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.

Metrics

  • 2,493
    Page views
  • 660
    Downloads
  • 5
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Developmental Biology
    2. Evolutionary Biology
    Alexandre P Thiery et al.
    Research Article Updated

    Development of tooth shape is regulated by the enamel knot signalling centre, at least in mammals. Fgf signalling regulates differential proliferation between the enamel knot and adjacent dental epithelia during tooth development, leading to formation of the dental cusp. The presence of an enamel knot in non-mammalian vertebrates is debated given differences in signalling. Here, we show the conservation and restriction of fgf3, fgf10, and shh to the sites of future dental cusps in the shark (Scyliorhinus canicula), whilst also highlighting striking differences between the shark and mouse. We reveal shifts in tooth size, shape, and cusp number following small molecule perturbations of canonical Wnt signalling. Resulting tooth phenotypes mirror observed effects in mammals, where canonical Wnt has been implicated as an upstream regulator of enamel knot signalling. In silico modelling of shark dental morphogenesis demonstrates how subtle changes in activatory and inhibitory signals can alter tooth shape, resembling developmental phenotypes and cusp shapes observed following experimental Wnt perturbation. Our results support the functional conservation of an enamel knot-like signalling centre throughout vertebrates and suggest that varied tooth types from sharks to mammals follow a similar developmental bauplan. Lineage-specific differences in signalling are not sufficient in refuting homology of this signalling centre, which is likely older than teeth themselves.

    1. Developmental Biology
    2. Evolutionary Biology
    Sophie Pantalacci
    Insight

    The tooth shape of sharks and mice are regulated by a similar signaling center despite their teeth having very different geometries.