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The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin

INTRODUCTION: Pine wilt disease (PWD) is responsible for extensive economic and ecological damage to Pinus spp. forests and plantations worldwide. PWD is caused by the pine wood nematode (PWN, Bursaphelenchus xylophilus) and transmitted into pine trees by a vector insect, the Japanese pine sawyer (J...

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Autores principales: Jia, Jiayu, Chen, Long, Yu, Wenjing, Cai, Shouping, Su, Shunde, Xiao, Xiangxi, Tang, Xinghao, Jiang, Xiangqing, Chen, Daoshun, Fang, Yu, Wang, Jinjin, Luo, Xiaohua, Li, Jian, Huang, Yunpeng, Su, Jun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10663349/
https://www.ncbi.nlm.nih.gov/pubmed/38023855
http://dx.doi.org/10.3389/fpls.2023.1257744
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author Jia, Jiayu
Chen, Long
Yu, Wenjing
Cai, Shouping
Su, Shunde
Xiao, Xiangxi
Tang, Xinghao
Jiang, Xiangqing
Chen, Daoshun
Fang, Yu
Wang, Jinjin
Luo, Xiaohua
Li, Jian
Huang, Yunpeng
Su, Jun
author_facet Jia, Jiayu
Chen, Long
Yu, Wenjing
Cai, Shouping
Su, Shunde
Xiao, Xiangxi
Tang, Xinghao
Jiang, Xiangqing
Chen, Daoshun
Fang, Yu
Wang, Jinjin
Luo, Xiaohua
Li, Jian
Huang, Yunpeng
Su, Jun
author_sort Jia, Jiayu
collection PubMed
description INTRODUCTION: Pine wilt disease (PWD) is responsible for extensive economic and ecological damage to Pinus spp. forests and plantations worldwide. PWD is caused by the pine wood nematode (PWN, Bursaphelenchus xylophilus) and transmitted into pine trees by a vector insect, the Japanese pine sawyer (JPS, Monochamus alternatus). Host infection by PWN will attract JPS to spawn, which leads to the co-existence of PWN and JPS within the host tree, an essential precondition for PWD outbreaks. Through the action of their metabolites, microbes can manipulate the co-existence of PWN and JPS, but our understanding on how key microorganisms engage in this process remains limited, which severely hinders the exploration and utilization of promising microbial resources in the prevention and control of PWD. METHODS: In this study we investigated how the PWN-associated fungus Aspergillus promotes the co-existence of PWN and JPS in the host trees (Pinus massoniana) via its secondary metabolite, sterigmatocystin (ST), by taking a multi-omics approach (phenomics, transcriptomics, microbiome, and metabolomics). RESULTS: We found that Aspergillus was able to promote PWN invasion and pathogenicity by increasing ST biosynthesis in the host plant, mainly by suppressing the accumulation of ROS (reactive oxygen species) in plant tissues that could counter PWN. Further, ST accumulation triggered the biosynthesis of VOC (volatile organic compounds) that attracts JPS and drives the coexistence of PWN and JPS in the host plant, thereby encouraging the local transmission of PWD. Meanwhile, we show that application of an Aspergillus inhibitor (chiricanine A treatment) results in the absence of Aspergillus and decreases the in vivo ST amount, thereby sharply restricting the PWN development in host. This further proved that Aspergillus is vital and sufficient for promoting PWD transmission. DISCUSSION: Altogether, these results document, for the first time, how the function of Aspergillus and its metabolite ST is involved in the entire PWD transmission chain, in addition to providing a novel and long-term effective nematicide for better PWD control in the field.
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spelling pubmed-106633492023-01-01 The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin Jia, Jiayu Chen, Long Yu, Wenjing Cai, Shouping Su, Shunde Xiao, Xiangxi Tang, Xinghao Jiang, Xiangqing Chen, Daoshun Fang, Yu Wang, Jinjin Luo, Xiaohua Li, Jian Huang, Yunpeng Su, Jun Front Plant Sci Plant Science INTRODUCTION: Pine wilt disease (PWD) is responsible for extensive economic and ecological damage to Pinus spp. forests and plantations worldwide. PWD is caused by the pine wood nematode (PWN, Bursaphelenchus xylophilus) and transmitted into pine trees by a vector insect, the Japanese pine sawyer (JPS, Monochamus alternatus). Host infection by PWN will attract JPS to spawn, which leads to the co-existence of PWN and JPS within the host tree, an essential precondition for PWD outbreaks. Through the action of their metabolites, microbes can manipulate the co-existence of PWN and JPS, but our understanding on how key microorganisms engage in this process remains limited, which severely hinders the exploration and utilization of promising microbial resources in the prevention and control of PWD. METHODS: In this study we investigated how the PWN-associated fungus Aspergillus promotes the co-existence of PWN and JPS in the host trees (Pinus massoniana) via its secondary metabolite, sterigmatocystin (ST), by taking a multi-omics approach (phenomics, transcriptomics, microbiome, and metabolomics). RESULTS: We found that Aspergillus was able to promote PWN invasion and pathogenicity by increasing ST biosynthesis in the host plant, mainly by suppressing the accumulation of ROS (reactive oxygen species) in plant tissues that could counter PWN. Further, ST accumulation triggered the biosynthesis of VOC (volatile organic compounds) that attracts JPS and drives the coexistence of PWN and JPS in the host plant, thereby encouraging the local transmission of PWD. Meanwhile, we show that application of an Aspergillus inhibitor (chiricanine A treatment) results in the absence of Aspergillus and decreases the in vivo ST amount, thereby sharply restricting the PWN development in host. This further proved that Aspergillus is vital and sufficient for promoting PWD transmission. DISCUSSION: Altogether, these results document, for the first time, how the function of Aspergillus and its metabolite ST is involved in the entire PWD transmission chain, in addition to providing a novel and long-term effective nematicide for better PWD control in the field. Frontiers Media S.A. 2023-11-08 /pmc/articles/PMC10663349/ /pubmed/38023855 http://dx.doi.org/10.3389/fpls.2023.1257744 Text en Copyright © 2023 Jia, Chen, Yu, Cai, Su, Xiao, Tang, Jiang, Chen, Fang, Wang, Luo, Li, Huang and Su https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Jia, Jiayu
Chen, Long
Yu, Wenjing
Cai, Shouping
Su, Shunde
Xiao, Xiangxi
Tang, Xinghao
Jiang, Xiangqing
Chen, Daoshun
Fang, Yu
Wang, Jinjin
Luo, Xiaohua
Li, Jian
Huang, Yunpeng
Su, Jun
The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin
title The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin
title_full The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin
title_fullStr The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin
title_full_unstemmed The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin
title_short The novel nematicide chiricanine A suppresses Bursaphelenchus xylophilus pathogenicity in Pinus massoniana by inhibiting Aspergillus and its secondary metabolite, sterigmatocystin
title_sort novel nematicide chiricanine a suppresses bursaphelenchus xylophilus pathogenicity in pinus massoniana by inhibiting aspergillus and its secondary metabolite, sterigmatocystin
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10663349/
https://www.ncbi.nlm.nih.gov/pubmed/38023855
http://dx.doi.org/10.3389/fpls.2023.1257744
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