Biological control of wheat take-all disease using some biofilm-forming Bacillus subtilis strains

Babaeipoor, E., Mirzaei, S., Rezaee Danesh, Y., Arjmandian, A. & Chaichi, M. 2011. Evaluation of some antagonistic bacteria in biological control of Gaeumannomyces graminis var. tritici causal agent of wheat take-all disease in Iran. African Journal of Microbiology Research, 5: 5165-5173.

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.

Branda, S.S., Vik, A., Friedman, L. & Kolter, R. 2005. Biofilms: the matrix revisited. Trends Microbiology, 13: 20-26.

Cavaglieri, L., Passone, A. & Etcheverry, M. 2004. Screening procedures for selecting rhizobacteria with biocontrol effects upon Fusarium verticillioides growth and fumonisin B1 production. Research in Microbiology, 55: 747-754.

Chaurasia, B., Pandey, A., Palni, L.M.S., Trivedi, P., Kumar, B. & Colvin, N. 2005. Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiological Research, 160: 75-81.

Davey, M.E. & O’Toole, G.A. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Review, 64: 847-867.

Derakhshan, A., Safaei, N. & Alizadeh, A. 2008. Evaluation of epiphytotic bacteria for biocontrol of head blight and monitoring stability of antagonist population on wheat in greenhouse. Iranian Journal of Plant Pathology, 44: 267-288.

Farrokhi, F., Hajian Shahri, M., Salari, M. & Rouhani, H. 2015. The efficacy of Pythium oligandrum in the biological control of Rhizoctonia solani, the causal agent of sugar beet damping-off under greenhouse conditions. Biocontrol in Plant Protection, 3: 57-71.

Fiddaman, P.J. & Rossal, S. 1993. The production of antifungal volatile by Bacillus subtilis. Journal of Applied Bacteriology, 74: 119-126.

Fiddaman, P.J. & Rossal, S. 1994. Effect of substrate on the production of antifungal volatiles from Bacillus subtilis. Journal of Applied Bacteriology, 76: 395-405.

Foroutan, A., Rahimian, H. & Alizadeh, A. 2005. Effect of antagonistic bacteria on Fusarium head blight. Iranian Journal of Plant Pathology, 41: 455˗473. (In Persian with English summary).

Fouly, H.M., Wilkinson, H.T. & Chen, W. 1997. Restriction analysis of internal transcribed spacers and the small subunit gene of ribosomal DNA among four Gaeumannomyces species. Mycologia, 89: 590-597.

García-Gutiérrez, L., Zeriouh, H., Romero, D., Cubero, J., De Vicente, A. & Pérez-García, A. 2013. The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate- and salicylic acid-dependent defense responses. Microbial Biotechnology, 6: 264-274.

Garrett, S.D. 1981. Introduction, pp. 1-14. In: Asher, M.J.C. & Shipton, P.J. (eds.), Biology and Control of take-all.Academic Press, London.

Ghahfarokhi, R.M. & Goltapeh, M.E. 2010. Potential of the root endophytic fungus Piriformospora indica; Sebacina vermifera and Trichoderma species in biocontrol of take-all disease of wheat Gaeumannomyces graminis var. tritici in vitro, in Iran. Journal of Agriculture Science and Technology, 6: 11-18.

Henis, Y. & Inbar, M. 1968. Effect of Bacillus subtilis on growth and sclerotium formation by Rhizoctonia solani. Phytopathology, 58: 933-938.

Hornby, D., Bateman, G.L., Gutteridge, R.J., Lucas, P., Osbourn, A.E., Ward, E. & Yarham, D.J. 1998. Take-all Disease of Cereals: A Regional Perspective. CAB International, London, 384 pp.

Hsieh, F., Li, M., Lin, T. & Kao, S. 2004. Rapid detection and characterization of surfactin producing Bacillus subtilis and closely related species based on PCR. Current Microbiology, 49: 186-191.

ISTA. 2003. ISTA Handbook on Seedling Evaluation. Bassersdorf: ISTA.

Johansson, P.M., Johnsson, L., & Gerhardson B. 2003. Suppression of wheat-seedling diseases caused by Fusarium culmorum and Microdochium nivale using bacterial seed treatment. Plant Pathology, 52: 219-227.

Jolideh, F., Marefat, A.R. & Nareri, B. 2012. Occurrence of wheat take-all disease caused by Gaeumannomyces graminis var. tritici in Zanjan province and evaluation of inhibitory effect of wheat rhizosphere bacteria on the causal agent of the disease. Plant Protection (Scientific Journal of Agriculture),
35: 19-30. (In Persian with English summary).

Junaid, J.M., Dar, N.A., Bhat, T.A., Bhat, A.H. & Bhat, M.A. 2013. Commercial biocontrol agents and their mechanism of action in the management of plant pathogens. International Journal of Modern Plant and Animal Sciences, 1: 39-57.

Kempf, H.J. & Wolf, G. 1989. Erwinia herbicola as a biocontrol agent of Fusarium culmorum and Puccinia recondite f. sp. tritici on wheat. Phytopathology, 79: 990-994.

Khezri, M., Ahmadzadeh, M., Salehi-Jouzani, Gh., Behboudi, K., Ahangaran, A., Mousivand, M. & Rahimian, H. 2011. Characterization of some biofilm-forming Bacillus subtilis and evaluation of their biocontrol potential against Fusarium culmorum. Journal of Plant Pathology, 93: 373-382.

Khezri, M. 2016. Influence of some environmental and nutritional conditions on biofilm formation of probiotic Bacillus subtilis strains. Biological Control of Pests and Plant Diseases, 4: 157-165. (In Persian with English summary).

Kim, D.S., Cook, R.J. & Weller, D.M. 1997. Bacillus sp. L324-92 for biological control of three root diseases of wheat grown with reduced tillage. Phytopathology, 87: 551-558.

Kim, H.S., Park, J., Choi, S.W., Choi, K.H., Lee, G.P., Ban, S.J., Lee, C.H. & Chung, S.K. 2003. Isolation and characterization of Bacillus strain for biological control. Journal of Microbiology, 41: 196˗201.

Kloepper, J.W., Ryu, C.M. & Zhang, S.A. 2004. Induced system resistance and promotion of plant growth by Bacillus spp. Phytopathology, 94: 1259-1266.

Kovács, A.T., Smits, W.K., Miron´czuk, A.M. & Kuipers, O.P. 2009. Ubiquitous late competence genes in Bacillus species indicate the presence of functional DNA uptake machineries. Environmental Microbiology, 11: 1911-1922.

Kumar, A., Saini, P. & Shrivastava, J.N. 2009. Production of peptide antifungal antibiotic and biocontrol activity of Bacillus subtilis. Indian Journal of Experimental Biology, 47: 57-62.

Kwak, Y.S. & Weller, D.M. 2013. Take-all of Wheat and Natural Disease Suppression: A Review. The Plant Pathology Journal, 29: 125-135.

Lagzian, A., Saberi Riseh, R., Khodaygan, P., Sedaghati, E. & Dashti, D. 2013. Introduced Pseudomonas fluorescens VUPf5 as an important biocontrol agent for controlling Gaeumannomyces graminis var. tritici the causal agent of take-all disease in wheat. Archive of Phytopathology and Plant Protection, 46: 2104-2116.

Leclere, V., Bechet, M., Adam, A., Guez, J.S., Wathelet, B. & Ongena, M. 2005. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism’s antagonistic and biocontrol activities. Applied and Environmental Microbiology, 71: 4577-4584.

Mohammadi, K., Rahimian, H., Etebarian, H.R. & Ghalandar, M. 2005. Biological control of common root rot of wheat by antagonistic bacteria isolated from wheat rhizosphere. Iranian Journal of Plant Pathology, 41: 173-177.

Molina, M.A., Ramos, J.L. & Urgel, M.E. 2003. Plant-associated biofilms. Review in Environmental Science and Biotechnology, 2: 99-108.

Morikawa, M. 2006. Beneficial biofilm formation by industrial bacteria Bacillus subtilis and related species. Journal of Bioscience and Bioengineering, 101: 1-8.

Morris, C. & Monier, J.M. 2003. The ecological significance of biofilm formation by plant-associated bacteria. Annual Review of Phytopathology, 41: 429-453.

Nagórska, K., Hinc, K., Stauch, M.A. & Obuchowski, M. 2008. Influence of the sigma B stress factor and yxaB, the gene for a putative exopolysaccharide syntheses under sigmaB control, on biofilm formation. Journal of Bacteriology, 190: 3546-3556.

Nasraoui, B., Hajlaoui, M.R., Aïssa, A.D. & Kremer, R.J. 2007. Biological control of wheat take-all disease: I-Characterization of antagonistic bacteria from diverse soils toward Gaeumannomyces graminis var. tritici. Tunisian Journal of Plant Protection, 2: 23-34.

Ongena, M., Duby, F., Jourdan, E., Beaudry, T., Jadin, V., Dommes, J. & Thonart, P. 2005. Bacillus subtilis M4 decreases plant susceptibility towards fungal pathogens by increasing host resistance associated with differential gene expression. Applied Microbiology and Biotechnology, 67: 692-698.

Ongena, M. & Jacques, P. 2007. Bacillus lipopeptides: Versatile weapons for plant disease control. Trends Microbiology, 16:115-125.

Onkar, D. & James, B. 1995. Basic Plant Pathology Methods. London, Lewis publisher. 448pp.

Orio, A.G.A., Brücher, E. & Ducasse, D.A. 2016. A strain of Bacillus subtilis subsp. subtilis shows a specific antagonistic activity against the soil-borne pathogen of onion Setophoma terrestris. European Journal of Plant Pathology, 144: 217-223.

Pyoung, K., Ryu, J., Kim, Y.H. & Chi, W. T. 2010. Production of Biosurfactant Lipopeptides Iturin A, Fengycin, and Surfactin A from Bacillus subtilis CMB32 for Control of Colletotrichum gloeosporioides. Journal of Microbiology and Biotechnology, 20: 138-145.

Prigent-Combaret, C., Vidal, O., Dorel, C. and Lejeune, P. 1999. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. Journal of Bacteriology, 181: 5993-6002.

Quecine, M.C., Araujo, W.L., Marcon, J., Gai1, C.S. Azevedo, J.L. & Pizzirani-Kleiner, A.A. 2008. Chitinolytic activity of endophytic Streptomyces and potential for biocontrol. Letters in Applied Microbiology, 47: 486-491.

Rajabi, G. H., & Behrozin, M. 2003. Pests and Diseases of Wheat in Iran. Agricultural Education Publications, 186 pp. (In Persian).

Sadeghi, L., Alizadeh, A., Safaei, N. & Ghalandar, M. 2009. Identification of Iranian populations of Gaeumannomyces graminis var. tritici using morphological, molecular and pathological studies. Iranian Journal of Plant Pathology, 45: 99-114. (In Persian with English summary).

Sakalauskas, S., Kacergius, A., Janusauskaite, D. & Citavicius, D. 2014. Bacteria with a broad-spectrum of antagonistic activity against pathogenic fungi of cereals. Zemdirbyste-Agriculture, 101:185-192.

Schoeny, A., Lucas, P. & Jeuffroy, M.H. 1998. Influence of the incidence and severity of take-all of winter wheat on yield losses and responses to different nitrogen fertilizations, pp. 83-88. In: Proceedings of the British Crop Protection Conference-Pests and Diseases, 1998. Farnham, UK.

Singleton, L.L. 1992. Methods for Research on Soilborne Phytopathogenic Fungi. APS Press, St. Paul, MN, 266 pp.

Stein, T. 2005. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Molecular Microbiology, 56: 845-857.

Sumi, C.D., Yang, B.W., Yeo, I. & Hahm, Y.T. 2015. Antimicrobial peptides of the genus Bacillus: a new era for antibiotics. Canadian Journal of Microbiology, 61: 93-103.

Wang, X., Mavrodi, D.V., Ke, L., Mavrodi, O.V., Yang, M., Thomashow, L.S., Zheng, N., Weller, D.M. & Zhang, J. 2015. Biocontrol and plant growth-promoting activity of rhizobacteria from Chinese fields with contaminated soils. Microbial Biotechnology, 8: 404-418.

Weller, D.M. & Cook, R.J. 1983. Suppression of take-all of wheat by seed treatment with fluorescent pseudomonades. Phytopathology, 73: 463-469.

Wiese, M.V. 1987. Compendium of wheat. Second Edition. APS Press, St. Paul, MN, 112 pp.

Yi, H.S., Ahn ,Y.R., Song, G.C., Ghim, S.Y., Lee, S., Lee, G. & Ryu, C.M. 2016. Impact of a bacterial volatile 2, 3-butanediol on Bacillus subtilis rhizosphere robustness. Frontiers in Microbiology, 7: 1-11.

Zeriouh, H., De Vicente, A., Pérez-García, A. & Romero, D. 2014. Surfactin triggers biofilm formation of Bacillus subtilis in melon phylloplane and contributes to the biocontrol activity. Environmental Microbiology, 16: 2196-2211.