Neuropeptide ACP facilitates lipid oxidation and utilization during long-term flight in locusts

  1. Li Hou
  2. Siyuan Guo
  3. Yuanyuan Wang
  4. Xin Nie
  5. Pengcheng Yang
  6. Ding Ding
  7. Beibei Li
  8. Le Kang  Is a corresponding author
  9. Xianhui Wang  Is a corresponding author
  1. Institute of Zoology, Chinese Academy of Sciences, China
  2. Chinese Academy of Sciences, China

Abstract

Long-term flight depends heavily on intensive energy metabolism in animals; however, the neuroendocrine mechanisms underlying efficient substrate utilization remain elusive. Here, we report that the adipokinetic hormone/corazonin-related peptide (ACP) can facilitate muscle lipid utilization in a famous long-term migratory flighting species, Locusta migratoria. By peptidomic analysis and RNAi screening, we identified brain-derived ACP as a key flight-related neuropeptide. ACP gene expression increased notably upon sustained flight. CRISPR/Cas9-mediated knockout of ACP gene and ACP receptor gene (ACPR) significantly abated prolonged flight of locusts. Transcriptomic and metabolomic analyses further revealed that genes and metabolites involved in fatty acid transport and oxidation were notably downregulated in the flight muscle of ACP mutants. Finally, we demonstrated that a fatty acid-binding protein (FABP) mediated the effects of ACP in regulating muscle lipid metabolism during long-term flight in locusts. Our results elucidated a previously undescribed neuroendocrine mechanism underlying efficient energy utilization associated with long-term flight.

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, 2, 3, 4, 5, and 6.

The following data sets were generated
    1. Yang P
    (2020) RNA-Seq of fat body and muscle tissues in ACP mutant locusts
    National Genomics Data Center, Beijing Institute of Genomics.

Article and author information

Author details

  1. Li Hou

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Siyuan Guo

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Yuanyuan Wang

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Xin Nie

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Pengcheng Yang

    Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Ding Ding

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Beibei Li

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Le Kang

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    lkang@ioz.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4262-2329
  9. Xianhui Wang

    State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
    For correspondence
    wangxh@ioz.ac.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8732-829X

Funding

National Natural Science Foundation of China (Grant NO. 31930012)

  • Xianhui Wang

National Natural Science Foundation of China (Grant NO. 32070497)

  • Li Hou

Chinese Academy of Sciences (nos. 152111KYSB20180036)

  • Le Kang

Youth Innovation Promotion Association of the Chinese Academy of Sciences (No. 2021079)

  • Li Hou

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

Reviewing Editor

  1. Raghu Padinjat, National Centre for Biological Sciences, India

Publication history

  1. Received: November 29, 2020
  2. Accepted: June 18, 2021
  3. Accepted Manuscript published: June 21, 2021 (version 1)
  4. Accepted Manuscript updated: July 1, 2021 (version 2)
  5. Version of Record published: July 30, 2021 (version 3)

Copyright

© 2021, Hou 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. Li Hou
  2. Siyuan Guo
  3. Yuanyuan Wang
  4. Xin Nie
  5. Pengcheng Yang
  6. Ding Ding
  7. Beibei Li
  8. Le Kang
  9. Xianhui Wang
(2021)
Neuropeptide ACP facilitates lipid oxidation and utilization during long-term flight in locusts
eLife 10:e65279.
https://doi.org/10.7554/eLife.65279

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