A novel rhizobacterium Bk7 for biological control of brown sheath rot of rice caused by Pseudomonas fuscovaginae and its mode of action

European Journal of Plant Pathology

Volumn 138, Issue 4, 2014, Pages 819-834

  Kakar, Kaleem Ullah ^a   Duan, Y P ^b   Nawaz, Zarqa ^c   Sun, Guochang ^d   Almoneafy, Abdlwareth A ^a   Hassan, M Auwal ^e   Elshakh, Ahmed ^a   Li, Bin ^a   Xie, Guan Lin ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c ZHEJIANG UNIVERSITY   (China)

^d INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^e ZHEJIANG UNIVERSITY   (China)

Author keywords

Antimicrobial peptide coding genes; Biofilm formation; Brown sheath rot of rice; Multiplex PCR; RT qPCR

Indexed keywords

ANTIMICROBIAL ACTIVITY; BACTERIAL DISEASE; BIOCONTROL AGENT; BIOFILM; DISEASE INCIDENCE; GROWTH RATE; POLYMERASE CHAIN REACTION; RHIZOBACTERIUM;

BACILLUS (BACTERIUM); BACILLUS AMYLOLIQUEFACIENS; BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS FUSCOVAGINAE; RHIZOBIUM;

EID: 84895789721     PISSN: 09291873     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10658-013-0356-7     Document Type: Article

References (77)

1. Ahmad, F., Ahmad, I., & Khan, M. S. (2008). Screening of free-living rhizobacteria for their multiple plant growth promoting activities. Microbiological Research, 163, 173-181.
2. Almoneafy, A. A., Ojaghian, M. R., Seng-fu, X., Ibrahim, M., Guan-Lin, X., Yu, S., et al. (2013). Synergistic effect of acetyl salicylic acid and DL-Beta-aminobutyric acid on biocontrol efficacy of Bacillus strains against tomato bacterial wilt. Tropical Plant Pathology, 38, 102-113.
3. Aneja, K. R. (2001). Experiments in microbiology, plant pathology, tissue culture and mushroom production technology: new age international limited. Annals of the Phytopathological Society of Japan, 42, 540-548.
4. Bais, H. P., Fall, R., & 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 Physiology, 134, 307-319.
5. Beneduzi, A., Peres, D., Vargas, L. K., Bodanese-Zanettini, M. H., & Passaglia, L. M. P. (2008). Evaluation of genetic diversity and plant growth promoting activities of nitrogen-fixing bacilli isolated from rice fields in South Brazil. Applied Soil Ecology, 39, 311-320.
6. Carrillo, C., Teruel, J. A., Aranda, F. J., & Ortiz, A. (2003). Molecular mechanism of membrane permeabilization by the peptide antibiotic surfactin. Biochimica et Biophysica Acta - Biomembranes, 1611, 91-97.
7. Chae Gun, P., Shoda, M., & Kubota, H. (1990). Suppressive effect of Bacillus subtilis and its products on phytopathogenic microorganisms. Journal of Fermentation and Bioengineering, 69, 1-7.
8. Chen, X. H., Scholz, R., Borriss, M., Junge, H., Mögel, G., Kunz, S., et al. (2009). Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. Journal of Biotechnology, 140, 38-44.
9. Chumthong, A., Kanjanamaneesathian, M., Pengnoo, A., & Wiwattanapatapee, R. (2008). Water-soluble granules containing Bacillus megaterium for biological control of rice sheath blight: formulation, bacterial viability and efficacy testing. World Journal of Microbiology and Biotechnology, 24, 2499-2507.
10. Cother, E. J., Stodart, B., Noble, D. H., Reinke, R., & Ven, R. J. (2009). Polyphasic identification of Pseudomonas fuscovaginae causing sheath and glume lesions on rice in Australia. Australasian Plant Pathology, 38, 247-261.
11. Davey, M. E., & O'toole, G. A. (2000). Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews, 64(4), 847-867.
12. FAO (2011). Food and Agricultural Organization (FAOSTAT) Production. http://faostat. fao. org/. Accessed 5 May 2013.
13. Figueiredo, M. d. V. B., Seldin, L., de Araujo, F. F., & Mariano, R. d. L. R. (2011). Plant growth promoting rhizobacteria: fundamentals and applications. In Plant growth and health promoting bacteria (pp. 21-43). Berlin Heidelberg: Springer.
14. Fravel, D. R. (1988). Role of antibiosis in the biocontrol of plant diseases*. Annual Review of Phytopathology, 26, 75-91.
15. Gao, W., Zhang, W., & Meldrum, D. R. (2011). RT-qPCR based quantitative analysis of gene expression in single bacterial cells. Journal of Microbiological Methods, 85(3), 221-227.
16. Glick, B. R., Todorovic, B., Czarny, J., Cheng, Z., Duan, J., & McConkey, B. (2007). Promotion of plant growth by bacterial acc deaminase. Critical Reviews in Plant Sciences, 26(5-6), 227-242.
17. Gordon, S. A., & Weber, R. P. (1951). Colorimetric estimation of indoleacetic acid. Plant Physiology, 26(1), 192-195.
18. Govindasamy, V., Senthilkumar, M., Magheshwaran, V., Kumar, U., Bose, P., Sharma, V., et al. (2011). Bacillus and Paenibacillus spp.: Potential PGPR for sustainable agriculture. In D. K. Maheshwari (Ed.), Plant growth and health promoting bacteria (Vol. 18, pp. 333-364, Microbiology Monographs) Berlin: Springer.
19. Grosch, R., Faltin, F., Lottmann, J., Kofoet, A., & Berg, G. (2005). Effectiveness of 3 antagonistic bacterial isolates to control Rhizoctonia solani Kühn on lettuce and potato. Canadian Journal of Microbiology, 51, 345-353.
20. Guo, J.-H., Qi, H.-Y., Guo, Y.-H., Ge, H.-L., Gong, L.-Y., Zhang, L.-X., et al. (2004). Biocontrol of tomato wilt by plant growth-promoting rhizobacteria. Biological Control, 29, 66-72.
21. Hallmann, J., Quadt-Hallmann, A., Mahaffee, W., & Kloepper, J. (1997). Bacterial endophytes in agricultural crops. Canadian Journal of Microbiology, 43(10), 895-914.
22. Harish, S., Kavino, M., Kumar, N., Balasubramanian, P., & Samiyappan, R. (2009). Induction of defense-related proteins by mixtures of plant growth promoting endophytic bacteria against Banana bunchy top virus. Biological Control, 51, 16-25.
23. Hayat, R., Ali, S., Amara, U., Khalid, R., & Ahmed, I. (2010). Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology, 60, 579-598.
24. Hiradate, S., Yoshida, S., Sugie, H., Yada, H., & Fujii, Y. (2002). Mulberry anthracnose antagonists (iturins) produced by Bacillus amyloliquefaciens RC-2. Phytochemistry, 61, 693-698.
25. Idriss, E. E., Makarewicz, O., Farouk, A., Rosner, K., Greiner, R., Bochow, H., et al. (2002). Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology, 148, 2097-2109.
26. Joshi, R., & McSpadden-Gardener, B. B. (2006). Identification and characteri-zation of novel genetic markers associated with biological control activities in Bacillus subtilis. Phytopathology, 96, 145-154.
27. Kakar, K. U., Nawaz, Z., Cui, Z., Almoneafy, A. A., Zhu, B., & Xie, G.-L. (2013). Characterizing the mode of action of Brevibacillus laterosporus B4 for control of bacterial brown strip of rice caused by A. avenae subsp. avenae RS-1. World Journal of Microbiology and Biotechnology, 29, 1-10.
28. Kenig, M., Vandamme, E., & Abraham, E. (1976). The mode of action of bacilysin and anticapsin and biochemical properties of bacilysin-resistant mutants. Journal of General Microbiology, 94(1), 46-54.
29. Kerkar, S., Raiker, L., Tiwari, A., Mayilraj, S., & Dastager, S. (2012). Biofilm-associated indole acetic acid producing bacteria and their impact in the proliferation of biofilm mats in solar salterns. Biologia, 67, 454-460.
30. Khan, M., Zaidi, A., Wani, P., & Oves, M. (2009). Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environmental Chemistry Letters, 7, 1-19.
31. Koumoutsi, A., Chen, X. H., Henne, A., Liesegang, H., Hitzeroth, G., Franke, P., et al. (2004). Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens Strain FZB42. Journal of Bacteriology, 186, 1084-1096.
32. Krebs, B., Hoeding, B., Kubart, S. M., Workie, A., Junge, H., Schmiedeknecht, G., et al. (1998). Use of Bacillus subtilis as biocontrol agent. I. Activities and characterization of Bacillus subtilis strains. Journal of Plant Disease and Protection, 105, 181-197.
33. Landa, B., Navas-Cortés, J., & Jiménez-Díaz, R. (2004). Influence of temperature on plant-rhizobacteria interactions related to biocontrol potential for suppression of fusarium wilt of chickpea. Plant Pathology, 53(3), 341-352.
34. Leelasuphakul, W., Sivanunsakul, P., & Phongpaichit, S. (2006). Purification, characterization and synergistic activity of β-1, 3-glucanase and antibiotic extract from an antagonistic Bacillus subtilis NSRS 89-24 against rice blast and sheath blight. Enzyme and Microbial Technology, 38, 990-997.
35. Li, Q., Li, Y., Zhu, X., & Cai, B. (2008). Isolation and characterization of atrazine-degrading Arthrobacter Sp. Ad26 and use of this strain in bioremediation of contaminated soil. Journal of Environmental Sciences, 20, 1226-1230.
36. Li, B., Liu, B.-P., Yu, R.-R., Lou, M.-M., Wang, Y.-L., Xie, G.-L., et al. (2011a). Phenotypic and molecular characterization of rhizobacterium Burkholderia sp. strain R456 antagonistic to Rhizoctonia solani, sheath blight of rice. World Journal of Microbiology and Biotechnology, 27, 2305-2313.
37. Li, W., Li, L., Li, K., Lin, J., Sun, X., & Tang, K. (2011b). Expression of biologically active human insulin-like growth factor 1 in Arabidopsis thaliana seeds via oleosin fusion technology. Biotechnology and Applied Biochemistry, 58, 139-146.
38. Lin, S. C., Lin, K. G., Lo, C. C., & Lin, Y. M. (1998). Enhanced biosurfactant production by a Bacillus licheniformis mutant. Enzyme and Microbial Technology, 23, 267-273.
39. Liu, H., Tian, W.-X., Ibrahim, M., Li, B., Zhang, G.-Q., Zhu, B., et al. (2012). Characterization of pilP, a gene required for twitching motility, pathogenicity, and biofilm formation of Acidovorax avenae subsp. avenae RS-1. European Journal of Plant Pathology, 134(3), 551-560.
40. Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25, 402-408.
41. Mattiuzzo, M., Bertani, I., Ferluga, S., Cabrio, L., Bigirimana, J., & Guarnaccia, C. (2011). The plant pathogen Pseudomonas fuscovaginae contains two conserved quorum sensing systems involved in virulence and negatively regulated by RsaL and the novel regulator RsaM. Environmental Microbiology, 13, 145-162.
42. Mora, I., Cabrefiga, J., & Montesinos, E. (2011). Antimicrobial peptide genes in Bacillus strains from plant environments. International Microbiology, 14, 213-223.
43. Moyne, A. L., Shelby, R., Cleveland, T. E., & Tuzun, S. (2001). Bacillomycin D: an iturin with antifungal activity against Aspergillus flavus. Journal of Applied Microbiology, 90, 622-629.
44. Murashige, T., & Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum, 15, 473-497.
45. Ng, L., Sariah, M., Sariam, O., Radziah, O., & Abidin, M. Z. (2012). Rice seed bacterization for promoting germination and seedling growth under aerobic cultivation system. Australian Journal of Crop Science, 6(1), 170.
46. Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., et al. (2007). Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental Microbiology, 9, 1084-1090.
47. Paynter, Q. (2005). Evaluating the impact of the biological control agent Carmenta mimosa on the woody wetland weed Mimosa pigra in Australia. Journal of Applied Ecology, 42, 1054-1062.
48. Peypoux, F., Bonmatin, J. M., & Wallach, J. (1999). Recent trends in the biochemistry of surfactin. Applied Microbiology and Biotechnology, 51, 553-563.
49. Pikovskaya, R. I. (1948). Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya, 17, 362-370.
50. Quintero, Y., Poblet, M., Guillamón, J. M., & Mas, A. (2009). Quantification of the expression of reference and alcohol dehydrogenase genes of some acetic acid bacteria in different growth conditions. Journal of Applied Microbiology, 106, 666-674.
51. Ramey, B. E., Matthysse, A. G., & Fuqua, C. (2004). The FNR-type transcriptional regulator SinR controls maturation of Agrobacterium tumefaciens biofilms. Molecular Microbiology, 52, 1495-1511.
52. Raupach, G. S., & Kloepper, J. W. (2000). Biocontrol of cucumber diseases in the field by plant growth-promoting rhizobacteria with and without methyl bromide fumigation. Plant Disease, 84, 1073-1075.
53. Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Wei, H.-X., Paré, P. W., et al. (2003). Bacterial volatiles promote growth in Arabidopsis. Proceedings of the National Academy of Sciences, 100, 4927-4932.
54. Schwyn, B., & Neilands, J. B. (1987). Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry, 160, 47-56.
55. Seneviratne, G., Zavahir, J. S., Bandara, W. M. M. S., & Weerasekara, M. L. M. A. W. (2007). Fungal-bacterial biofilms: their development for novel biotechnological applications. World Journal of Microbiology and Biotechnology, 24, 739-743.
56. Seneviratne, G., Zavahir, J. S., Bandara, W. M. M. S., & Weerasekara, M. L. M. A. W. (2008). Fungal-bacterial biofilms: their development for novel biotechnological applications. World Journal of Microbiology and Biotechnology, 24, 739-743.
57. Seneviratne, G., Thilakaratne, R., Jayasekara, A., Seneviratne, K., Padmathilake, K. R. E., & Silva, M. (2009). Developing beneficial microbial biofilms on roots of non legumes: A novel biofertilizing technique. In M. S. Khan, A. Zaidi, & J. Musarrat (Eds.), Microbial strategies for crop improvement (pp. 51-62). Berlin: Springer.
58. Seneviratne, G., Weerasekara, M. L. M. A. W., Seneviratne, K. A. C. N., Zavahir, J. S., Kecskés, M. L., & Kennedy, I. R. (2011). Importance of biofilm formation in plant growth promoting rhizobacterial action. In D. K. Maheshwari (Ed.), Plant growth and health promoting bacteria (Vol. 18, pp. 81-95, Microbiology Monographs): Berlin: Springer.
59. Singh, J. S., Pandey, V. C., & Singh, D. P. (2011). Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agriculture, Ecosystems & Environment, 140, 339-353.
60. Song, F., & Goodman, R. M. (2001). Molecular biology of disease resistance in rice. Physiological and Molecular Plant Pathology, 59, 1-11.
61. Srinivas, K. P., Sreekanth Reddy, M., Hema, M., & Sreenivasulu, P. (2013). Multiplex RT-PCR for parallel detection of three RNA viruses associated with stripe and mosaic diseases of sorghum in India. European Journal of Plant Pathology, 137, 211-215.
62. Stanley, N. R., Britton, R. A., Grossman, A. D., & Lazazzera, B. A. (2003). Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. Journal of Bacteriology, 185(6), 1951-1957.
63. Tanii, A., Miyajima, K., & Akita, T. (1976). The sheath brown rot disease of rice and its causal bacterium Pseudomonas fuscovaginae sp. nov.
64. Timmusk, S., Grantcharova, N., & Wagner, E. G. H. (2005). Paenibacillus polymyxa invades plant roots and forms biofilms. Applied and Environmental Microbiology, 71(11), 7292-7300.
65. Vasudevan, P., Reddy, M., Kavitha, S., Velusamy, P., Paulraj, R., Purushothaman, S., et al. (2002). Role of biological preparations in enhancement of rice seedling growth and grain yield. Current Science, 83(9), 1140-1143.
66. Wang, Y., Li, L., Li, B., Wu, G., Tang, Q., Ibrahim, M., et al. (2012). Action of chitosan against Xanthomonas pathogenic bacteria isolated from Euphorbia pulcherrima. Molecules, 17, 7028-7041.
67. Weller, D. M. (1988). Biological control of soilborne plant pathogens in the rhizosphere with bacteria. Annual Review of Phytopathology, 26, 379-407.
68. Wiwattanapatapee, R., Chumthong, A., Pengnoo, A., & Kanjanamaneesathian, M. (2007). Effervescent fast-disintegrating bacterial formulation for biological control of rice sheath blight. Journal of Controlled Release, 119, 229-235.
69. Xu, J. M., Cheng, H. H., Koskinen, W. C., & Molina, J. A. E. (1997). Characterization of potentially bioreactive soil organic carbon and nitrogen by acid hydrolysis. Nutrient Cycling in Agroecosystems, 49, 267-271.
70. Yang, J. H., Liu, H. X., Zhu, G. M., Pan, Y. L., Xu, L. P., & Guo, J. H. (2008). Diversity analysis of antagonists from rice-associated bacteria and their application in biocontrol of rice diseases. Journal of Applied Microbiology, 104, 91-104.
71. Yang, D., Wang, B., Wang, J., Chen, Y., & Zhou, M. (2009). Activity and efficacy of Bacillus subtilis strain NJ-18 against rice sheath blight and Sclerotinia stem rot of rape. Biological Control, 51, 61-65.
72. Yu, G. Y., Sinclair, J. B., Hartman, G. L., & Bertagnolli, B. L. (2002). Production of iturin A by Bacillus amyloliquefaciens suppressing Rhizoctonia solani. Soil Biology and Biochemistry, 34, 955-963.
73. Zaidi, A., Khan, M., Ahemad, M., & Oves, M. (2009). Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiologica et Immunologica Hungarica, 56, 263-284.
74. Zehnder, G., Yao, C., Murphy, J., Sikora, E., & Kloepper, J. (2000). Induction of resistance in tomato against cucumber mosaic cucumovirus by plant growth-promoting rhizobacteria. BioControl, 45, 127-137.
75. Zeigler, R. S., & Alvarez, E. (1987). Bacterial sheath brown rot of rice by Pseudomonas fuscovaginae in Latin America. Plant Disease, 71, 592-597.
76. Zhang, R. S., Liu, Y. F., Luo, C. P., Wang, X. Y., Liu, Y. Z., Qiao, J. Q., et al. (2012). Bacillus amyloliquefaciens Lx-11, a potential biocontrol agent against rice bacterial leaf streak. Journal of Plant Pathology, 94, 609-619.
77. Zhao, J., Li, Y., Zhang, C., Yao, Z., Zhang, L., Bie, X., et al. (2012). Genome shuffling of Bacillus amyloliquefaciens for improving antimicrobial lipopeptide production and an analysis of relative gene expression using FQ RT-PCR. Journal of Industrial Microbiology & Biotechnology, 39, 889-896.