Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense

Fusarium wilt of banana (FWB), caused by Fusarium oxysporum f. sp. cubense (Foc), especially tropical race 4 (TR4), presents the foremost menace to the global banana production. Extensive efforts have been made to search for efficient biological control agents for disease management. Our previous st...

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Main Authors: Xiaxia Wang, Zhenghua Du, Chanxin Chen, Shuang Guo, Qianzhuo Mao, Wei Wu, Ruimei Wu, Wenbo Han, Peifeng Xie, Yiping Zeng, Wenna Shan, Zonghua Wang, Xiaomin Yu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1177393/full
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author Xiaxia Wang
Xiaxia Wang
Zhenghua Du
Zhenghua Du
Chanxin Chen
Chanxin Chen
Shuang Guo
Shuang Guo
Qianzhuo Mao
Wei Wu
Ruimei Wu
Wenbo Han
Peifeng Xie
Yiping Zeng
Wenna Shan
Zonghua Wang
Zonghua Wang
Xiaomin Yu
author_facet Xiaxia Wang
Xiaxia Wang
Zhenghua Du
Zhenghua Du
Chanxin Chen
Chanxin Chen
Shuang Guo
Shuang Guo
Qianzhuo Mao
Wei Wu
Ruimei Wu
Wenbo Han
Peifeng Xie
Yiping Zeng
Wenna Shan
Zonghua Wang
Zonghua Wang
Xiaomin Yu
author_sort Xiaxia Wang
collection DOAJ
description Fusarium wilt of banana (FWB), caused by Fusarium oxysporum f. sp. cubense (Foc), especially tropical race 4 (TR4), presents the foremost menace to the global banana production. Extensive efforts have been made to search for efficient biological control agents for disease management. Our previous study showed that Streptomyces sp. XY006 exhibited a strong inhibitory activity against several phytopathogenic fungi, including F. oxysporum. Here, the corresponding antifungal metabolites were purified and determined to be two cyclic lipopeptide homologs, lipopeptin A and lipopeptin B. Combined treatment with lipopeptin complex antagonized Foc TR4 by inhibiting mycelial growth and conidial sporulation, suppressing the synthesis of ergosterol and fatty acids and lowering the production of fusaric acid. Electron microscopy observation showed that lipopeptide treatment induced a severe disruption of the plasma membrane, leading to cell leakage. Lipopeptin A displayed a more pronounced antifungal activity against Foc TR4 than lipopeptin B. In pot experiments, strain XY006 successfully colonized banana plantlets and suppressed the incidence of FWB, with a biocontrol efficacy of up to 87.7%. Additionally, XY006 fermentation culture application improved plant growth parameters and induced peroxidase activity in treated plantlets, suggesting a possible role in induced resistance. Our findings highlight the potential of strain XY006 as a biological agent for FWB, and further research is needed to enhance its efficacy and mode of action in planta.
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spelling doaj.art-1be9108dafcb4dd385550909c85d823d2023-04-27T05:35:32ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11773931177393Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubenseXiaxia Wang0Xiaxia Wang1Zhenghua Du2Zhenghua Du3Chanxin Chen4Chanxin Chen5Shuang Guo6Shuang Guo7Qianzhuo Mao8Wei Wu9Ruimei Wu10Wenbo Han11Peifeng Xie12Yiping Zeng13Wenna Shan14Zonghua Wang15Zonghua Wang16Xiaomin Yu17State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaSchool of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaSchool of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaCollege of Horticulture, Fujian Agriculture and Forestry University, Fuzhou, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Institute of Plant Virology, Ningbo University, Ningbo, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaState Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, ChinaFujian Universities Engineering Research Center of Marine Biology and Drugs, Fuzhou Institute of Oceanography, Minjiang University, Fuzhou, ChinaFAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, ChinaFusarium wilt of banana (FWB), caused by Fusarium oxysporum f. sp. cubense (Foc), especially tropical race 4 (TR4), presents the foremost menace to the global banana production. Extensive efforts have been made to search for efficient biological control agents for disease management. Our previous study showed that Streptomyces sp. XY006 exhibited a strong inhibitory activity against several phytopathogenic fungi, including F. oxysporum. Here, the corresponding antifungal metabolites were purified and determined to be two cyclic lipopeptide homologs, lipopeptin A and lipopeptin B. Combined treatment with lipopeptin complex antagonized Foc TR4 by inhibiting mycelial growth and conidial sporulation, suppressing the synthesis of ergosterol and fatty acids and lowering the production of fusaric acid. Electron microscopy observation showed that lipopeptide treatment induced a severe disruption of the plasma membrane, leading to cell leakage. Lipopeptin A displayed a more pronounced antifungal activity against Foc TR4 than lipopeptin B. In pot experiments, strain XY006 successfully colonized banana plantlets and suppressed the incidence of FWB, with a biocontrol efficacy of up to 87.7%. Additionally, XY006 fermentation culture application improved plant growth parameters and induced peroxidase activity in treated plantlets, suggesting a possible role in induced resistance. Our findings highlight the potential of strain XY006 as a biological agent for FWB, and further research is needed to enhance its efficacy and mode of action in planta.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1177393/fullantifungal effectStreptomycesbanana Fusarium wiltlipopeptidebiocontrol
spellingShingle Xiaxia Wang
Xiaxia Wang
Zhenghua Du
Zhenghua Du
Chanxin Chen
Chanxin Chen
Shuang Guo
Shuang Guo
Qianzhuo Mao
Wei Wu
Ruimei Wu
Wenbo Han
Peifeng Xie
Yiping Zeng
Wenna Shan
Zonghua Wang
Zonghua Wang
Xiaomin Yu
Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense
Frontiers in Microbiology
antifungal effect
Streptomyces
banana Fusarium wilt
lipopeptide
biocontrol
title Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense
title_full Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense
title_fullStr Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense
title_full_unstemmed Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense
title_short Antifungal effects and biocontrol potential of lipopeptide-producing Streptomyces against banana Fusarium wilt fungus Fusarium oxysporum f. sp. cubense
title_sort antifungal effects and biocontrol potential of lipopeptide producing streptomyces against banana fusarium wilt fungus fusarium oxysporum f sp cubense
topic antifungal effect
Streptomyces
banana Fusarium wilt
lipopeptide
biocontrol
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1177393/full
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