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.

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

  • 3,894
    views
  • 962
    downloads
  • 20
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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

Share this article

https://doi.org/10.7554/eLife.62875

Further reading

    1. Developmental Biology
    Yanlin Hou, Zhengwen Nie ... Hans R Scholer
    Research Article

    During the first lineage segregation, mammalian embryos generate the inner cell mass (ICM) and trophectoderm (TE). ICM gives rise to the epiblast (EPI) that forms all cell types of the body, an ability referred to as pluripotency. The molecular mechanisms that induce pluripotency in embryos remain incompletely elucidated. Using knockout (KO) mouse models in conjunction with low-input ATAC-seq and RNA-seq, we found that Oct4 and Sox2 gradually come into play in the early ICM, coinciding with the initiation of Sox2 expression. Oct4 and Sox2 activate the pluripotency-related genes through the putative OCT-SOX enhancers in the early ICM. Furthermore, we observed a substantial reorganization of chromatin landscape and transcriptome from the morula to the early ICM stages, which was partially driven by Oct4 and Sox2, highlighting their pivotal role in promoting the developmental trajectory toward the ICM. Our study provides new insights into the establishment of the pluripotency network in mouse preimplantation embryos.

    1. Developmental Biology
    2. Neuroscience
    Maria I Lazaro-Pena, Carlos A Diaz-Balzac
    Insight

    The ligand Netrin mediates axon guidance through a combination of haptotaxis over short distances and chemotaxis over longer distances.