Three-dimensional reconstruction of a whole insect reveals its phloem sap-sucking mechanism at nano-resolution

  1. Xin-Qiu Wang
  2. Jian-sheng Guo
  3. Dan-Ting Li
  4. Yang Yu
  5. Jaco Hagoort
  6. Bernard Moussian
  7. Chuan Xi Zhang  Is a corresponding author
  1. Zhejiang University, China
  2. Carl Zeiss (Shanghai) Co Ltd, China
  3. University of Amsterdam, Netherlands
  4. Université Côte d'Azur, CNRS, Inserm, France
  5. Ningbo University, China

Abstract

Using serial block face scanning electron microscopy (SBF-SEM), we report on the internal 3D structures of the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae) at nanometer resolution for the first time. Within the reconstructed organs and tissues, we found many novel and fascinating internal structures in the planthopper such as naturally occurring three four-way rings connecting adjacent spiracles to facilitate efficient gas exchange, and fungal endosymbionts in a single huge insect cell occupying 22% of the abdomen volume to enable the insect to live on plant sap. To understand the muscle and stylet movement during phloem sap-sucking, the cephalic skeleton and muscles were reconstructed in feeding nymphs. The results revealed an unexpected contraction of the protractors of the stylets, and suggested a novel feeding model for the phloem sap-sucking.

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 Figures 1-5.

Article and author information

Author details

  1. Xin-Qiu Wang

    Institute of Insect Science, Zhejiang University, Hangzhou, China
    Competing interests
    No competing interests declared.
  2. Jian-sheng Guo

    Center of Cryo-electron Microscopy, Zhejiang University, Hangzhou, China
    Competing interests
    No competing interests declared.
  3. Dan-Ting Li

    Institute of Insect Science, Zhejiang University, Hangzhou, China
    Competing interests
    No competing interests declared.
  4. Yang Yu

    Carl Zeiss (Shanghai) Co Ltd, Shanghai, China
    Competing interests
    Yang Yu, Yang Yu is affiliated with Carl Zeiss (Shanghai) Co., Ltd. The author has no financial interests to declare.
  5. Jaco Hagoort

    Department of Medical Biology, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    No competing interests declared.
  6. Bernard Moussian

    Université Côte d'Azur, CNRS, Inserm, Nice, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2854-9500
  7. Chuan Xi Zhang

    Institute of Plant Virology, Ningbo University, Ningbo, China
    For correspondence
    chxzhang@zju.edu.cn
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7784-1188

Funding

National Natural Science Foundation of China (31630057)

  • Chuan Xi Zhang

National Natural Science Foundation of China (31871954)

  • Chuan Xi Zhang

Natural Science Foundation of Zhejiang Province (LQ20C040003)

  • Jian-sheng Guo

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

Reviewing Editor

  1. Michael B Eisen, University of California, Berkeley, United States

Publication history

  1. Received: September 7, 2020
  2. Accepted: February 22, 2021
  3. Accepted Manuscript published: February 23, 2021 (version 1)
  4. Version of Record published: April 1, 2021 (version 2)
  5. Version of Record updated: April 12, 2021 (version 3)

Copyright

© 2021, Wang 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. Xin-Qiu Wang
  2. Jian-sheng Guo
  3. Dan-Ting Li
  4. Yang Yu
  5. Jaco Hagoort
  6. Bernard Moussian
  7. Chuan Xi Zhang
(2021)
Three-dimensional reconstruction of a whole insect reveals its phloem sap-sucking mechanism at nano-resolution
eLife 10:e62875.
https://doi.org/10.7554/eLife.62875
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