Volatile DMNT directly protects plants against Plutella xylostella by disrupting peritrophic matrix barrier in midgut

  1. Chen Chen
  2. Hongyi Chen
  3. Shijie Huang
  4. Taoshan Jiang
  5. Chuanhong Wang
  6. Zhen Tao
  7. Chen He
  8. Qingfeng Tang
  9. Peijin Li  Is a corresponding author
  1. Anhui Agricultual University, China
  2. Anhui Agricultural University, China

Abstract

Insect pests negatively affect crop quality and yield; identifying new methods to protect crops against insects therefore has important agricultural applications. Our analysis of transgenic Arabidopsis thaliana plants showed that overexpression of PENTACYCLIC TRITERPENE SYNTHASE 1 (PEN1), encoding the key biosynthetic enzyme for the natural plant product (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), led to significant resistance against a major insect pest, Plustella xylostella. DMNT treatment severely damaged the peritrophic matrix (PM), a physical barrier isolating food and pathogens from the midgut wall cells. DMNT repressed the expression of PxMucin in midgut cells and knocking down PxMucin resulted in PM rupture and P. xylostella death. A 16S RNA survey revealed that DMNT significantly disrupted midgut microbiota populations and that midgut microbes were essential for DMNT-induced killing. Therefore, we propose that the midgut microbiota assists DMNT in killing P. xylostella. These findings may provide a novel approach for plant protection against P. xylostella.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 1-6, Figure 1-figure supplement 1, 3-5, Figure 4-figure supplement 2, Figure 5-figure supplement 2, and Figure 6-figure supplement 2-3.

Article and author information

Author details

  1. Chen Chen

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Hongyi Chen

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Shijie Huang

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Taoshan Jiang

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Chuanhong Wang

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Zhen Tao

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Chen He

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Qingfeng Tang

    The School of Plant Protection, Anhui Agricultural University, Hefei, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Peijin Li

    The School of Life Sciences, Anhui Agricultual University, Hefei, China
    For correspondence
    Peijin.li@ahau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1579-7553

Funding

National Key Research and Development Program of China (2017YFD0301301)

  • Peijin Li

National Key Research and Development Program of China (2016YFD0101803)

  • Peijin Li

Natural Science Foundation of China (31670264)

  • Peijin Li

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Youngsung Joo, Chungbuk National University, Republic of Korea

Publication history

  1. Received: October 11, 2020
  2. Accepted: February 17, 2021
  3. Accepted Manuscript published: February 18, 2021 (version 1)
  4. Version of Record published: March 2, 2021 (version 2)

Copyright

© 2021, Chen et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Chen Chen
  2. Hongyi Chen
  3. Shijie Huang
  4. Taoshan Jiang
  5. Chuanhong Wang
  6. Zhen Tao
  7. Chen He
  8. Qingfeng Tang
  9. Peijin Li
(2021)
Volatile DMNT directly protects plants against Plutella xylostella by disrupting peritrophic matrix barrier in midgut
eLife 10:e63938.
https://doi.org/10.7554/eLife.63938
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