Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree

Mulberry (Morus) is an economically important woody tree that is suitable for use in sericulture as forage and in medicine. However, this broad-leaved tree is facing multiple threats ranging from phytopathogens to insect pests. Here, a Gram-positive, endospore-forming bacterium (ZJU1) was frequently...

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Main Authors: Sen Xie, Marine Vallet, Chao Sun, Maritta Kunert, Anja David, Xiancui Zhang, Bosheng Chen, Xingmeng Lu, Wilhelm Boland, Yongqi Shao
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Bioengineering and Biotechnology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fbioe.2019.00488/full
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spelling doaj-679841bba9c743798954695b34a4a3592020-11-25T01:54:25ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852020-01-01710.3389/fbioe.2019.00488500753Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) TreeSen Xie0Marine Vallet1Chao Sun2Maritta Kunert3Anja David4Xiancui Zhang5Bosheng Chen6Xingmeng Lu7Wilhelm Boland8Yongqi Shao9Yongqi Shao10Institute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, ChinaMax Planck Fellow Group on Plankton Community Interaction, Max Planck Institute for Chemical Ecology, Jena, GermanyAnalysis Center of Agrobiology and Environmental Sciences, Zhejiang University, Hangzhou, ChinaDepartment of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena, GermanyDepartment of Natural Product Biosynthesis, Max Planck Institute for Chemical Ecology, Jena, GermanyInstitute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, ChinaInstitute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, ChinaInstitute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, ChinaDepartment of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, Jena, GermanyInstitute of Sericulture and Apiculture, College of Animal Sciences, Zhejiang University, Hangzhou, ChinaKey Laboratory for Molecular Animal Nutrition, Ministry of Education, Hangzhou, ChinaMulberry (Morus) is an economically important woody tree that is suitable for use in sericulture as forage and in medicine. However, this broad-leaved tree is facing multiple threats ranging from phytopathogens to insect pests. Here, a Gram-positive, endospore-forming bacterium (ZJU1) was frequently isolated from healthy mulberry plants by screening for foliar endophytes showing antagonism against pathogens and pests. Whole-genome sequencing and annotation resulted in a genome size of 4.06 Mb and classified the bacterium as a novel strain of Bacillus amyloliquefaciens that has rarely been identified from tree leaves. An integrative approach combining traditional natural product chemistry, activity bioassays, and high-resolution mass spectrometry confirmed that strain ZJU1 uses a blend of antimicrobials including peptides and volatile organic compounds to oppose Botrytis cinerea, a major phytopathogenic fungus causing mulberry gray mold disease. We showed that the inoculation of endophyte-free plants with ZJU1 significantly decreased both leaf necrosis and mortality under field conditions. In addition to the direct interactions of endophytes with foliar pathogens, in planta studies suggested that the inoculation of endophytes also induced plant systemic defense, including high expression levels of mulberry disease resistance genes. Moreover, when applied to the generalist herbivore Spodoptera litura, ZJU1 was sufficient to reduce the pest survival rate below 50%. A previously undiscovered crystal toxin (Cry10Aa) could contribute to this insecticidal effect against notorious lepidopteran pests. These unique traits clearly demonstrate that B. amyloliquefaciens ZJU1 is promising for the development of successful strategies for biocontrol applications. The search for new plant-beneficial microbes and engineering microbiomes is therefore of great significance for sustainably improving plant performance.https://www.frontiersin.org/article/10.3389/fbioe.2019.00488/fullendophytefungal pathogenlepidopteran pestmulberrysymbiosis
collection DOAJ
language English
format Article
sources DOAJ
author Sen Xie
Marine Vallet
Chao Sun
Maritta Kunert
Anja David
Xiancui Zhang
Bosheng Chen
Xingmeng Lu
Wilhelm Boland
Yongqi Shao
Yongqi Shao
spellingShingle Sen Xie
Marine Vallet
Chao Sun
Maritta Kunert
Anja David
Xiancui Zhang
Bosheng Chen
Xingmeng Lu
Wilhelm Boland
Yongqi Shao
Yongqi Shao
Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree
Frontiers in Bioengineering and Biotechnology
endophyte
fungal pathogen
lepidopteran pest
mulberry
symbiosis
author_facet Sen Xie
Marine Vallet
Chao Sun
Maritta Kunert
Anja David
Xiancui Zhang
Bosheng Chen
Xingmeng Lu
Wilhelm Boland
Yongqi Shao
Yongqi Shao
author_sort Sen Xie
title Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree
title_short Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree
title_full Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree
title_fullStr Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree
title_full_unstemmed Biocontrol Potential of a Novel Endophytic Bacterium From Mulberry (Morus) Tree
title_sort biocontrol potential of a novel endophytic bacterium from mulberry (morus) tree
publisher Frontiers Media S.A.
series Frontiers in Bioengineering and Biotechnology
issn 2296-4185
publishDate 2020-01-01
description Mulberry (Morus) is an economically important woody tree that is suitable for use in sericulture as forage and in medicine. However, this broad-leaved tree is facing multiple threats ranging from phytopathogens to insect pests. Here, a Gram-positive, endospore-forming bacterium (ZJU1) was frequently isolated from healthy mulberry plants by screening for foliar endophytes showing antagonism against pathogens and pests. Whole-genome sequencing and annotation resulted in a genome size of 4.06 Mb and classified the bacterium as a novel strain of Bacillus amyloliquefaciens that has rarely been identified from tree leaves. An integrative approach combining traditional natural product chemistry, activity bioassays, and high-resolution mass spectrometry confirmed that strain ZJU1 uses a blend of antimicrobials including peptides and volatile organic compounds to oppose Botrytis cinerea, a major phytopathogenic fungus causing mulberry gray mold disease. We showed that the inoculation of endophyte-free plants with ZJU1 significantly decreased both leaf necrosis and mortality under field conditions. In addition to the direct interactions of endophytes with foliar pathogens, in planta studies suggested that the inoculation of endophytes also induced plant systemic defense, including high expression levels of mulberry disease resistance genes. Moreover, when applied to the generalist herbivore Spodoptera litura, ZJU1 was sufficient to reduce the pest survival rate below 50%. A previously undiscovered crystal toxin (Cry10Aa) could contribute to this insecticidal effect against notorious lepidopteran pests. These unique traits clearly demonstrate that B. amyloliquefaciens ZJU1 is promising for the development of successful strategies for biocontrol applications. The search for new plant-beneficial microbes and engineering microbiomes is therefore of great significance for sustainably improving plant performance.
topic endophyte
fungal pathogen
lepidopteran pest
mulberry
symbiosis
url https://www.frontiersin.org/article/10.3389/fbioe.2019.00488/full
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