Antifungal potential of Lactiplantibacillus plantarum AM2 against the banana pathogen Fusarium oxysporum f. sp. cubense Tropical Race 4

Document Type : Original Research

Authors
1 Department of Cell and Molecular Biology, Faculty of Biotechnology and Biomolecular Sciences, University of Putra Malaysia, Serdang, Selangor, Malaysia.
2 Research Center for Applied Microbiology, Research Organization for Life Sciences, National Research and Innovation Agency (BRIN), Jl. Raya Jakarta-Bogor Km. 46, Cibinong, Bogor, West Java 16911, Indonesia.
3 Laboratory of Sustainable Agronomy and Crop Protection, Institute of Plantation Studies, University of Putra Malaysia, Serdang, Selangor, Malaysia.
Abstract
Fusarium wilt of bananas is a serious disease affecting banana plantations worldwide. In an effort to sustainably manage the disease, biological control is considered a promising alternative to agrochemicals that can cause detrimental effects on humans and the ecosystem. In this study, we investigated the biological control potential of the present collection of beneficial bacteria, including Lactiplantibacillus plantarum AM2, Streptomyces morookaensis NRRL B-12429, Bacillus velezensis B4158, B. atrophaeus B363B, and B. amyloliquefaciens B942, through a dual culture assay and a greenhouse experiment. The studied causal agent of Fusarium wilt in banana was Fusarium oxysporum f. sp. cubense Tropical Race 4 (Foc TR4). The inhibition range in vitro was between 31.0% to 42.1%, and the highest growth inhibition of Foc TR4 was observed for L. plantarum AM2. Infected banana plantlets that received the treatment with L. plantarum AM2 also showed a significant reduction in disease severity index, as low as 24% compared to the treatment with other beneficial bacteria. This study showed that L. plantarum AM2 has a good antagonistic effect on Foc TR4 mycelial growth and the most potential to control Fusarium wilt disease in bananas.

Keywords


Asari, S., Matzén, S., Petersen, M.A., Bejai, S., and Meijer, J. 2016. Multiple effects of Bacillus amyloliquefaciens volatile compounds: plant growth promotion and growth inhibition of phytopathogens. FEMS Microbiol Ecol, 92(6):fiw070
Bergsma, S., Euverink, G. J. W., Charalampogiannis, N., Poulios, E., Janssens, T. K., and Achinas, S. 2022. Biotechnological and medical aspects of lactic acid bacteria used for plant protection: A comprehensive review. BioTech, 11(3): 40
Besset-Manzoni, Y., Joly, P., Brutel, A., Gerin, F., Soudiere, O., Langin, T., and Prigent-Combaret, C. 2019. Does in vitro selection of biocontrol agents guarantee success in planta? A study case of wheat protection against Fusarium seedling blight by soil bacteria. PLoS One, 14(12): e0225655.
Bubici, G., Kaushal, M., Prigigallo, M. I., Gómez-Lama Cabanás, C., and Mercado-Blanco, J. 2019. Biological control agents against Fusarium wilt of banana. Front. Microbiol, 10: 616.
Caro, L. P. 2020. Wages and working conditions in the banana sector: the case of Costa Rica, Ethiopia, India, Indonesia, and Viet Nam: Background note. International Labour Organization (ILO).
Deepthi, B. V., Poornachandra Rao, K., Chennapa, G., Naik, M. K., Chandrashekara, K. T., and Sreenivasa, M. Y. 2016. Antifungal attributes of Lactobacillus plantarum MYS6 against fumonisin-producing Fusarium proliferatum associated with poultry feeds. PLoS One, 11(6): e0155122
He, P., Li, S., Xu, S., Fan, H., Wang, Y., Zhou, W., Fu, G., Han, G., Wang, Y.Y., and Zheng, S.J. 2021. Monitoring Tritrophic Biocontrol Interactions Between Bacillus spp., Fusarium oxysporum f. sp. cubense, Tropical Race 4, and Banana Plants in vivo Based on Fluorescent Transformation System. Front Microbiol, 13(12):754918.
Purkayastha, G. D., Mangar, P., Saha, A., and Saha, D. 2018. Evaluation of the biocontrol efficacy of a Serratia marcescens strain indigenous to tea rhizosphere for the management of root rot disease in tea. PloS one, 13(2): e0191761.
Dita, M. A., Teixeira, L., Li, C., Zheng, S., O'Neill, W., Daniels, J., Pérez-Vicente, L., Carreel, F., Roussel, V., Carlier, J., Abadie, C., Carpentier, S.C., Iyyakutty, R., Kissel, E., van Wesemael, J., Chase, R., Tomekpe, K., and Roux, N. (eds.) 2021. Practical guidelines for early screening and field evaluation of banana against Fusarium wilt, Pseudocercospora leaf spots and drought. Bioversity International. Montpellier, France. 83 p.
EFSA BIOHAZ Panel. 2023. Updated list of QPS-recommended microorganisms for safety risk assessments carried out by EFSA. The European Food Safety Authority (EFSA). Retrieved December 10, 2023, from https://zenodo.org/records/8124409
Fan, H., Li, S., Zeng, L., He, P., Xu, S., Bai, T., Huang, Y., Guo, Z., and Zheng, S.-J. 2021. Biological control of Fusarium oxysporum f. sp. cubense Tropical Race 4 using natively isolated Bacillus spp. YN0904 and YN1419. J Fungi, 7(10): 795.
Fira, D., Dimkić, I., Berić, T., Lozo, J., and Stanković, S. 2018. Biological control of plant pathogens by Bacillus species. J Biotech, 285: 44-55.
FAO. (2022). Banana market review- Preliminary results 2021. Rome.
Fu, L., Penton, C. R., Ruan, Y., Shen, Z., Xue, C., Li, R., and Shen, Q. 2017. Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol Biochem, 104: 39-48.
Jaffar, N. S., Jawan, R., and Chong, K. P. 2023. The potential of lactic acid bacteria in mediating the control of plant diseases and plant growth stimulation in crop production-A mini review. Front Plant Sci, 13: 1047945.
Kavková, M., Bazalová, O., Cihlář, J., Bohatá, A., Lencová, J., & Konvalina, P. 2023. Characterization of wild strains of lactic acid bacteria isolated from legumes and their biocontrol potential against Fusarium spp. Agronomy, 13(12): 2911.
Lahlali, R., Ezrari, S., Radouane, N., Kenfaoui, J., Esmaeel, Q., El Hamss, H., Belabess, Z., and Barka, E. A. 2022. Biological control of plant pathogens: A global perspective. Microorganisms, 10(3): 596.
Li, C., Zuo, C., Deng, G., Kuang, R., Yang, Q., Hu, C., Sheng, O., Zhang, S., Ma, L., Wei, Y., Yang, J., Liu, S., Biswas, M.K., Viljoen, A., and Yi, G. 2013. Contamination of bananas with beauvericin and fusaric acid produced by Fusarium oxysporum f. sp. cubense. PloS one, 8(7): e70226.
Li, Q., Zeng, X., Fu, H., Wang, X., Guo, X., and Wang M. 2023. Lactiplantibacillus plantarum: A comprehensive review of its antifungal and anti-mycotoxic effects. Trends Food Sci Tech, 136: 224-238.
Ordóñez, N. (2018). A global genetic diversity analysis of Fusarium oxysporum f. sp. cubense: the Panama disease pathogen of banana [Doctoral dissertation, Wageningen University and Research].
Parikh, L., Eskelson, M. J., and Adesemoye, A. O. 2018. Relationship of in vitro and in planta screening: improving the selection process for biological control agents against Fusarium root rot in row crops. Arch Phytopathol Plant Protect, 51(3-4): 156-169.
Pérez-Vicente, L., Dita, M. A., and Martínez-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). Food and Agriculture Organization of The United Nations.
Ploetz, R. C. (2015). Fusarium wilt of banana. Phytopathol, 105(12): 1512-1521.
Rajaofera, M.J.N, Wang, Y., Dahar, G.Y., Jin, P., Fan, L., Xu, L., Liu, W., and Miao, W. 2019. Volatile organic compounds of Bacillus atrophaeus HAB-5 inhibit the growth of Colletotrichum gloeosporioides. Pestic Biochem Physiol, 156:170-176.
Raman, J., Kim, J. S., Choi, K. R., Eun, H., Yang, D., Ko, Y. J., and Kim, S. J. 2022. Application of lactic acid bacteria (LAB) in sustainable agriculture: Advantages and limitations. Intl J Mol Sci, 23(14): 7784.
Riolo, M., Luz, C., Santilli, E., Meca, G., & Cacciola, S. O. 2023. Antifungal activity of selected lactic acid bacteria from olive drupes. Food Biosci, 52: 102422.
Sánchez-Espinosa, A.C., Villarruel-Ordaz, J.L., and Maldonado-Bonilla, L.D. 2020. The cause and potential solution to the Fusarium wilt disease in banana plants. Terra Latinoam, 38(2): 435-442.
Saravanan, R., Nakkeeran, S., Saranya, N., Kavino, M., Ragapriya, V., Varanavasiappan, S., Raveendran, M., Krishnamoorthy, A.S., Malathy, V.G., and Haripriya, S. 2022. Biohardening of banana cv. Karpooravalli (ABB; Pisang Awak) with Bacillus velezensis YEBBR6 promotes plant growth and reprograms the innate immune response against Fusarium oxysporum f.sp. cubense. Front Sustain Food Syst, 6:845512.
Scortichini, M. 2022. Sustainable management of diseases in horticulture: Conventional and new options. Horticulturae, 8(6): 517.
Seddik, H.A., Bendali, F., Gancel, F., Fliss, I., Spano, G., and Drider, D. 2017. Lactobacillus plantarum and its probiotic and food potentialities. Probiotics Antimicro, 9(2): 111-122.
Vanitha, P. R., Somashekaraiah, R., Divyashree, S., Pan, I., and Sreenivasa, M. Y. 2023. Antifungal activity of probiotic strain Lactiplantibacillus plantarum MYSN7 against Trichophyton tonsurans. Front Microbiol, 14: 1192449.
Wei, C., Yu, L., Qiao, N., Wang, S., Tian, F., Zhao, J., Zhang, H., Zhai, Q., and Chen, W. 2020. The characteristics of patulin detoxification by Lactobacillus plantarum 13M5. Food Chem Toxicol, 146: 111787.
Xiang, D., Yang, X., Liu, B., Chu, Y., Liu, S., and Li, C. 2023. Bio-priming of banana tissue culture plantlets with endophytic Bacillus velezensis EB1 to improve Fusarium wilt resistance. Front Microbiol, 14: 1146331.
Zhang, N., X, He, Zhang, J., Raza, W., Yang, X.-M., Ruan, Y.-Z., Shen, Q.-R., Huang, and Q.-W. 2014. Suppression of Fusarium Wilt of Banana with Application of Bio-Organic Fertilizers. Pedosphere, 24 (5): 613-624.
Zheng, J., Wittouck, S., Salvetti, E., Franz, C.M.A.P., Harris, H.M.B., Mattarelli, P., O'Toole, P.W., Pot, B., Vandamme, P., Walter, J., Watanabe, K., Wuyts, S., Felis, G.E., Gänzle, M.G., and Lebeer, S. 2020. A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and :union: of Lactobacillaceae and Leuconostocaceae. Intl J System Evol Microbiol, 70(4): 2782-2858.
Zhu, Y., Xu, Y., & Yang, Q. 2021a. Antifungal properties and AFB1 detoxification activity of a new strain of Lactobacillus plantarum. J Hazard Mater, 414(7): 125569.
Zhu, Z., Tian, Z., & Li, J. 2021b. A Streptomyces morookaensis strain promotes plant growth and suppresses Fusarium wilt of banana. Trop Plant Pathol, 46: 175-185.