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

Li Hou,Pengcheng Yang,Xianhui Wang,Siyuan Guo,Xin Nie,Beibei Li,Ding Ding,Le Kang,Yuanyuan Wang

doi:10.7554/elife.65279

Li Hou, Pengcheng Yang + Show 7 more

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https://doi.org/10.7554/elife.65279

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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.

Highlights

Flight is an extraordinary biological trait that has only evolved in several kinds of animals and is notably effective in searching for food and mates, finding habitats, defending against predators, and adapting to seasonal changes in environment (Krause and Godin, 1996; Borgemeister et al, 1997; Chapman et al, 2010)
The results showed that the number of differentially expressed genes (DEGs) in flight muscle was greater than that in fat body (520 in flight muscle and 318 in fat body, Log2 FC >1, false discovery rate (FDR) < 0.05, reads per kb million mapped (RPKM) > 0.5)
RNA interference (RNAi) knockdown of fatty-acid-binding protein (FABP) resulted in a 99.3% decrease in FABP mRNA levels (Figure 4—figure supplement 4) and clearly suppressed the expression levels of multiple beta-oxidation-related genes, including CROT, CPT2, ACDM, ACADS, ACADSB, ECH-6, ACAT1, and CRAT (Figure 3G). These results indicated that the lipid metabolism pathway was significantly suppressed in the flight muscle of adipokinetic hormone (AKH)/corazonin-related peptide (ACP)-/- locusts and that FABP may serve as an important molecular target of ACP peptide signaling

Summary

Introduction

Flight is an extraordinary biological trait that has only evolved in several kinds of animals (e.g. insects, bats, and birds) and is notably effective in searching for food and mates, finding habitats, defending against predators, and adapting to seasonal changes in environment (Krause and Godin, 1996; Borgemeister et al, 1997; Chapman et al, 2010) Despite these adaptive advantages, flight is one of the most intense and energy-demanding physiological processes, especially for insects that possess long-term flight capacity, such as locusts and butterflies (Mentel et al, 2003; Zhan et al, 2014). Complex and precise spatial and temporal regulation of energy metabolism is essential for long-term

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