Biological control of downy mildew of maize caused by Peronosclerospora sorghi under environmentally controlled conditions
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Abstract
Downy mildew disease, caused by Peronosclerospora sorghi, is one of the most serious diseases of maize. The disease is currently managed by seed treatment with metalaxyl fungicides. However, problems regarding environmental pollution resulting from the use of fungicides and development of fungicide resistance within populations of P. sorghi are of increasing concern. Assuming that biological control by means of using antagonistic microorganisms may be an alternative for the management of this disease, the efficacy of biocontrol agents viz., Bacillus subtilis G1, Bacillus amyloliquefaciens B2, Brevibacillus brevis 57 and Pseudomonas fluorescens Pf1 for the management of downy mildew of maize and for promoting plant growth was evaluated. The results indicated that seed treatment with B. subtilis G1 and B. amyloliquefaciens B2 significantly (P = 0.05) increased the germination percentage and seedling vigour of maize as assessed by roll towel method. Among them, B. subtilis G1 was the most effective and recorded 9% and 31% increases in germination percentage and seedling vigour of maize respectively, as compared to the control. A talc- based powder formulation of B. subtilis G1 when applied through seed at the rate of 10 g/kg reduced the downy mildew incidence up to 54% under greenhouse conditions. Results of this study suggest that B. subtilis G1 is a promising bioagent for the management of downy mildew of maize and for promoting plant growth. This antagonist could be further exploited for commercial scale up for ecofriendly management of downy mildew of maize under localized climatic conditions.
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Keywords
Bacillus subtilis, Biocontrol, Downy mildew, Peronosclerospora sorghi, Zea mays
References
Amin, N., Daha, L., Nasruddin, A., Junaed, M. and Iqbal, A. (2013). The use of endophytic fungi as biopesticide against downy mildew Peronosclerospora spp. on maize. Acad. Res Int. 4: 153-159.
Anahosur, K. H. and Patil, S. H. (1980). Chemical control of sorghum downy mildew in India. Plant Dis. 64: 1004-1006.
Baki, A.A.A. and Anderson, J.D. (1973). Vigour determina-tion in soybean seed by multiple criteria. Crop Sci. 31: 630-633.
Beauregard, P.B., Chai, Y., Vlamakis, H., Losick, R. and Kolter, R. (2013). Bacillus subtilis biofilm induction by plant polysaccharides. Proc. Natl. Acad. Sci USA 110: 1621-1630.
Bock, C.H., Jeger, M.J., Mughogho, L.K., Cardwell, K.F., Mtisi, E., Kaula, G. and Mukansabimana, D. (2000). Variability of Peronosclerospora sorghi isolates from different geographic locations and hosts in Africa. My-col Res. 104: 61-68.
Bock, C.H., Jeger, M.J., Mughogho, L.K., Mtisi, E. and Cardwell, K.F. (1998). Production of conidia by Per-onosclerospora sorghi on sorghum crops in Zimbabwe. Plant Pathol. 47: 243-251.
Bonman, J.M., Renfro, B.L. and Singburaudom, N. (1983). Correlation between resistance in maize to local and systemic infection by Peronosclerospora sorghi in Thailand. Plant Dis. 67: 219-220.
Choudhary, D.K. and Johri, B.N. (2009). Interactions of Bacillus spp. and plants with special reference to in-duced systemic resistance (ISR). Microbiol. Res. 164: 493-513.
Cohen, Y. and Sherman, Y. (1977). The role of airborne conidia in epiphytotics of Sclerospora sorghi on sweet corn. Phytopathology 67: 515-521.
Craig, J. (1982). Identification of sorghum downy mildew resistance in corn by leaf reaction to conidial inoculum. Phytopathology 72: 351-352.
Earl, A.M., Losick, R. and Kolter, R. (2008). Ecology and genomics of Bacillus subtilis. Trends Microbiol. 16: 269-275.
Furuya, S., Mochizuki, M., Aoki, Y., Kobayashi, H., Takaya-nagi, T., Shimizu, M. and Suzuki, S. (2011). Isolation and characterization of Bacillus subtilis KS1 for the biocontrol of grapevine fungal diseases. Biocontrol Sci. Technol. 21: 705-720.
Gomez, K.A. and Gomez, A.A. (1984). Statistical procedure for agricultural research. New York, USA.
Guo, Q., Li, S., Lu, X., Zhang, X., Wang, P. and Ma, P. (2014). Complete genome sequence of Bacillus subtilis BAB-1, a biocontrol agent for suppression of tomato gray mold. Genome Announc. 2(4):e00744-14.
Hu, X., Roberts, D.P., Xie, L., Maul, J.E., Yu, C., Li, Y., Jiang, M., Liao, X., Che, Z. and Liao, X. (2014). For-mulations of Bacillus subtilis BY-2 suppress Sclerotinia sclerotiorum on oilseed rape in the field. Biol. Control 70: 54-64.
International Seed Testing Association. (1996). International Rules for Seed Testing. Seed Sci. Technol. Supp. 24: 155-202.
Isakeit, T. and Jaster, J. (2005). Texas has a new pathotype of Peronosclerospora sorghi, the cause of sorghum downy mildew. Plant Dis. 89: 529.
Jayaraj, J., Radhakrishnan, N.V., Kannan, R., Sakthivel, K., Suganya, D., Venkatesan, S. and Velazhahan, R. (2005). Development of new formulations of Bacillus subtilis for management of tomato damping-off caused by Pythium aphanidermatum. Biocontrol Sci. Technol. 15: 55-65.
Khabbaz, S.E. and Abbasi, P.A. (2014). Isolation, characteri-zation, and formulation of antagonistic bacteria for the management of seedlings damping-off and root rot disease of cucumber. Can. J. Microbiol. 60: 25-33.
King, E.O., Ward, M. K. and Raney, D. E. (1954). Two sim-ple media for the demonstration of pyocyanine and fluorescein. J. Lab. Clin. Med. 44: 301-307.
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.
Lahlali, R., Peng, G., Gossen, B.D., McGregor, L., Yu, F.Q., Hynes, R.K., Hwang, S.F., McDonald, M.R. and Boyetchko, S.M. (2013). Evidence that the biofungicide Serenade (Bacillus subtilis) suppresses clubroot on ca-nola via antibiosis and induced host resistance. Phyto-pathology 103: 245-254.
Liu, Y., Tao, J., Yan, Y., Li, B., Li, H. and Li, C. (2011). Biocontrol efficiency of Bacillus subtilis SL-13 and characterization of an antifungal chitinase. Chin. J. Chem. Eng. 19: 128-134.
Lukman, R., Afifuddin, A. and Lubberstedt, T. (2013). Un-raveling the genetic diversity of maize downy mildew in Indonesia. J. Plant Pathol. Microb. 4: 162.
Manjula, K. and Podile, A.R. (2005). Production of fungal cell wall degrading enzymes by a biocontrol strain of Bacillus subtilis AF1. Ind. J. Exp. Bot. 43: 892-896.
Mathiyazhagan, S., Karthikeyan, M., Sandosskumar, R. and Velazhahan, R. (2008). Analysis of variability among the isolates of Peronosclerospora sorghi from sorghum and corn based on restriction fragment length polymor-phism of ITS region of ribosomal DNA. Arch. Phytopa-thol. Plant Protect. 41: 231-237.
Meena, B., Marimuthu, T., Vidyasekaran, P. and Velazha-han, R. (2001). Biological control of root rot of ground-nut with antagonistic Pseudomonas fluorescens strains. J. Plant Dis. Protect. 108: 368-381.
Narayana, Y.D., Mughogho, L.K. and Bandyopadhyay, R. (1995). Evaluation of greenhouse inoculation tech-niques to screen sorghum for resistance to downy mil-dew. Euphytica 86: 49-53.
Ongena, M. and Jacques, P. (2008). Bacillus lipopeptides: versatile weapons for plant disease control. Trends Mi-crobiol 16: 115-125.
Perez-Garcia, A., Romero, D., De Vicente, A. (2011). Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotech. 22: 187-193.
Perumal, R., Isakeit, T., Menz, M., Katile, S., No, E.G. and Magill, C.W. (2006). Characterization and genetic dis-tance analysis of isolates of Peronosclerospora sorghi using AFLP fingerprinting. Mycol. Res. 110: 471-78.
Ramalingham, A. and Rajasab, A.H. (1981). Epidemiology of sorghum downy mildew. VI. Relative importance of oospores and conidia in epidemics of systemic infec-tion. Proc. Indian Nat. Sci. Acad. Part B 47: 625-630.
Rashid, Z., Zaidi, P. H., Vinavan, M. T., Sharma, S. S. and Srirama Setty, T. A. (2013). Downy mildew resistance in maize (Zea mays L.) across Peronosclerospora spe-cies in lowland tropical Asia. Crop Prot. 43: 183-191.
Sadoma, M.T, El-Sayed, A.B.B. and El-Moghazy, S.M. (2011). Biological control of downy mildew disease of maize caused by Peronosclerospora sorghi using cer-tain biocontrol agents alone or in combination. J. Agric. Res. Kafer El-Sheikh Univ. 37 (1): 1-11.
Schisler, D.A., Slininger, P.J., Behle, R.W. and Jackson, M.A. (2004). Formulation of Bacillus spp. for biological control of plant diseases. Phytopathology 94: 1267-1271.
Shifa. H., Gopalakrishnan, C. and Velazhahan R. (2015a). Efficacy of Bacillus subtilis G-1 in suppression of stem rot caused by Sclerotium Rolfsii and growth promotion of groundnut. International Journal of Agriculture, Environment and Biotechnology. 8(1): 111-118.
Shifa. H., Gopalakrishnan, C. and Velazhahan R. (2015b). Characterisation of antifungal antibiotics produced by Bacillus subtilis G-1 antagonistic to Sclerotium rolfsii. Biochem. Cell. Archives. 15(1): 99-104.
Sireesha, Y. and Velazhahan, R. (2015). Assessing genetic diversity in Peronosclerospora sorghi causing downy mildew on maize and sorghum. Indian Phytopath. 68 (1): 73-77.
Sivasakthi, S., Usharani, G. and Saranraj, P. (2014). Biocon-trol potentiality of plant growth promoting bacteria (PGPR)- Pseudomonas fluorescens and Bacillus sub-tilis: A review. African J. Agric. Res. 9: 1265-1277.
Stein, T. (2005). Bacillus subtilis antibiotics: structures, synthe-ses and specific functions. Mol. Microbiol. 56: 845-857.
Thompson, D.C. (1996). Evaluation of bacterial antagonist for reduction of summer patch symptoms in Kentucky blue grass. Plant Dis. 80: 856-862.
Vidhyasekaran, P. and Muthamilan, M. (1995). Development of formulations of Pseudomonas fluorescens for control of chickpea wilt. Plant Dis. 79: 782-786.
Yanez-Mendizabal, V., Vinas, I., Usall, J., Torres, R., Sol-sona, C., Abadias, M. and Teixido, N. (2012). Formula-tion development of the biocontrol agent Bacillus subtilis strain CPA-8 by spray-drying. J. Appl. Microbiol. 112: 954-965.
Yen, T.T.O., Prasanna, B.M., Setty, T.A.S. and Rathore, R.S. (2004). Genetic variability for resistance to sorghum downy mildew (Peronosclerospora sorghi) and Rajasthan downy mildew (P. heteropogoni) in the tropical/sub-tropical Asian maize germplasm. Euphytica. 138: 23-31.
Zhao, P., Quan, C., Wang, Y., Wang, J. and Fan, S. (2014). Bacillus amyloliquefaciens Q-426 as a potential biocon-trol agent against Fusarium oxysporum f. sp. spinaciae. J. Basic Microbiol. 54: 448-456.
Anahosur, K. H. and Patil, S. H. (1980). Chemical control of sorghum downy mildew in India. Plant Dis. 64: 1004-1006.
Baki, A.A.A. and Anderson, J.D. (1973). Vigour determina-tion in soybean seed by multiple criteria. Crop Sci. 31: 630-633.
Beauregard, P.B., Chai, Y., Vlamakis, H., Losick, R. and Kolter, R. (2013). Bacillus subtilis biofilm induction by plant polysaccharides. Proc. Natl. Acad. Sci USA 110: 1621-1630.
Bock, C.H., Jeger, M.J., Mughogho, L.K., Cardwell, K.F., Mtisi, E., Kaula, G. and Mukansabimana, D. (2000). Variability of Peronosclerospora sorghi isolates from different geographic locations and hosts in Africa. My-col Res. 104: 61-68.
Bock, C.H., Jeger, M.J., Mughogho, L.K., Mtisi, E. and Cardwell, K.F. (1998). Production of conidia by Per-onosclerospora sorghi on sorghum crops in Zimbabwe. Plant Pathol. 47: 243-251.
Bonman, J.M., Renfro, B.L. and Singburaudom, N. (1983). Correlation between resistance in maize to local and systemic infection by Peronosclerospora sorghi in Thailand. Plant Dis. 67: 219-220.
Choudhary, D.K. and Johri, B.N. (2009). Interactions of Bacillus spp. and plants with special reference to in-duced systemic resistance (ISR). Microbiol. Res. 164: 493-513.
Cohen, Y. and Sherman, Y. (1977). The role of airborne conidia in epiphytotics of Sclerospora sorghi on sweet corn. Phytopathology 67: 515-521.
Craig, J. (1982). Identification of sorghum downy mildew resistance in corn by leaf reaction to conidial inoculum. Phytopathology 72: 351-352.
Earl, A.M., Losick, R. and Kolter, R. (2008). Ecology and genomics of Bacillus subtilis. Trends Microbiol. 16: 269-275.
Furuya, S., Mochizuki, M., Aoki, Y., Kobayashi, H., Takaya-nagi, T., Shimizu, M. and Suzuki, S. (2011). Isolation and characterization of Bacillus subtilis KS1 for the biocontrol of grapevine fungal diseases. Biocontrol Sci. Technol. 21: 705-720.
Gomez, K.A. and Gomez, A.A. (1984). Statistical procedure for agricultural research. New York, USA.
Guo, Q., Li, S., Lu, X., Zhang, X., Wang, P. and Ma, P. (2014). Complete genome sequence of Bacillus subtilis BAB-1, a biocontrol agent for suppression of tomato gray mold. Genome Announc. 2(4):e00744-14.
Hu, X., Roberts, D.P., Xie, L., Maul, J.E., Yu, C., Li, Y., Jiang, M., Liao, X., Che, Z. and Liao, X. (2014). For-mulations of Bacillus subtilis BY-2 suppress Sclerotinia sclerotiorum on oilseed rape in the field. Biol. Control 70: 54-64.
International Seed Testing Association. (1996). International Rules for Seed Testing. Seed Sci. Technol. Supp. 24: 155-202.
Isakeit, T. and Jaster, J. (2005). Texas has a new pathotype of Peronosclerospora sorghi, the cause of sorghum downy mildew. Plant Dis. 89: 529.
Jayaraj, J., Radhakrishnan, N.V., Kannan, R., Sakthivel, K., Suganya, D., Venkatesan, S. and Velazhahan, R. (2005). Development of new formulations of Bacillus subtilis for management of tomato damping-off caused by Pythium aphanidermatum. Biocontrol Sci. Technol. 15: 55-65.
Khabbaz, S.E. and Abbasi, P.A. (2014). Isolation, characteri-zation, and formulation of antagonistic bacteria for the management of seedlings damping-off and root rot disease of cucumber. Can. J. Microbiol. 60: 25-33.
King, E.O., Ward, M. K. and Raney, D. E. (1954). Two sim-ple media for the demonstration of pyocyanine and fluorescein. J. Lab. Clin. Med. 44: 301-307.
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.
Lahlali, R., Peng, G., Gossen, B.D., McGregor, L., Yu, F.Q., Hynes, R.K., Hwang, S.F., McDonald, M.R. and Boyetchko, S.M. (2013). Evidence that the biofungicide Serenade (Bacillus subtilis) suppresses clubroot on ca-nola via antibiosis and induced host resistance. Phyto-pathology 103: 245-254.
Liu, Y., Tao, J., Yan, Y., Li, B., Li, H. and Li, C. (2011). Biocontrol efficiency of Bacillus subtilis SL-13 and characterization of an antifungal chitinase. Chin. J. Chem. Eng. 19: 128-134.
Lukman, R., Afifuddin, A. and Lubberstedt, T. (2013). Un-raveling the genetic diversity of maize downy mildew in Indonesia. J. Plant Pathol. Microb. 4: 162.
Manjula, K. and Podile, A.R. (2005). Production of fungal cell wall degrading enzymes by a biocontrol strain of Bacillus subtilis AF1. Ind. J. Exp. Bot. 43: 892-896.
Mathiyazhagan, S., Karthikeyan, M., Sandosskumar, R. and Velazhahan, R. (2008). Analysis of variability among the isolates of Peronosclerospora sorghi from sorghum and corn based on restriction fragment length polymor-phism of ITS region of ribosomal DNA. Arch. Phytopa-thol. Plant Protect. 41: 231-237.
Meena, B., Marimuthu, T., Vidyasekaran, P. and Velazha-han, R. (2001). Biological control of root rot of ground-nut with antagonistic Pseudomonas fluorescens strains. J. Plant Dis. Protect. 108: 368-381.
Narayana, Y.D., Mughogho, L.K. and Bandyopadhyay, R. (1995). Evaluation of greenhouse inoculation tech-niques to screen sorghum for resistance to downy mil-dew. Euphytica 86: 49-53.
Ongena, M. and Jacques, P. (2008). Bacillus lipopeptides: versatile weapons for plant disease control. Trends Mi-crobiol 16: 115-125.
Perez-Garcia, A., Romero, D., De Vicente, A. (2011). Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotech. 22: 187-193.
Perumal, R., Isakeit, T., Menz, M., Katile, S., No, E.G. and Magill, C.W. (2006). Characterization and genetic dis-tance analysis of isolates of Peronosclerospora sorghi using AFLP fingerprinting. Mycol. Res. 110: 471-78.
Ramalingham, A. and Rajasab, A.H. (1981). Epidemiology of sorghum downy mildew. VI. Relative importance of oospores and conidia in epidemics of systemic infec-tion. Proc. Indian Nat. Sci. Acad. Part B 47: 625-630.
Rashid, Z., Zaidi, P. H., Vinavan, M. T., Sharma, S. S. and Srirama Setty, T. A. (2013). Downy mildew resistance in maize (Zea mays L.) across Peronosclerospora spe-cies in lowland tropical Asia. Crop Prot. 43: 183-191.
Sadoma, M.T, El-Sayed, A.B.B. and El-Moghazy, S.M. (2011). Biological control of downy mildew disease of maize caused by Peronosclerospora sorghi using cer-tain biocontrol agents alone or in combination. J. Agric. Res. Kafer El-Sheikh Univ. 37 (1): 1-11.
Schisler, D.A., Slininger, P.J., Behle, R.W. and Jackson, M.A. (2004). Formulation of Bacillus spp. for biological control of plant diseases. Phytopathology 94: 1267-1271.
Shifa. H., Gopalakrishnan, C. and Velazhahan R. (2015a). Efficacy of Bacillus subtilis G-1 in suppression of stem rot caused by Sclerotium Rolfsii and growth promotion of groundnut. International Journal of Agriculture, Environment and Biotechnology. 8(1): 111-118.
Shifa. H., Gopalakrishnan, C. and Velazhahan R. (2015b). Characterisation of antifungal antibiotics produced by Bacillus subtilis G-1 antagonistic to Sclerotium rolfsii. Biochem. Cell. Archives. 15(1): 99-104.
Sireesha, Y. and Velazhahan, R. (2015). Assessing genetic diversity in Peronosclerospora sorghi causing downy mildew on maize and sorghum. Indian Phytopath. 68 (1): 73-77.
Sivasakthi, S., Usharani, G. and Saranraj, P. (2014). Biocon-trol potentiality of plant growth promoting bacteria (PGPR)- Pseudomonas fluorescens and Bacillus sub-tilis: A review. African J. Agric. Res. 9: 1265-1277.
Stein, T. (2005). Bacillus subtilis antibiotics: structures, synthe-ses and specific functions. Mol. Microbiol. 56: 845-857.
Thompson, D.C. (1996). Evaluation of bacterial antagonist for reduction of summer patch symptoms in Kentucky blue grass. Plant Dis. 80: 856-862.
Vidhyasekaran, P. and Muthamilan, M. (1995). Development of formulations of Pseudomonas fluorescens for control of chickpea wilt. Plant Dis. 79: 782-786.
Yanez-Mendizabal, V., Vinas, I., Usall, J., Torres, R., Sol-sona, C., Abadias, M. and Teixido, N. (2012). Formula-tion development of the biocontrol agent Bacillus subtilis strain CPA-8 by spray-drying. J. Appl. Microbiol. 112: 954-965.
Yen, T.T.O., Prasanna, B.M., Setty, T.A.S. and Rathore, R.S. (2004). Genetic variability for resistance to sorghum downy mildew (Peronosclerospora sorghi) and Rajasthan downy mildew (P. heteropogoni) in the tropical/sub-tropical Asian maize germplasm. Euphytica. 138: 23-31.
Zhao, P., Quan, C., Wang, Y., Wang, J. and Fan, S. (2014). Bacillus amyloliquefaciens Q-426 as a potential biocon-trol agent against Fusarium oxysporum f. sp. spinaciae. J. Basic Microbiol. 54: 448-456.
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Biological control of downy mildew of maize caused by Peronosclerospora sorghi under environmentally controlled conditions. (2016). Journal of Applied and Natural Science, 8(1), 279-283. https://doi.org/10.31018/jans.v8i1.786
