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Evaluation of Soil Streptomyces spp. for the Biological Control of Fusarium Wilt Disease and Growth Promotion in Tomato and Banana

  • Praphat, Kawicha (Plant Pest and Biocontrol Research Unit, Department of Agriculture and Resources, Faculty of Natural Resources and Agro-Industry, Kasetsart University Chalermphrakiat Sakon Nakhon Province Campus) ;
  • Jariya, Nitayaros (Plant Pest and Biocontrol Research Unit, Department of Agriculture and Resources, Faculty of Natural Resources and Agro-Industry, Kasetsart University Chalermphrakiat Sakon Nakhon Province Campus) ;
  • Prakob, Saman (Plant Pest and Biocontrol Research Unit, Department of Agriculture and Resources, Faculty of Natural Resources and Agro-Industry, Kasetsart University Chalermphrakiat Sakon Nakhon Province Campus) ;
  • Sirikanya, Thaporn (Department of Biology, Faculty of Science, Mahasarakham University) ;
  • Thanwanit, Thanyasiriwat (Plant Pest and Biocontrol Research Unit, Department of Agriculture and Resources, Faculty of Natural Resources and Agro-Industry, Kasetsart University Chalermphrakiat Sakon Nakhon Province Campus) ;
  • Khanitta, Somtrakoon (Department of Biology, Faculty of Science, Mahasarakham University) ;
  • Kusavadee, Sangdee (Preclinical Group, Faculty of Medicine, Mahasarakham University) ;
  • Aphidech, Sangdee (Department of Biology, Faculty of Science, Mahasarakham University)
  • Received : 2022.08.28
  • Accepted : 2022.12.29
  • Published : 2023.02.01

Abstract

Fusarium oxysporum f. sp. lycopersici (Fol) and Fusarium oxysporum f. sp. cubense (Foc), are the causal agent of Fusarium wilt disease of tomato and banana, respectively, and cause significant yield losses worldwide. A cost-effective measure, such as biological control agents, was used as an alternative method to control these pathogens. Therefore, in this study, six isolates of the Streptomyces-like colony were isolated from soils and their antagonistic activity against phytopathogenic fungi and plant growth-promoting (PGP) activity were assessed. The results showed that these isolates could inhibit the mycelial growth of Fol and Foc. Among them, isolate STRM304 showed the highest percentage of mycelial growth reduction and broad-spectrum antagonistic activity against all tested fungi. In the pot experiment study, the culture filtrate of isolates STRM103 and STRM104 significantly decreased disease severity and symptoms in Fol inoculated plants. Similarly, the culture filtrate of the STRM304 isolate significantly reduced the severity of the disease and symptoms of the disease in Foc inoculated plants. The PGP activity test presents PGP activities, such as indole acetic acid production, phosphate solubilization, starch hydrolysis, lignin hydrolysis, and cellulase activity. Interestingly, the application of the culture filtrate from all isolates increased the percentage of tomato seed germination and stimulated the growth of tomato plants and banana seedlings, increasing the elongation of the shoot and the root and shoot and root weight compared to the control treatment. Therefore, the isolate STRM103 and STRM104, and STRM304 could be used as biocontrol and PGP agents for tomato and banana, respectively, in sustainable agriculture.

Keywords

Acknowledgement

This research project was financially supported by Mahasarakham University (MSU). The authors also thank the Department of Agriculture and Resources, Faculty of Natural Resources and Agro-Industry, Kasetsart University Chalermphrakiat Sakon Nakhon Province Campus, and Mahasarakham University, Faculty of Science for supporting equipment and space for this study.

References

  1. Al-Askar, A. A., Abdul Khair, W. M. and Rashad, Y. M. 2011. In vitro antifungal activity of Streptomyces spororaveus RDS28 against some phytopathogenic fungi. Afr. J. Agric. Res. 6:2835-2842.
  2. Al-Askar, A. A., Rashad, Y. M. and Abdulkhair, W. M. 2013. Antagonistic activity of an endemic isolate of Streptomyces tendae RDS16 against phytopathogenic fungi. Afr. J. Microbiol. Res. 7:509-516.
  3. Alijani, Z., Amini, J., Ashengroph, M. and Bahramnejad, B. 2019. Antifungal activity of volatile compounds produced by Staphylococcus sciuri strain MarR44 and its potential for the biocontrol of Colletotrichum nymphaeae, causal agent strawberry anthracnose. Int. J. Food Microbiol. 307:108276.
  4. Ambrico, A. and Trupo, M. 2017. Efficacy of cell free supernatant from Bacillus subtilis ET-1, an Iturin A producer strain, on biocontrol of green and gray mold. Postharvest Biol. Technol. 134:5-10. https://doi.org/10.1016/j.postharvbio.2017.08.001
  5. Amini, J. and Sidovich, D. F. 2010. The effects of fungicides on Fusarium oxysporum f. sp. lycopersici associated with Fusarium wilt of tomato. J. Plant Prot. Res. 50:172-178.
  6. Arcury, T. A. and Quandt, S. A. 2003. Pesticides at work and at home: exposure of migrant farm workers. Lancet 362:2021. https://doi.org/10.1016/S0140-6736(03)14387-5
  7. Bano, N. and Musarrat, J. 2003. Characterization of a new Pseudomonas aeruginosa strain NJ-15 as a potential biocontrol agent. Curr. Microbiol. 46:324-328. https://doi.org/10.1007/s00284-002-3857-8
  8. Basak, B. B. and Biswas, D. R. 2009. Influence of potassium solubilizing microorganisms (Bacillus mucilaginous) and waste mica on potassium uptake dynamics by sudan grass (Sorghum vulgare Pers.) grown under two Alfisols. Plant Soil 317:235-255. https://doi.org/10.1007/s11104-008-9805-z
  9. Bauer, J. S., Hauck, N., Christof, L., Mehnaz, S., Gust, B. and Gross, H. 2016. The systematic investigation of the quorum sensing system of the biocontrol strain Pseudomonas chlororaphis subsp. aurantiaca PB-St2 unveils aurI to be a biosynthetic origin for 3-oxo-homoserine lactones. PLoS ONE 11:e0167002.
  10. Ben Abdallah, D., Tounsi, S., Gharsallah, H., Hammami, A. and Frikha-Gargouri, O. 2018. Lipopeptides from Bacillus amyloliquefaciens strain 32a as promising biocontrol compounds against the plant pathogen Agrobacterium tumefaciens. Environ. Sci. Pollut. Res. 25:36518-36529. https://doi.org/10.1007/s11356-018-3570-1
  11. Bertram, R., Schlicht, M., Mahr, K., Nothaft, H., Saier, M. H. Jr. and Titgemeyer, F. 2004. In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J. Bacteriol. 186:1362-1373. https://doi.org/10.1128/JB.186.5.1362-1373.2004
  12. Bhai, R. S., Lijina, A., Prameela, T. P., Krishna, P. B. and Thampi, A. 2016. Biocontrol and growth promotive potential of Streptomyces spp. in black pepper (Piper nigrum L.). J. Biol. Control 30:177-189. https://doi.org/10.18311/jbc/2016/15592
  13. Bressan, W. and Figueiredo, J. E. F. 2008. Efficacy and dose-response relationship in biocontrol of Fusarium disease in maize by Streptomyces spp. Eur. J. Plant Pathol. 120:311-316. https://doi.org/10.1007/s10658-007-9220-y
  14. Chater, K. F., Biro, S., Lee, K. J., Palmer, T. and Schrempf, H. 2010. The complex extracellular biology of Streptomyces. FEMS Microbiol. Rev. 34:171-198. https://doi.org/10.1111/j.1574-6976.2009.00206.x
  15. Chen, A., Sun, J., Matthews, A., Armas-Egas, L., Chen, N., Hamill, S., Mintoff, S., Tran-Nguyen, L. T. T., Batley, J. and Aitken, E. A. B. 2019. Assessing variations in host resistance to Fusarium oxysporum f. sp. cubense race 4 in Musa species, with a focus on the subtropical race 4. Front. Microbiol. 10:1062.
  16. Cross, T. 1989. Growth and examination of Actinomycetes some guidelines. In: Bergey's manual of systematic bacteriology, eds. by S. T. Williams, M. E. Sharpe and J. G. Holt, Vol. 4, pp. 2340-2343. Williams and Wilkins Company, Baltimore, MD, USA.
  17. de Lima Procopio, R. E., da Silva, I. R., Martins, M. K., de Azevedo, J. L. and de Araujo, J. M. 2012. Antibiotics produced by Streptomyces. Braz. J. Infect. Dis. 16:466-471. https://doi.org/10.1016/j.bjid.2012.08.014
  18. Dias, M. P., Bastos, M. S., Xavier, V. B., Cassel, E., Astarita, L. V. and Santarem, E. R. 2017. Plant growth and resistance promoted by Streptomyces spp. in tomato. Plant Physiol. Biochem. 118:479-493. https://doi.org/10.1016/j.plaphy.2017.07.017
  19. Duan, Y., Chen, J., He, W., Chen, J., Pang, Z., Hu, H. and Xie, J. 2020. Fermentation optimization and disease suppression ability of a Streptomyces ma. FS-4 from banana rhizosphere soil. BMC Microbiol. 20:24.
  20. El-Tarabily, K. A., Nassar, A. H., Hardy, G. E. S. J. and Sivasithamparam, K. 2009. Plant growth promotion and biological control of Pythium aphanidermatum, a pathogen of cucumber, by endophytic actinomycetes. J. Appl. Microbiol. 106:13-26. https://doi.org/10.1111/j.1365-2672.2008.03926.x
  21. El-Tarabily, K. A. and Sivasithamparam, K. 2006. Non-streptomycete actinomycetes as biocontrol agents of soilborne fungal plant pathogens and as plant growth promoters. Soil Biol Biochem. 38:1505-1520. https://doi.org/10.1016/j.soilbio.2005.12.017
  22. Ezziyyani, M., Requena, M. E., Egea-Gilabert, C. and Candela, M. E. 2007. Biological control of Phytophthora root rot of pepper using Trichoderma harzianum and Streptomyces rochei in combination. J. Phytopathol. 155:342-349. https://doi.org/10.1111/j.1439-0434.2007.01237.x
  23. Ghorbel, S., Kammoun, M., Soltana, H., Nasri, M. and Hmidet, N. 2014. Streptomyces flavogriseus HS1: isolation and characterization of extracellular proteases and their compatibility with laundry detergents. Biomed. Res. Int. 2014:345980.
  24. Hamdali, H., Hafidi, M., Virolle, M. J. and Ouhdouch, Y. 2008. Growth promotion and protection against damping-off of wheat by two rock phosphate solubilizing actinomycetes in a P-deficient soil under greenhouse conditions. Appl. Soil Ecol. 40:510-517. https://doi.org/10.1016/j.apsoil.2008.08.001
  25. Hao, D., Gao, P., Liu, P., Zhao, J., Wang, Y., Yang, W., Lu, Y., Shi, T. and Zhang, X. 2011. AC3-33 a novel secretory protein, inhibits Elk1 transcriptional activity via ERK pathway. Mol. Biol. Rep. 38:1375-1382. https://doi.org/10.1007/s11033-010-0240-x
  26. Kanini, G. S., Katsifas, E. A., Savvides, A. L., Hatzinikolaou, D. G. and Karagouni, A. D. 2013a. Greek indigenous streptomycetes as biocontrol agents against the soil-borne fungal plant pathogen Rhizoctonia solani. J. Appl. Microbiol. 114:1468-1479. https://doi.org/10.1111/jam.12138
  27. Kanini, G. S., Katsifas, E. A., Savvides, A. L. and Karagouni, A. D. 2013b. Streptomyces rochei ACTA1551, an indigenous Greek isolate studied as a potential biocontrol agent against Fusarium oxysporum f. sp. lycopersici. Biomed. Res. Int. 2013:387230.
  28. Kawicha, P., Laopha, A., Chamnansing, W., Sopawed, W., Wongcharone, A. and Sangdee, A. 2020. Biocontrol and plant growth-promoting properties of Streptomyces isolated from vermicompost soil. Indian Phytopathol. 73:655-666. https://doi.org/10.1007/s42360-020-00267-2
  29. Keikha, N., Mousavi, S. A. A., Nakhaei, A. R., Yadegari, M. H., Bonjar, G. H. S. and Amiri, S. 2015. In vitro evaluation of enzymatic and antifungal activities of soil-Actinomycetes isolates and their molecular identification by PCR. Jundishapur J. Microbiol. 8:e14874.
  30. Khamna, S., Yokota, A., Peberdy, J. F. and Lumyong, S. 2010. Indole-3-acetic acid production by Streptomyces sp. isolated from some Thai medicinal plant rhizosphere soils. EurAsian J. Biolsci. 4:23-32.
  31. Kirankumar, R., Jagadeesh, K. S., Krishnaraj, P. U. and Patil, M. S. 2008. Enhanced growth promotion of tomato and nutrient uptake by plant growth promoting rhizobacterial isolates in presence of tobacco mosaic virus pathogen. Karnataka J. Agric. Sci. 21:309-311.
  32. Ling, L., Han, X., Li, X., Zhang, X., Wang, H., Zhang, L., Cao, P., Wu, Y., Wang, X., Zhao, J. and Xiang, W. 2020. A Streptomyces sp. NEAU-HV9: isolation, identification, and potential as a biocontrol agent against Ralstonia solanacearum of tomato plants. Microorganisms 8:351.
  33. Liu, G., Chater, K. F., Chandra, G., Niu, G. and Tan, H. 2013. Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol. Mol. Biol. Rev. 77:112-143. https://doi.org/10.1128/MMBR.00054-12
  34. Marois, J. J. 1990. Biological control of diseases caused by Fusarium oxysporum. In: Fusarium wilt of banana, ed. by R. C. Ploetz, pp. 77-81. APS Press, St. Paul, MN, USA.
  35. McGovern, R. J. 2015. Management of tomato diseases caused by Fusarium oxysporum. Crop Prot. 73:78-92. https://doi.org/10.1016/j.cropro.2015.02.021
  36. Mintoff, S. J. L., Nguyen, T. V., Kelly, C., Cullen, S., Hearnden, M., Williams, R., Daniells, J. W. and Tran-Nguyen, L. T. T. 2021. Banana cultivar field screening for resistance to Fusarium oxysporum f. sp. cubense tropical race 4 in the Northern Territory. J. Fungi 7:627.
  37. Moore, N. Y., Pegg, K. G., Bentley, S. and Smith, L. J. 2001. Fusarium wilt of banana: global problems and perspectives. In: Banana Fusarium wilt management: towards sustainable cultivation, eds. by A. B. Molina, N. H. Nikmasdek and K. W. Liew, pp. 11-30. INIBAP-ASPNET, Los Banos, Laguna, Philippines.
  38. Mukherjee, G. and Sen, S. K. 2006. Purification, characterization, and antifungal activity of chitinase from Streptomyces venezuelae P10. Curr. Microbiol. 53:265-269. https://doi.org/10.1007/s00284-005-0412-4
  39. Panchapakesan, A. and Shankar, N. 2016. Fungal cellulases: an overview. In: New and future developments in microbial biotechnology and bioengineering, ed. by V. Gupta, pp. 9-18. Elsevier, Amsterdam, Netherlands.
  40. Panhwar, Q. A., Othman, R., Rahman, Z. A., Meon, S. and Ismail, M. R. 2012. Isolation and characterization of phosphate-solubilizing bacteria from aerobic rice. Afr. J. Biotechnol. 11:2711-2719.
  41. Perez-Vicente, L. F., Dita, M. A. and Martinez de la Parte, E. 2014. Technical manual prevention and diagnostic of Fusarium wilt (Panama disease) of banana caused by Fusarium oxysporum f. sp. cubense tropical race 4 (TR4). In: Workshop on Diagnosis of Fusarium Wilt (Panama Disease) Caused by Fusarium oxysporum f. sp. cubense Tropical Race 4: Mitigating the Threat and Preventing Its Spread in the Caribbean, pp. 1-74. Food and Agriculture Organization of the United Nations, Rome, Italy.
  42. Reis, A., Costa, H., Boiteux, L. S. and Lopes, C. A. 2005. First report of Fusarium oxysporum f. sp. lycopersici race 3 on tomato in Brazil. Fitopatol. Bras. 30:426-428. https://doi.org/10.1590/S0100-41582005000400017
  43. Sajitha, K. L. and Florence, E. J. M. 2013. Effects of Streptomyces sp. on growth of rubberwood sapstain fungus Lasiodiplodia theobromae. J. Trop. For. Sci. 25:393-399.
  44. Sangdee, A., Kornphachara, S. and Srisawat, N. 2016. In vitro screening of antagonistic activity of soil Streptomyces against plant pathogenic fungi and assessment of its characters. J. Agric. Technol. 12:173-185.
  45. Shen, Z., Ruan, Y., Chao, X., Zhang, J., Li, R. and Shen, Q. 2015. Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol. Fertil. Soils 51:553-562. https://doi.org/10.1007/s00374-015-1002-7
  46. Singh, V., Tripathi, C. K. M. and Bihari, V. 2008. Production, optimization and purification of an antifungal compound from Streptomyces capoamus MTCC 8123. Med. Chem Res. 17:94-102. https://doi.org/10.1007/s00044-007-9040-9
  47. Song, W., Zhou, L., Yang, C., Cao, X., Zhang, L. and Liu, X. 2004. Tomato Fusarium wilt and its chemical control strategies in a hydroponic system. Crop Prot. 23:243-247. https://doi.org/10.1016/j.cropro.2003.08.007
  48. Srividya, S., Thapa, A., Bhat, D. V., Golmei, K. and Dey, N. 2012. Streptomyces sp. 9p as effective biocontrol against chilli soilborne fungal phytopathogens. Eur. J. Exp. Biol. 2:163-173.
  49. Stackebrandt, E. and Ebers, J. 2006. Taxonomic parameters revisited: tarnished gold standards. Microbiol. Today 33:152-155.
  50. Subramaniam, G., Arumugam, S. and Rajendran, V. 2016. Plant growth promoting actinobacteria: a new avenue for enhancing the productivity and soil fertility of grain legumes. Springer, Singapore. 298 pp.
  51. Suresh, P., Vellasamy, S., Almaary, K. S., Dawoud, T. M. and Elbadawi, Y. B. 2021. Fluorescent pseudomonads (FPs) as a potential biocontrol and plant growth promoting agent associated with tomato rhizosphere. J. King Saud Univ. Sci. 33:101423.
  52. Taechowisan, T., Chuaychot, N., Chanaphat, S., Wanbanjob, A. and Tantiwachwutikul, P. 2009. Antagonistic effects of Streptomyces sp. SRM1 on Colletotrichum musae. Biotechnology 8:86-92. https://doi.org/10.3923/biotech.2009.86.92
  53. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197
  54. Trejo-Estrada, S. R., Paszczynski, A. and Crawford, D. L. 1998a. Antibiotics and enzymes produced by the biocontrol agent Streptomyces violaceusniger YCED-9. J. Ind. Microbiol. Biotechnol. 21:81-90. https://doi.org/10.1038/sj/jim/2900549
  55. Trejo-Estrada, S. R., Sepulveda, I. R. and Crawford, D. L. 1998b. In vitro and in vivo antagonism of Streptomyces violaceusniger YCED9 against fungal pathogens of turf grass. World J. Microbiol. Biotechnol. 14:865-872. https://doi.org/10.1023/A:1008877224089
  56. Verma, V. C., Singh, S. K. and Prakash, S. 2012. Bio-control and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss. J. Basic Microbiol. 51:550-556. https://doi.org/10.1002/jobm.201000155
  57. Vurukonda, S. S. K. P., Giovanardi, D. and Stefani, E. 2018. Plant growth promoting and biocontrol activity of Streptomyces spp. as endophytes. Int. J. Mol. Sci. 19:952.
  58. Wang, Y., Xia, Q., Wang, G., Zhang, H., Lu, X., Sun, J. and Zhang, X. 2017. Differential gene expression in banana roots in response to Fusarium wilt. Can. J. Plant Pathol. 39:163-175. https://doi.org/10.1080/07060661.2017.1342693
  59. Watve, M. G., Tickoo, R., Jog, M. M. and Bhole, B. D. 2001. How many antibiotics are produced by the genus Streptomyces? Arch Microbiol. 176:386-390. https://doi.org/10.1007/s002030100345
  60. Weisburg, W. G., Barns, S. M., Pelletier, D. A. and Lane, D. J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173:697-703. https://doi.org/10.1128/jb.173.2.697-703.1991
  61. Weller, D. M. 2007. Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250-256. https://doi.org/10.1094/PHYTO-97-2-0250
  62. Xio, K., Kinkel, L. L. and Samac, D. A. 2002. Biological control of Phytophthora root rots on alfalfa and soybean with Streptomyces. Biol. Control 23:285-295. https://doi.org/10.1006/bcon.2001.1015
  63. Zivkovic, S., Stojanovic, S., Ivanovic, Z., Gavrilovic, V., Popovic, T. and Balaz, J. 2010. Screening of antagonistic activity of microorganisms against Colletotrichum acutatum and Colletotrichum gloeosporioides. Arch. Biol. Sci. Belgrade 62:611-623. https://doi.org/10.2298/ABS1003611Z
  64. Zuo, C., Deng, G., Li, B., Huo, H., Li, C., Hu, C., Kuang, R., Yang, Q., Dong, T., Sheng, O. and Yi, G. 2018. Germplasm screening of Musa spp. for resistance to Fusarium oxysporum f. sp. cubense tropical race 4 (Foc TR4). Eur. J. Plant Pathol. 151:723-734. https://doi.org/10.1007/s10658-017-1406-3