Metabolomic analysis reveals that carnitines are key regulatory metabolites in phase transition of the locusts

Abstract

Phenotypic plasticity occurs prevalently and plays a vital role in adaptive evolution. However, the underlying molecular mechanisms responsible for the expression of alternate phenotypes remain unknown. Here, a density-dependent phase polyphenism of Locusta migratoria was used as the study model to identify key signaling molecules regulating the expression of phenotypic plasticity. Metabolomic analysis, using high-performance liquid chromatography and gas chromatography-mass spectrometry, showed that solitarious and gregarious locusts have distinct metabolic profiles in hemolymph. A total of 319 metabolites, many of which are involved in lipid metabolism, differed significantly in concentration between the phases. In addition, the time course of changes in the metabolic profiles of locust hemolymph that accompany phase transition was analyzed. Carnitine and its acyl derivatives, which are involved in the lipid β-oxidation process, were identified as key differential metabolites that display robust correlation with the time courses of phase transition. RNAi silencing of two key enzymes from the carnitine system, carnitine acetyltransferase and palmitoyltransferase, resulted in a behavioral transition from the gregarious to solitarious phase and the corresponding changes of metabolic profiles. In contrast, the injection of exogenous acetylcarnitine promoted the acquisition of gregarious behavior in solitarious locusts. These results suggest that carnitines mediate locust phase transition possibly through modulating lipid metabolism and influencing the nervous system of the locusts.aggregation | metabolic profiling | phase change P henotypic plasticity is the ability of an organism with a single genotype to change its phenotype in response to different environments and is currently seen as an important aspect of adaptation (1-3). Several regulatory mechanisms associated with phenotypic plasticity, including hormonal activity, gene expression, alternative splicing, and DNA methylation, have recently been identified in a number of genetic-model organisms (4, 5). However, the key signaling circuits or regulatory networks mediating the differential expression of plastic phenotypes triggered by environmental cues are still largely unknown, especially in noncanonical study models (6).The migratory locust, Locusta migratoria, a worldwide agricultural pest, displays remarkable phase polyphenism, in which the expression of numerous physiological, morphological, and behavioral traits occurs in response to changes in local population density (7). As one of the striking examples of phenotypic plasticity, locusts provide an ideal model system to study the mechanisms underlying phenotypic plasticity (3). Locust crowding induces the aggregating, more active, and conspicuously colored gregarious phase, whereas isolation leads to the shy, sedentary, and cryptically colored solitarious phase. In addition, phase polyphenism involves variation in many physiological traits, such as immunity, reproduction, and endocrine and energy metab...

Syntaxin 1A modulates the sexual maturity rate and progeny egg size related to phase changes in locusts

“…Since CAT is involved in the lipid b-oxidation process and plays an important role in regulation of behavior change between G and S locusts (Wu et al, 2012), it was selected as representative gene of lipid metabolism to test whether it was involved in modulating reproduction traits between G and S locusts. At the same time, Rheb, which regulates TOR directly, was also selected.…”

“…Evident differences in the body colour, behavior, immunity, metabolism and egg size exist between high-density gregarious (G) and low-density solitarious (S) locusts. We have previously explored the differences in gene expression and biological characteristics between two phase individuals as well as the molecular mechanism of locust phase changes in behavior, metabolomics and immunity response Guo et al, 2013;Jiang et al, 2012;Kang et al, 2004;Ma et al, 2011;Wang et al, 2013;Wu et al, 2012;Yang et al, 2014). However, the molecular mechanism of reproductive trait changes in response to change in population density of migratory locusts is unknown.…”

Cell Metabolomics

“…Cell metabolomics is an emerging field that addresses fundamental biological questions and allows observation of metabolic phenomena in cells. Thus, metabolomics has been used for optimizing cell cultures for antibody production (Wu et al, 2012), testing drugs (Sabidó et al, 2012), cell transfections, determinant of apoptosis, and comparing lung cancer cell phenotypes, identifying novel underlying metabolic pathways (Ward et al, 2011).…”

MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts

“…A number of genes and small RNAs are differentially expressed between solitarious and gregarious locusts (19)(20)(21)(22)(23), indicating that transcriptome reprogramming occurs in response to population Significance Developmental synchrony, resulting from reduced fluctuation in individual development rate, is critical for swarming, migration, and social relationships of colonial animals. However, the molecular regulators of synchronous development are poorly understood.…”