83.
  121. Someya, N., Ikeda, S., Morohoshi, T., Tsujimoto, N. M., Yoshida, T., Sawada, H., Ikeda, T. and Tsuchiya, K. 2011. Diversity of culturable chitinolytic bacteria from rhizospheres of agronomic plants in Japan. Microbes Environ. 26: 7-14. https://doi.org/10.1264/jsme2.ME10149
  122. Someya, N., Kataoka, N., Komagata, T., Hirayae, K., Hibi, T. and Akutsu, K. 2000. Biological control of cyclamen soilborne diseases by Serratia marcescens strain B2. Plant Dis. 84: 334-340. https://doi.org/10.1094/PDIS.2000.84.3.334
  123. Someya, N., Nakajima, M., Hirayae, K., Hibi, T. and Akutsu, K. 2001. Synergistic antifungal activity of chitinolytic enzymes and prodigiosin produced by biocontrol bacterium, Serratia marcescens strain B2 against gray mold pathogen, Botrytis cinerea. J. Gen. Plant Pathol. 67: 312-317. https://doi.org/10.1007/PL00013038
  124. Someya, N., Nakajima, M., Watanabe, K., Hibi, T. and Akutsu, K. 2005. Potential of Serratia marcescens strain B2 for biological control of rice sheath blight. Biocontrol Sci. Technol. 15: 105-109. https://doi.org/10.1080/09583150400016092
  125. Spiegel, Y., Chet, I. and Cohn, E. 1987. Use of chitin for controlling plant plant-parasitic nematodes. II. Mode of action. Plant Soil 98: 337-345. https://doi.org/10.1007/BF02378355
  126. Spiegel, Y., Cohn, E., Galper, S., Sharon, E. and Chet, I. 1991. Evaluation of a newly isolated bacterium, Pseudomonas chitinolytica sp. nov., for controlling the root-knot nematode Meloidogynejavanica. Biocontrol Sci. Technol. 1: 115-125. https://doi.org/10.1080/09583159109355191
  127. Subbanna, A. R. N. S., Khan, M. S. and Shivashankara, H. 2016. Characterization of antifungal Paenibacillus illinoisensis strain UKCH21 and its chitinolytic properties. Afr. J. Microbiol. Res. 10: 1380-1387. https://doi.org/10.5897/AJMR2016.8248
  128. Sullivan, R. F., Holtman, M. A., Zylstra, G. J., White, J. F. and Kobayashi, D. Y. 2003. Taxonomic positioning of two biological control agents for plant diseases as Lysobacter enzymogenes based on phylogenetic analysis of 16S rDNA, fatty acid composition and phenotypic characteristics. J. Appl. Microbiol. 94: 1079-1086. https://doi.org/10.1046/j.1365-2672.2003.01932.x
  129. Tian, B., Yang, J., Lian, L., Wang, C., Li, N. and Zhang, K. Q. 2007a. Role of an extracellular neutral protease in infection against nematodes by Brevibacillus laterosporus strain G4. Appl. Microbiol. Biotechnol. 74: 372-380. https://doi.org/10.1007/s00253-006-0690-1
  130. Tian, B., Yang, J. and Zhang, K. Q. 2007b. Bacteria used in the biological control of plant-parasitic nematodes: populations, mechanisms of action, and future prospects. FEMS Microbiol. Ecol. 61: 197-213. https://doi.org/10.1111/j.1574-6941.2007.00349.x
  131. Ueda, H., Nakajima, H., Hori, Y., Goto, T. and Okuhara, M. 1994. Action of FR901228, a novel antitumor bicyclic depsipeptide produced by Chromobacterium violaceum no. 968, on Ha-ras transformed NIH3T3 cells. Biosci. Biotechnol. Biochem. 58: 1579-1583. https://doi.org/10.1271/bbb.58.1579
  132. Vaidya, R. J., Shah, I. M., Vyas, P. R. and Chhatpar, H. S. 2001. Production of chitinase and its optimization from a novel isolate Alcaligenes xylosoxydans: potential in antifungal biocontrol. World J. Microbiol. Biotechnol. 17: 691-696. https://doi.org/10.1023/A:1012927116756
  133. Wang, K., Yan, P. S., Cao, L. X., Ding, Q. L., Shao, C. and Zhao, T. F. 2013. Potential of chitinolytic Serratia marcescens strain JPP1 for biological control of Aspergillus parasiticus and aflatoxin. BioMed Res. Int. 2013: 397142.
  134. Westerdahl, B. B., Carlson, H. L., Grant, J., Radewald, J. D., Welch, N., Anderson, C. A., Darso, J., Kirby, D. and Shibuya, F. 1992. Management of plant-parasitic nematodes with a chitin-urea soil amendment and other materials. J. Nematol. 24: 669-680.
  135. Wiwat, C., Thaithanun, S., Pantuwatana, S. and Bhumiratana, A. 2000. Toxicity of chitinase-producing Bacillus thuringiensis ssp. kurstaki HD-1 (G) toward Plutella xylostella. J. Invertebr. Pathol. 76: 270-277. https://doi.org/10.1006/jipa.2000.4976
  136. Xu, S. J., Hong, S. J., Choi, W. and Kim, B. S. 2014. Antifungal activity of Paenibacillus kribbensis strain T-9 isolated from soils against several plant pathogenic fungi. Plant Pathol. J. 30: 102-108. https://doi.org/10.5423/PPJ.OA.05.2013.0052
  137. Yu, F., Zaleta-Rivera, K., Zhu, X., Huffman, J., Millet, J. C., Harris, S. D., Yuen, G., Li, X. C. and Du, L. 2007. Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action. Antimcrob. Agents Chemother. 51: 64-72. https://doi.org/10.1128/AAC.00931-06
  138. Yuen, G., Broderick, K., Moore, W. and Caswell-Chen, E. 2006. Effects of Lysobacter enzymogenes C 3 and its antibiotic dihydromaltophilin on nematodes. Phytopathology 96: S128.
  139. Yuen, G. Y., Jochum, C. C., Osborne, L. E. and Jin, Y. 2003. Biocontrol of Fusarium head blight in wheat by Lysobacter enzymogenes C3. Phytopathology 93: S93.
  140. Yuen, G. Y., Steadman, J. R., Lindgren, D. T., Schaff, D. and Jochum, C. 2001. Bean rust biological control using bacterial agents. Crop Prot. 20: 395-402. https://doi.org/10.1016/S0261-2194(00)00154-X
  141. Zhang, W., Li, Y., Qian, G., Wang, Y., Chen, H., Li, Y. Z., Liu, F., Shen, Y. and Du, L. 2011. Identification and characterization of the anti-methicillin-resistant Staphylococcus aureus WAP-8294A2 biosynthetic gene cluster from Lysobacter enzymogenes OH11. Antimcrob. Agents Chemother. 55: 5581-5589. https://doi.org/10.1128/AAC.05370-11
  142. Zhang, Z. and Yuen, G. Y. 1999. Biological control of Bipolaris sorokiniana on tall fescue by Stenotrophomonas maltophilia strain C3. Phytopathology 89: 817-822. https://doi.org/10.1094/PHYTO.1999.89.9.817
  143. Zhang, Z., Yuen, G. Y., Sarath, G. and Penheiter, A. R. 2001. Chitinases from the plant disease biocontrol agent, Stenotrphomonas maltophiliao C3. Phytopathology 91: 204-211. https://doi.org/10.1094/PHYTO.2001.91.2.204

Cited by

  1. Organic Rice (Oryza sativa L.) Production in Eco-friendly Complex using Gelatin·Chitin Microorganisms vol.26, pp.4, 2018, https://doi.org/10.11625/KJOA.2018.26.4.629