Rhizosphere Streptomyces formulas as the biological control agent of phytopathogenic fungi Fusarium oxysporum and plant growth promoter of soybean
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Abstract. Sari M, Nawangsih AA, Wahyudi AT. 2021. Rhizosphere Streptomyces formulas as the biological control agent of phytopathogenic fungi Fusarium oxysporum and plant growth promoter of soybean. Biodiversitas 22: 3015-3023. Rhizosphere Streptomyces are considered as promising sources of plant growth-promoting rhizobacteria (PGPR) and biocontrol agents against pathogenic fungi, particularly Fusarium oxysporum causing root rot, cotyledon rot, hypocotyl rot, and stunted growth in soybean. Formulation of rhizosphere Streptomyces with appropriate carrier materials is necessary to facilitate storage and application in plants. This study aimed to develop a formulation of rhizosphere Streptomyces, apply the formula to control F. oxysporum, and promote soybean plant growth. Five Streptomyces isolates, i.e., Streptomyces panaciradicis ARK 13, Streptomyces tritolerans ARK 17, Streptomyces recifensis ARK 63, Streptomyces tendae ARK 91, and Streptomyces manipurensis ARK 94 were used in this study. All of the isolates could grow in potato broth, rice bran extract, and molasses as alternative media. The highest biomass produced from the molasses growth medium. All five isolates had antifungal activity against F. oxysporum with the inhibition percentage ranging from 41% to 76%, and all of them were detected to have the iaaM gene. Indole-3-acetic acid (IAA) hormone produced by these isolates were ranging from 8.99-15.14 mg L-1, with the phosphate solubilization index of 2.13-2.47. Five rhizosphere Streptomyces formulas with the main carrier of peat could maintain the viability with the population density of 108 CFU g-1 for 8 weeks of storage at room temperature. Two formulas, F17 and F94, were the best formulas to control disease caused by F. oxysporum with disease suppression of 74% in sterile soil and 80-85% in non-sterile soil. Formula F17 and F94 significantly increased soybean growth in sterile and non-sterile soils. Therefore, these formulas could be recommended as biocontrol and plant growth promoters of soybean.
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References
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Arias MMD, Leandro LF, Munkvold GP. 2013. Aggressiveness of Fusarium species and impact of root infection on growth and yield of soybeans. Ecol Epidemiol 8(103): 822-832. https://doi.org/10.1094/phyto-08-12-0207-r.
Arias MMD, Munkvold GP, Ellis ML, Leandro LES. 2013. Distribution and frequency of Fusarium species associated with soybean roots in Iowa. Plant Dis 97: 1157-1562. https://doi.org/10.1094/PDIS-11-12-1059-RE.
Arora NK, Mishra J. 2016. Prospecting the roles of metabolites and additives in future bioformulations for sustainable agriculture. Appl Soil Ecol 107:405-407. https://doi.org/10.1016/j.apsoil.2016.05.020.
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, Clément C, Ouhdouch Y, Wezel GP. 2016. Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 80: 1-43. https://doi.org/10.1128/MMBR.00019-15.
Basso LC, Basso TO, Rocha SN. 2011. Ethanol production in Brazil: the industrial process and its impact on yeast fermentation. Biofuel Prod-Rec Dev Pros 1530: 85-100. https://doi.org/10.5772/17047.
Bhosle HJ, Kadam TA, Mirajgave RS, Holkar SK. 2018. Optimization and characterization of antifungal metabolite from a soil actinomycete Streptomyces indiaensis SRT. Indian J Biotechnol 17(2): 261-271.
Casteriano A, Wilkes MA, Deaker R. 2013. Physiological changes in rhizobia after growth in peat extract may be related to improved desiccation tolerance. Appl and Environ Microbiol 79(13): 3998-4007. https://doi.org/10.1128/AEM.00082-13.
Cui J, Wang Y, Han J, Cai B. 2016. Analyses of the community compositions of root rot pathogenic fungi in the soybean rhizosphere soil. Chil J Agr Res 76(2): 179-187. https://doi.org/10.4067/S0718-58392016000200007.
Duan Y, Chen J, He W, Chen J, Pang Z, Hu H, Xie J. 2020. Fermentation optimization and disease suppression ability of a Streptomyces ma. FS-4 from banana rhizosphere soil. BMC Microbiol 20(24): 1-12. https://doi.org/10.1186/s12866-019-1688-z.
Ellis ML, Arias MMD, Jimenez DRC, Munkvold GP, Leandro LF. 2013. First report of Fusarium commune causing damping-off, seed rot, and seedling root rot on soybean (Glycine max) in the United States. Plant Dis 97(2): 284. https://doi.org/10.1094/PDIS-07-12-0644-PDN.
Farried, Al-Shaimaa M, Mohamed HM, El-Dsouky, El-Rewainy HM. 2018. Isolation and characterization of phosphate solubilizing actinomycetes from rhizosphere soil. Assiut J Agric Sci 49(4): 125-137.
Glick BR. 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica 1-15. https://doi.org/10.6064/2012/963401.
Gopalakrishnan S, Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, Vidya MS, Deepthi K, Rupela O. 2011. Evaluation of actinomycete isolates obtained from herbal vermicompost for the biological control of Fusarium wilt of chickpea. Crop Prot 30(8): 1070-1078. https://doi.org/10.1016/j.cropro.2011.03.006.
Gopalakrishnan S, Sathya A, Vijayabharathi R, Srinivas V. 2016. Formulation of plant growth-promoting microbes for field applications. Microb Inocul Sustain Agric Produc 15: 239-251. https://doi.org/10.1007/978-81-322-2644-4_15.
Husnain SK, Khan SB, Atiq M, Rajput NA, Abbas W, Mohsin M. 2019. Screening of peas (Pisum sativum) varieties/ lines against fusarium wilt (Fusarium oxysporum f. sp. Pisi) and in vitro evaluation of fungicides against mycelial growth of pathogen. Pak J Phtopathol 31(1): 89-96. https://doi.org/10.33866/phytopathol.031.01.0492.
Jog R, Pandya M, Narshkumar G, Rajkumar S. 2014. Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160: 778-788. https://doi.org/10.1099/mic.0.074146-0.
Khabbaz SE, Abbasi PA. 2014. Isolation, characterization, and formulation of antagonistic bacteria for the management of seedlings damping-off and root rot disease of cucumber. Can J Microbiol 60(1): 25-33. https://doi.org/10.1139/cjm-2013-0675.
Khalil MS, Moubasher H, Hasan FF. 2014. Biological control of rice blast disease by Streptomyces flavotricini. Res J Pharm Biol Chem Sci 5: 1453-1461.
Khamna S, Yokota A, Peberdy JF, Lumyong S. 2010. Indole-3-acetic acid production by Streptomyces sp. isolated from Thai medicinal plant rhizosphere soils. EurAsia J BioSci 4: 23-32. https://doi.org/10.5053/ejobios.2010.4.0.4.
Khare A, Singh BK, Upadhyay RS. 2010. Biological control of Pythium aphanidermatum causing damping-off of mustard by mutants of Trichoderma viridae 1433. J Agric Technol 6: 231-243.
Lin L, Xu X. 2013. Indole-3-acetic acid production by endophytic Sreptomyces sp. En-1 isolated from medical plants. Curr Microbiol. 67: 209-217. https://doi.org/10.1007/s00284-013-0348-z.
Maier M, Souza CA, Casa RT. 2018. Cropping systems on root rot and soybean seed yield. Ciência Rural 48(7): 1-8. https://doi.org/10.1590/0103-8478cr20170460.
Mariastuti HD, Listiyowati S, Wahyudi AT. 2018. Antifungal activity of soybean rhizosphere actinomycetes producing bioactive compounds against Fusarium oxysporum. Biodiversitas 19(6): 2127-2133. https://doi.org/10.13057/biodiv/d190619.
Myo EM, Ge B, Ma J, Cui H, Liu B, Shi L, Jiang M, Zhang K. 2019. Indole-3-acetic acid production by Streptomyces fradiae NKZ-259 and its formulation to enhance plant growth. BMC Microbiol 19(155): 1-14.
Olanrewaju OS, Babalola OO. 2019. Streptomyces: implications and interactions in plant growth promotion. Appl Microbiol Biotechnol 103: 1179-1188. https://doi.org/10.1007/s00253-018-09577-y.
Passari AK, Chandra P, Zothanpuia, Mishra VK, Leo VV, Gupta VK, Kumar B, Singh BP. 2016. Detection of biosynthetic gene and phytohormone production by endophytic actinobacteria associated with Solanum lycopersicum and their plant-growth-promoting effect. Res Microbiol 167(8): 692-705. https://doi.org/10.1016/j.resmic.2016.07.001.
Rajeswari P. 2015. Control of Fusarium oxysporum causing fusarium wilt by Trichoderma spp and Pseudomonas fluorescens on Arachis hypogaea L. Int J Adv Biotechnol Res 6: 57-65.
Rashad, Younes, Al-Askar, Abdulaziz, Ghoneem, Khalid, Ali S, Wesameldin, Hafez, Elsayed. 2017. Chitinolytic Streptomyces griseorubens E44G enhances the biocontrol efficacy against Fusarium wilt disease of tomato. Phytoparasitica 45(2): 227-237. https://doi.org/10.1007/s12600-017-0580-3.
Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H. 2012. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28: 1503-1509. https://doi.org/10.1007/s11274-011-0952-7.
Saurav K, Kannabiran K. 2010. Diversity and optimization of process parameters for the growth of Streptomyces VITSVK9 spp. isolated from Bay of Bengal, India. J Nat Env Sci 1(2): 56-65.
Sousa JADJ, Olivares FL. 2016. Plant growth promotion by Streptomycetes: Ecophysiology, mechanisms and applications. Chem and Biol Technol Agric 3(24): 1-12. https://doi.org/10.1186/s40538-016-0073-5.
Tamreihao K, Ningthoujam DS, Nimaichand S, Singh ES, Reena P, Singh SH, Nongthomba U. 2016. Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbioll Res 192: 260-270. https://doi.org/10.1016/j.micres.2016.08.005.
Wahyudi AT, Priyanto JA, Afrista R, Kurniati D, Astuti RI, Akhdiya A. 2019. Plant growth promoting activity of actinomycetes isolated from soybean rhizosphere. OnLine J Biol Sci 19(1): 1-8. https://doi.org/10.3844/ojbsci.2019.1.8.
Zacky FA, Ting ASY. 2015. Biocontrol of Fusarium oxysporum f.sp. cubense tropical race 4 by formulated cells and cell-free extracts of Streptomyces griseus in sterile soil environment. Biocontrol Sci Technol 25(6): 685-696. https://doi.org/10.1080/09583157.2015.1007921.
Zhang P, Jin T, Kumar Sahu S, Xu J, Shi Q, Liu H, Wang Y. 2019. The distribution of tryptophan-dependent indole-3-acetic acid synthesis pathways in bacteria unraveled by large-scale genomic analysis. Molecules 24(7): 1-14. https://doi.org/10.3390/molecules2407141.
Al-Askar AA, Abdulaziz KMW, Rashad YM. 2011. In vitro antifungal activity of Streptomyces spororaveus RDS28 against some phytopathogenic fungi. Afri J Agri Res 6(12): 2835-2842.
Arias MMD, Leandro LF, Munkvold GP. 2013. Aggressiveness of Fusarium species and impact of root infection on growth and yield of soybeans. Ecol Epidemiol 8(103): 822-832. https://doi.org/10.1094/phyto-08-12-0207-r.
Arias MMD, Munkvold GP, Ellis ML, Leandro LES. 2013. Distribution and frequency of Fusarium species associated with soybean roots in Iowa. Plant Dis 97: 1157-1562. https://doi.org/10.1094/PDIS-11-12-1059-RE.
Arora NK, Mishra J. 2016. Prospecting the roles of metabolites and additives in future bioformulations for sustainable agriculture. Appl Soil Ecol 107:405-407. https://doi.org/10.1016/j.apsoil.2016.05.020.
Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, Clément C, Ouhdouch Y, Wezel GP. 2016. Taxonomy, physiology, and natural products of actinobacteria. Microbiol Mol Biol Rev 80: 1-43. https://doi.org/10.1128/MMBR.00019-15.
Basso LC, Basso TO, Rocha SN. 2011. Ethanol production in Brazil: the industrial process and its impact on yeast fermentation. Biofuel Prod-Rec Dev Pros 1530: 85-100. https://doi.org/10.5772/17047.
Bhosle HJ, Kadam TA, Mirajgave RS, Holkar SK. 2018. Optimization and characterization of antifungal metabolite from a soil actinomycete Streptomyces indiaensis SRT. Indian J Biotechnol 17(2): 261-271.
Casteriano A, Wilkes MA, Deaker R. 2013. Physiological changes in rhizobia after growth in peat extract may be related to improved desiccation tolerance. Appl and Environ Microbiol 79(13): 3998-4007. https://doi.org/10.1128/AEM.00082-13.
Cui J, Wang Y, Han J, Cai B. 2016. Analyses of the community compositions of root rot pathogenic fungi in the soybean rhizosphere soil. Chil J Agr Res 76(2): 179-187. https://doi.org/10.4067/S0718-58392016000200007.
Duan Y, Chen J, He W, Chen J, Pang Z, Hu H, Xie J. 2020. Fermentation optimization and disease suppression ability of a Streptomyces ma. FS-4 from banana rhizosphere soil. BMC Microbiol 20(24): 1-12. https://doi.org/10.1186/s12866-019-1688-z.
Ellis ML, Arias MMD, Jimenez DRC, Munkvold GP, Leandro LF. 2013. First report of Fusarium commune causing damping-off, seed rot, and seedling root rot on soybean (Glycine max) in the United States. Plant Dis 97(2): 284. https://doi.org/10.1094/PDIS-07-12-0644-PDN.
Farried, Al-Shaimaa M, Mohamed HM, El-Dsouky, El-Rewainy HM. 2018. Isolation and characterization of phosphate solubilizing actinomycetes from rhizosphere soil. Assiut J Agric Sci 49(4): 125-137.
Glick BR. 2012. Plant growth-promoting bacteria: mechanisms and applications. Scientifica 1-15. https://doi.org/10.6064/2012/963401.
Gopalakrishnan S, Pande S, Sharma M, Humayun P, Kiran BK, Sandeep D, Vidya MS, Deepthi K, Rupela O. 2011. Evaluation of actinomycete isolates obtained from herbal vermicompost for the biological control of Fusarium wilt of chickpea. Crop Prot 30(8): 1070-1078. https://doi.org/10.1016/j.cropro.2011.03.006.
Gopalakrishnan S, Sathya A, Vijayabharathi R, Srinivas V. 2016. Formulation of plant growth-promoting microbes for field applications. Microb Inocul Sustain Agric Produc 15: 239-251. https://doi.org/10.1007/978-81-322-2644-4_15.
Husnain SK, Khan SB, Atiq M, Rajput NA, Abbas W, Mohsin M. 2019. Screening of peas (Pisum sativum) varieties/ lines against fusarium wilt (Fusarium oxysporum f. sp. Pisi) and in vitro evaluation of fungicides against mycelial growth of pathogen. Pak J Phtopathol 31(1): 89-96. https://doi.org/10.33866/phytopathol.031.01.0492.
Jog R, Pandya M, Narshkumar G, Rajkumar S. 2014. Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160: 778-788. https://doi.org/10.1099/mic.0.074146-0.
Khabbaz SE, Abbasi PA. 2014. Isolation, characterization, and formulation of antagonistic bacteria for the management of seedlings damping-off and root rot disease of cucumber. Can J Microbiol 60(1): 25-33. https://doi.org/10.1139/cjm-2013-0675.
Khalil MS, Moubasher H, Hasan FF. 2014. Biological control of rice blast disease by Streptomyces flavotricini. Res J Pharm Biol Chem Sci 5: 1453-1461.
Khamna S, Yokota A, Peberdy JF, Lumyong S. 2010. Indole-3-acetic acid production by Streptomyces sp. isolated from Thai medicinal plant rhizosphere soils. EurAsia J BioSci 4: 23-32. https://doi.org/10.5053/ejobios.2010.4.0.4.
Khare A, Singh BK, Upadhyay RS. 2010. Biological control of Pythium aphanidermatum causing damping-off of mustard by mutants of Trichoderma viridae 1433. J Agric Technol 6: 231-243.
Lin L, Xu X. 2013. Indole-3-acetic acid production by endophytic Sreptomyces sp. En-1 isolated from medical plants. Curr Microbiol. 67: 209-217. https://doi.org/10.1007/s00284-013-0348-z.
Maier M, Souza CA, Casa RT. 2018. Cropping systems on root rot and soybean seed yield. Ciência Rural 48(7): 1-8. https://doi.org/10.1590/0103-8478cr20170460.
Mariastuti HD, Listiyowati S, Wahyudi AT. 2018. Antifungal activity of soybean rhizosphere actinomycetes producing bioactive compounds against Fusarium oxysporum. Biodiversitas 19(6): 2127-2133. https://doi.org/10.13057/biodiv/d190619.
Myo EM, Ge B, Ma J, Cui H, Liu B, Shi L, Jiang M, Zhang K. 2019. Indole-3-acetic acid production by Streptomyces fradiae NKZ-259 and its formulation to enhance plant growth. BMC Microbiol 19(155): 1-14.
Olanrewaju OS, Babalola OO. 2019. Streptomyces: implications and interactions in plant growth promotion. Appl Microbiol Biotechnol 103: 1179-1188. https://doi.org/10.1007/s00253-018-09577-y.
Passari AK, Chandra P, Zothanpuia, Mishra VK, Leo VV, Gupta VK, Kumar B, Singh BP. 2016. Detection of biosynthetic gene and phytohormone production by endophytic actinobacteria associated with Solanum lycopersicum and their plant-growth-promoting effect. Res Microbiol 167(8): 692-705. https://doi.org/10.1016/j.resmic.2016.07.001.
Rajeswari P. 2015. Control of Fusarium oxysporum causing fusarium wilt by Trichoderma spp and Pseudomonas fluorescens on Arachis hypogaea L. Int J Adv Biotechnol Res 6: 57-65.
Rashad, Younes, Al-Askar, Abdulaziz, Ghoneem, Khalid, Ali S, Wesameldin, Hafez, Elsayed. 2017. Chitinolytic Streptomyces griseorubens E44G enhances the biocontrol efficacy against Fusarium wilt disease of tomato. Phytoparasitica 45(2): 227-237. https://doi.org/10.1007/s12600-017-0580-3.
Sadeghi A, Karimi E, Dahaji PA, Javid MG, Dalvand Y, Askari H. 2012. Plant growth promoting activity of an auxin and siderophore producing isolate of Streptomyces under saline soil conditions. World J Microbiol Biotechnol 28: 1503-1509. https://doi.org/10.1007/s11274-011-0952-7.
Saurav K, Kannabiran K. 2010. Diversity and optimization of process parameters for the growth of Streptomyces VITSVK9 spp. isolated from Bay of Bengal, India. J Nat Env Sci 1(2): 56-65.
Sousa JADJ, Olivares FL. 2016. Plant growth promotion by Streptomycetes: Ecophysiology, mechanisms and applications. Chem and Biol Technol Agric 3(24): 1-12. https://doi.org/10.1186/s40538-016-0073-5.
Tamreihao K, Ningthoujam DS, Nimaichand S, Singh ES, Reena P, Singh SH, Nongthomba U. 2016. Biocontrol and plant growth promoting activities of a Streptomyces corchorusii strain UCR3-16 and preparation of powder formulation for application as biofertilizer agents for rice plant. Microbioll Res 192: 260-270. https://doi.org/10.1016/j.micres.2016.08.005.
Wahyudi AT, Priyanto JA, Afrista R, Kurniati D, Astuti RI, Akhdiya A. 2019. Plant growth promoting activity of actinomycetes isolated from soybean rhizosphere. OnLine J Biol Sci 19(1): 1-8. https://doi.org/10.3844/ojbsci.2019.1.8.
Zacky FA, Ting ASY. 2015. Biocontrol of Fusarium oxysporum f.sp. cubense tropical race 4 by formulated cells and cell-free extracts of Streptomyces griseus in sterile soil environment. Biocontrol Sci Technol 25(6): 685-696. https://doi.org/10.1080/09583157.2015.1007921.
Zhang P, Jin T, Kumar Sahu S, Xu J, Shi Q, Liu H, Wang Y. 2019. The distribution of tryptophan-dependent indole-3-acetic acid synthesis pathways in bacteria unraveled by large-scale genomic analysis. Molecules 24(7): 1-14. https://doi.org/10.3390/molecules2407141.
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