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http://dx.doi.org/10.5423/PPJ.OA.03.2019.0060

Biocontrol of Citrus Canker Disease Caused by Xanthomonas citri subsp. citri Using an Endophytic Bacillus thuringiensis  

Islam, Md. Nurul (Department of Biotechnology, Yeungnam University)
Ali, Md. Sarafat (Department of Biotechnology, Yeungnam University)
Choi, Seong-Jin (Department of Biotechnology, Catholic University of Daegu)
Hyun, Jae-Wook (Citrus Research Station, National Institute of Horticultural and Herbal Science, Rural Development Administration)
Baek, Kwang-Hyun (Department of Biotechnology, Yeungnam University)
Publication Information
The Plant Pathology Journal / v.35, no.5, 2019 , pp. 486-497 More about this Journal
Abstract
Citrus canker is a devastating disease of citrus caused by Xanthomonas citri subsp. citri (Xcc). A total of 134 endophytic bacteria were isolated from various gymnospermic and angiospermic plants. They were screened for their antagonistic activities against three wild-type and six streptomycin-resistant Xcc strains. TbL-22 and TbL-26, both later identified as Bacillus thuringiensis, inhibited all the wild and resistant Xcc strains. TbL-22 exerted the highest antagonistic activity against XccW3 and XccM6 with inhibition zones of $20.64{\pm}0.69$ and $19.91{\pm}0.87mm$, respectively. Similarly ethyl acetate extract of TbL-22 showed highest inhibition zones $15.31{\pm}2.08$ and $19.37{\pm}3.17mm$ against XccW3 and XccM6, respectively. TbL-22 reduced canker incidence on infected leaves by 64.05% relative to positive controls. Scanning electron microscopy revealed that the cell membranes of Xcc treated with ethyl acetate extract of TbL-22 were ruptured, lysed, and swollen. B. thuringiensis TbL-22 can effectively and sustainably controls streptomycin-resistant citrus canker.
Keywords
Bacillus thuringiensis; biocontrol; citrus canker; endophytic bacteria;
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1 Backman, P. A. and Sikora, R. A. 2008. Endophytes: an emerging tool for biological control. Biol. Control 46:1-3.   DOI
2 Bais, H. P., Fall, R. and Vivanco, J. M. 2004. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol. 134:307-319.   DOI
3 Bajpai, V. K., Al-Reza, S. M., Choi, U. K., Lee, J. H. and Kang, S. C. 2009. Chemical composition, antibacterial and antioxidant activities of leaf essential oil and extracts of Metasequoia glyptostroboides Miki ex Hu. Food Chem. Toxicol. 47:1876-1883.   DOI
4 Behlau, F., Canteros, B. I., Minsavage, G. V., Jones, J. B. and Graham, J. H. 2011. Molecular characterization of copper resistance genes from Xanthomonas citri subsp. citri and Xanthomonas alfalfae subsp. citrumelonis. Appl. Environ. Microbiol. 77:4089-4096.   DOI
5 Berg, G., Eberl, L. and Hartmann, A. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7:1673-1685.   DOI
6 Brown, A. E. and Soepena, H. 1994. Pathogenicity of Colletotrichum acutatum and C. gloeosporioides on Hevea spp. Mycol. Res. 98:264-266.   DOI
7 Carter, A. P., Clemons, W. M., Brodersen, D. E., Morgan-Warren, R. J., Wimberly, B. T. and Ramakrishnan, V. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interaction with antibiotics. Nature 407:340-348.   DOI
8 Chattopadhyay, A., Bhatnagar, N. B. and Bhatnagar, R. 2004. Bacterial insecticidal toxins. Crit. Rev. Microbiol. 30:33-54.   DOI
9 Silo-Suh, L. A., Lethbridge, B. J., Raffel, S. J., He, H., Clardy, J. and Handelsman, J. 1994. Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl. Environ. Microbiol. 60:2023-2030.   DOI
10 Shang, H., Chen, J., Handelsman, J. and Goodman, R. M. 1999. Behavior of Pythium torulosum zoospores during their interaction with tobacco roots and Bacillus cereus. Curr. Microbiol. 38:199-204.   DOI
11 Sturz, A. V. and Nowak, J. 2000. Endophytic communities of rhizobacteria and the strategies required creating yield enhancing associations with crops. Appl. Soil Ecol. 15:183-190.   DOI
12 Sultana, R. and Kim, K. 2016. Bacillus thuringiensis C25 suppresses popcorn disease caused by Ciboria shiraiana in mulberry (Morus australis L.). Biocontrol Sci. Technol. 26:145-162.   DOI
13 Susilowati, R., Sabdono, A. and Widowati, I. 2015. Isolation and characterization of bacteria associated with brown algae Sargassum spp. from Panjang Island and their antibacterial activities. Proc. Environ. Sci. 23:240-246.   DOI
14 Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetic analysis version 6.0. Mol. Biol. Evol. 30:2725-2729.   DOI
15 Tan, X., Huang, S., Ren, J., Yan, W. and Cen, Z. 2007. Characterization of an endophytic bacterium strain Bc51 suppressing citrus canker. Acta Phytopathol. Sin. 37:9-17.   DOI
16 Tao, A., Pang, F., Huang, S., Yu, G., Li, B. and Wang, T. 2014. Characterization of endophytic Bacillus thuringiensis strains isolated from wheat plants as biocontrol agents against wheat flag smut. Biocontrol Sci. Technol. 24:901-924.   DOI
17 Das, A. K. and Singh, S. 1999. Management of bacterial canker in acid lime. Intensive Agric. 36:28-29.
18 Chen, C., Bauske, E. M., Musson, G., Rodriguezkabana, R. and Kloepper, J. W. 1995. Biological control of Fusarium wilt on cotton by use of endophytric bacteria. Biol. Control 5:83-91.   DOI
19 Cherif, A., Rezgui, W., Raddadi, N., Daffonchio, D. and Boudabous, A. 2008. Characterization and partial purification of entomocin 110, a newly identified bacteriocin from Bacillus thuringiensis subsp. entomocidus HD110. Microbiol. Res. 163:684-692.   DOI
20 Chithrashree, Udayashankar, A. C., Chandra Nayaka, S., Reddy, M. S. and Srinivas, C. 2011. Plant growth-promoting rhizobacteria mediate induced systemic resistance in rice against bacterial leaf blight caused by Xanthomonas oryzae pv. oryzae. Biol. Control 59:114-122.   DOI
21 Das, A. K. 2003. Citrus canker: a review. J. Appl. Hortic. 5:52-60.   DOI
22 Das, A. K. and Singh, S. 2001. Managing citrus bacterial diseases in the state of Maharashtra. Indian Hortic. 46:11-13.
23 Das, R., Mondal, B., Mondal, P., Khatua, D. C. and Mukherjee, N. 2014. Biological management of citrus canker on acid lime through Bacillus subtilis (S-12) in West Bengal, India. J. Biopest. 7:38-41.
24 Hallmann, J., Quadt-Hallmann, A., Miller, W. G., Sikora, R. A. and Lindow, S. E. 2002. Endophytic colonization of plants by the biocontrol agent Rhizobium etli G12 in relation to Meloidogyne incognita infection. Phytopathology 91:415-422.   DOI
25 Toure, Y., Ongena, M., Jacques, P., Guiro, A. and Thonart, P. 2004. Role of lipopeptides produced by Bacillus subtilis GA1 in the reduction of grey mould disease caused by Botrytis cinerea on apple. J. Appl. Microbiol. 96:1151-1160.   DOI
26 De Goes, K. C. G. P., de Castro Fisher, M. L., Cattelan, A. J., Nogueira, M. A., de Carvalho, C. G. P. and de Oliveira, A. L. M. 2012. Biochemical and molecular characterization of high population density bacteria isolated from sunflower. J. Microbiol. Biotechnol. 22:437-447.   DOI
27 De Oliveira Costa, L. E., de Queiroz, M. V., Borges, A. C., de Moraes, C. A. and de Araujo, E. F. 2012. Isolation and characterization of endophytic bacteria isolated from the leaves of the common bean (Phaseolus vulgaris). Braz. J. Microbiol. 43:1562-1575.   DOI
28 Dong, Y.-H., Gusti, A. R., Zhang, Q., Xu, J.-L. and Zhang, L.-H. 2002. Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl. Environ. Microbiol. 68:1754-1759.   DOI
29 Gottwald, T. R., Hughes, G., Graham, J. H., Sun, X. and Riley, T. 2001. The citrus canker epidemic in Florida: the scientific basis of regulatory eradication policy for an invasive species. Phytopathology 91:30-34.   DOI
30 Graham, J. H., Leite, R. P., Yonce, H. D. and Myers, M. 2008. Streptomycin controls citrus canker on sweet orange in Brazil and reduces risk of copper burn on grapefruit in Florida. Proc. Fla. State Hortic. Soc. 121:118-123.
31 Huang, T.-P., Tzeng, D. D.-S., Wong, A. C. L., Chen, C.-H., Lu, K.-M., Lee, Y.-H., Huang, W.-D., Hwang, B.-F. and Tzeng, K.-C. 2012. DNA polymorphisms and biocontrol of Bacillus antagonistic to citrus bacterial canker with indication of the interference of phyllosphere biofilms. PLoS ONE 7:e42124.   DOI
32 Keerthi, D., Nair, R. A. and Prasath, D. 2016. Molecular phylogenetics and anti-pythium activity of endophytes from rhizomes of wild ginger congener, Zingiber zerumbet Smith. World J. Microbiol. Biotechnol. 32:41.   DOI
33 Hyun, J.-W., Kim, H.-J., Yi, P.-H., Hwang, R.-Y. and Park, E.-W. 2012. Mode of action of streptomycin resistance in the citrus canker pathogen (Xanthomonas smithii subsp. citri) in Jeju Island. Plant Pathol. J. 28:207-211.   DOI
34 Jalan, N., Kumar, D., Yu, F., Jones, J. B., Graham, J. H. and Wang, N. 2013. Complete genome sequence of Xanthomonas citri subsp. citri strain Aw12879, a restricted-host-range citrus canker-causing bacterium. Genome Announc. 1:e00235-13.
35 Jouzani, G. S., Valijanian, E. and Sharafi, R. 2017. Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Appl. Microbiol. Biotechnol. 101:2691-2711.   DOI
36 Kloepper, J. W., Ryu, C. M. and Zhang, S. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259-1266.   DOI
37 Kim, B. S., Moon, S. S. and Hwang, B. K. 1999. Isolation, identification and antifungal activity of a macrolide antibiotic, oligomycin A, produced by Streptomyces libani. Can. J. Bot. 77:850-858.   DOI
38 Kim, P. I., Bai, H., Bai, D., Chae, H., Chung, S., Kim, Y., Park, R. and Chi, Y.-T. 2004. Purification and characterization of a lipopeptide produced by Bacillus thuringiensis CMB26. J. Appl. Microbiol. 97:942-949.   DOI
39 Kloepper, J. W. and Beauchamp, C. J. 1992. A review of issues related to measuring colonization of plant roots by bacteria. Can. J. Microbiol. 38:1219-1232.   DOI
40 Li, H.-Y., Wei, D.-Q., Shen, M. and Zhou, Z.-P. 2012. Endophytes and their role in phytoremediation. Fungal Divers. 54:11-18.   DOI
41 Wei, G., Kloepper, J. W. and Tuzun, S. 1996. Induced systemic resistance to cucumber diseases and increased plant growth by plant growth-promoting rhizobacteria under field conditions. Phytopathology 86:221-224.   DOI
42 Van Loon, L. C., Bakker, P. A. H. M. and Pieterse, C. M. J. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453-483.   DOI
43 Voloudakis, A. E., Reignier, T. M. and Cooksey, D. A. 2005. Regulation of resistance to copper in Xanthomonas axonopodis pv. vesicatoria. Appl. Environ. Microbiol. 71:782-789.   DOI
44 Webber, H. J. 1967. History and development of the Citrus industry. In: The Citrus industry, Vol. I, eds. by W. Reuther, L. D. Batchelor and H. J. Webber, pp. 1-39. University of California Press, Berkely, CA, USA.
45 Martinez-Medina, A., Fernandez, I., Sanchez-Guzman, M. J., Jung, S. C., Pascual, J. A. and Pozo, M. J. 2013. Deciphering the hormonal signaling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front. Plant Sci. 4:206.   DOI
46 Yang, H. L., Sun, X. L., Song, W. and Wang, Y. S. 2001. Studies on the rice endophytic bacteria Entetobacter cloacae MR12's identification and its effects of nitrogen fixation and biological control to plant disease. Acta Phytopathol. Sin. 31:92-93.   DOI
47 Zhou, Y., Choi, Y.-L., Sun, M. and Yu, Z. 2008. Novel roles of Bacillus thuringiensis to control plant diseases. Appl. Microbiol. Biotechnol. 80:563-572.   DOI
48 Das, A. K. and Singh, S. 2000. Management of acid lime canker by using chemicals with compatible cultural practices. In: Hitech Citrus Management: Proceedings of the International Symposium Citriculture, eds. by S. P. Ghosh and S. Singh, pp. 1054-1056. Indian Society of Citriculture and National Research Centre for Citrus, Nagpur, India.
49 Lin, D., Qu, L. J., Gu, H. and Chen, Z. 2001. A 3.1-kb genomic fragment of Bacillus subtilis encodes the protein inhibiting growth of Xanthomonas oryzae pv. oryzae. J. Appl. Microbiol. 91:1044-1050.   DOI
50 Liu, Y. Q., Heying, E. and Tanumihardjo, S. A. 2012. History, global distribution, and nutritional importance of citrus fruits. Compr. Rev. Food Sci. Food Saf. 11:530-545.   DOI
51 Patra, J. K., Das, G. and Baek, K.-H. 2015. Antibacterial mechanism of the action of Enteromorpha linza L. essential oil against Escherichia coli and Salmonella typhimurium. Bot. Stud. 56:13.   DOI
52 McManus, P. S., Stockwell, V. O., Sundin, G. W. and Jones, A. L. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443-465.   DOI
53 Mingma, R., Pathom-aree, W., Trakulnaleamsai, S., Thamchaipenet, A. and Duangmal, K. 2014. Isolation of rhizospheric and roots endophytic actinomycetes from Leguminosae plant and their activities to inhibit soybean pathogen, Xanthomonas campestris pv. glycine. World J. Microbiol. Biotechnol. 30:271-280.   DOI
54 Nam, H.-S., Yang, H.-J., Oh, B. J., Anderson, A. J. and Kim, Y. C. 2016. Biological control potential of Bacillus amyloliquefaciens KB3 isolated from the feces of Allomyrina dichotoma larvae. Plant Pathol. J. 32:273-280.   DOI
55 Paul, D. K. and Shaha, R. K. 2004. Nutrients, vitamins and minerals content in common citrus fruits in the northern region of Bangladesh. Pak. J. Biol. Sci. 7:238-242.   DOI
56 Quadt-Hallman, A., Kloepper, J. W. and Benhamou, N. 1997. Bacterial endophytes in cotton: mechanisms of entering the plant. Can. J. Microbiol. 43:557-582.
57 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.   DOI
58 Quispel, A. 1992. A search for signals in endophytic microorganisms. In: Molecular signals in plant-microbe communications, ed. by D. P. S. Verma, pp 471-490. CRC Press, Boca Raton, FL.
59 Raddadi, N., Belaouis, A., Tamagnini, I., Hansen, B. M., Hendriksen, N. B., Boudabous, A., Cherif, A. and Daffonchio, D. 2009. Characterization of polyvalent and safe Bacillus thuringiensis strains with potential use for biocontrol. J. Basic. Microbiol. 49:293-303.   DOI
60 Ramful, D., Bahorun, T., Bourdon, E., Tarnus, E. and Aruoma, O. I. 2010. Bioactive phenolics and antioxidant propensity of flavedo extracts of Mauritian citrus fruits: potential prophylactic ingredients for functional foods application. Toxicology 278:75-87.   DOI
61 Roh, E., Lee, S., Lee, Y., Ra, D., Choi, J., Moon, E. and Heu, S. 2009. Diverse antibacterial activity of Pectobacterium carotovorum subsp. carotovorum isolated in Korea. J. Microbiol. Biotechnol. 19:42-50.   DOI
62 Roh, J. Y., Choi, J. Y., Li, M. S., Jin, B. R. and Je, Y. H. 2007. Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J. Microbiol. Biotechnol. 17:547-559.
63 Rosenblueth, M. and Martinez-Romero, E. 2006. Bacterial endophytes and their interactions with hosts. Mol. Plant Microbe Interact. 19:827-837.   DOI
64 Schnepf, E., Crickmore, N., Van Rie, J., Lereclus, D., Baum, J., Feitelson, J., Zeigler, D. R. and Dean, D. H. 1998. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:775-806.   DOI