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

Author:

Wang Xin-Qiu1ORCID,Guo Jian-sheng2,Li Dan-Ting13,Yu Yang4,Hagoort Jaco5,Moussian Bernard6ORCID,Zhang Chuan-Xi3ORCID

Affiliation:

1. Institute of Insect Science, Zhejiang University, Hangzhou, China

2. Department of Pathology of Sir Run Run Shaw Hospital, and Center of Cryo-Electron Microscopy, School of Medicine, Zhejiang University, Hangzhou, China

3. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, China

4. Carl Zeiss (Shanghai) Co., Ltd.60 Meiyue Road, China (Shanghai) Pilot Free Trade Zone, Shanghai, China

5. Department of Medical Biology, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, Netherlands

6. Université Côte d’Azur, CNRS, Université Côte d’Azur, Institute of Biology Valrose, Parc Valrose, Inserm, France

Abstract

Using serial block-face scanning electron microscopy, 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.

Funder

National Natural Science Foundation of China

Natural Science Foundation of Zhejiang Province

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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