Dataset Information

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

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.

SUBMITTER: Hou L

PROVIDER: S-EPMC8324298 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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

Hou Li L Guo Siyuan S Wang Yuanyuan Y Nie Xin X Yang Pengcheng P Ding Ding D Li Beibei B Kang Le L Wang Xianhui X

eLife 20210621

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, <i>Locusta migratoria</i>. By peptidomic analysis and RNAi screening, we identified brain-derived ACP as a key flight-related neuropeptide. <i>ACP</i> gene e ...[more]

PMID: 34151772

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Project description:Desert locusts (Schistocerca gregaria) show an extreme form of phenotypic plasticity and can transform between a cryptic solitarious phase and a swarming gregarious phase. The two phases differ extensively in behavior, morphology and physiology but very little is known about the molecular basis of these differences. We used our recently generated Expressed Sequence Tag (EST) database derived from S. gregaria central nervous system (CNS) to design oligonucleotide microarrays and compare the expression of thousands of genes in the CNS of long-term gregarious and solitarious adult desert locusts. This identified 214 differentially expressed genes, of which 40% have been annotated to date. These include genes encoding proteins that are associated with CNS development and modeling, sensory perception, stress response and resistance, and fundamental cellular processes. Our microarray analysis has identified genes whose altered expression may enable locusts of either phase to deal with the different challenges they face. Genes for heat shock proteins and proteins which confer protection from infection were upregulated in gregarious locusts, which may allow them to respond to acute physiological challenges. By contrast the longer-lived solitarious locusts appear to be more strongly protected from the slowly accumulating effects of ageing by an upregulation of genes related to anti-oxidant systems, detoxification and anabolic renewal. Gregarious locusts also had a greater abundance of transcripts for proteins involved in sensory processing and in nervous system development and plasticity. Gregarious locusts live in a more complex sensory environment than solitarious locusts and may require a greater turnover of proteins involved in sensory transduction, and possibly greater neuronal plasticity. Two condition experiment: Solitarious central nervous system (CNS) vs gregarious CNS. 6 biological repeats per condition, balanced over 3 male and 3 females samples. The overall experimental design consisted of two identical repeats of an n+2 A-optimal design, organized per sex (n=6 per sex, 3 solitarious - 3 gregarious samples)

Project description:Previous studies of insect flight control have been statistical in approach, simply correlating wing kinematics with body kinematics or force production. Kinematics and forces are linked by Newtonian mechanics, so adopting a dynamics-based approach is necessary if we are to place the study of insect flight on its proper physical footing. Here we develop semi-empirical models of the longitudinal flight dynamics of desert locusts Schistocerca gregaria. We use instantaneous force-moment measurements from individual locusts to parametrize the nonlinear rigid body equations of motion. Since the instantaneous forces are approximately periodic, we represent them using Fourier series, which are embedded in the equations of motion to give a nonlinear time-periodic (NLTP) model. This is a proper mathematical generalization of an earlier linear-time invariant (LTI) model of locust flight dynamics, developed using previously published time-averaged versions of the instantaneous force recordings. We perform various numerical simulations, within the fitted range of the model, and across the range of body angles used by free-flying locusts, to explore the likely behaviour of the locusts upon release from the tether. Solutions of the NLTP models are compared with solutions of the nonlinear time-invariant (NLTI) models to which they reduce when the periodic terms are dropped. Both sets of models are unstable and therefore fail to explain locust flight stability fully. Nevertheless, whereas the measured forces include statistically significant harmonic content up to about the eighth harmonic, the simulated flight trajectories display no harmonic content above the fundamental forcing frequency. Hence, manoeuvre control in locusts will not directly reflect subtle changes in the higher harmonics of the wing beat, but must operate on a coarser time-scale. A state-space analysis of the NLTP models reveals orbital trajectories that are impossible to capture in the LTI and NLTI models, and inspires the hypothesis that asymptotic orbital stability is the proper definition of stability in flapping flight. Manoeuvre control on the scale of more than one wing beat would then consist in exciting transients from one asymptotically stable orbit to another. We summarize these hypotheses by proposing a limit-cycle analogy for flapping flight control and suggest experiments for verification of the limit-cycle control analogy hypothesis.

Dataset Information

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

Publications

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

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