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Differences in sNPF receptor-expressing neurons in brains of fire ant (Solenopsis invicta Buren) worker subcastes: indicators for division of labor and nutritional status?

ABSTRACT: In the red imported fire ant, Solenopsis invicta Buren, the neuronal and molecular mechanisms related to worker division of labor are poorly understood. Workers from different subcastes (major, medium and minors) perform different tasks, which are loosely associated with their size. We hypothesized that the short neuropeptide F (sNPF) signaling system (NPY-like) could be involved in mechanisms of worker division of labor and sensing or responding to colony nutritional requirements. Thus, we investigated the expression of the short neuropeptide F receptor (sNPFR) in the brain and subesophageal ganglion (SEG) of workers from colonies with and without brood. Across worker subcastes a total of 9 clusters of immunoreactive sNPFR cells were localized in the brain and the subesophageal ganglion (SEG); some of these cells were similar to those observed previously in the queen. Worker brain sNPFR cell clusters were found in the protocerebrum near mushroom bodies, in the central complex and in the lateral horn. Other sNPFR immunoreactive cells were found at the edge of the antennal lobes. Across subcastes, we observed both a constant and a differential pattern of sNPFR clusters, with a higher number of sNPFR cells found in minor than in major workers. Those sNPFR cells detected in all worker subcastes appear to be involved in olfaction or SEG functions. The differential expression of clusters in subcastes suggests that sNPFR signaling is involved in regulating behaviors associated with specific subcastes and thus, division of labor. Some sNPFR cells appear to be involved in nutrient sensing and/or brood care, feeding behavior and locomotion. In colonies without brood, workers showed a lower cluster number, and an overall reduced sNPFR signal. Our results suggest the sNPF signaling system is a candidate for the neurobiological control of worker division of labor and sensing brood presence, perhaps correlating with protein requirements and availability.

SUBMITTER: Castillo P

PROVIDER: S-EPMC3869854 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Project description:Neuropeptides and their receptors play vital roles in controlling the physiology and behavior of animals. Short neuropeptide F (sNPF) signaling regulates several physiological processes in insects such as feeding, locomotion, circadian rhythm and reproduction, among others. Previously, the red imported fire ant (Solenopsis invicta) sNPF receptor (S. invicta sNPFR), a G protein-coupled receptor, was immunolocalized in queen and worker brain and queen ovaries. Differential distribution patterns of S. invicta sNPFR protein in fire ant worker brain were associated both with worker subcastes and with presence or absence of brood in the colony. However, the cognate ligand for this sNPFR has not been characterized and attempts to deorphanize the receptor with sNPF peptides from other insect species which ended in the canonical sequence LRLRFamide, failed. Receptor deorphanization is an important step to understand the neuropeptide receptor downstream signaling cascade. We cloned the full length cDNA of the putative S. invicta sNPF prepropeptide and identified the putative "sNPF" ligand within its sequence. The peptide ends with an amidated Tyr residue whereas in other insect species sNPFs have an amidated Phe or Trp residue at the C-terminus. We stably expressed the HA-tagged S. invicta sNPFR in CHO-K1 cells. Two S. invicta sNPFs differing at their N-terminus were synthesized that equally activated the sNPFR, SLRSALAAGHLRYa (EC50 = 3.2 nM) and SALAAGHLRYa (EC50 = 8.6 nM). Both peptides decreased the intracellular cAMP concentration, indicating signaling through the Gαi-subunit. The receptor was not activated by sNPF peptides from other insect species, honey bee long NPF (NPY) or mammalian PYY. Further, a synthesized peptide otherwise identical to the fire ant sequence but in which the C-terminal amidated amino acid residue 'Y' was switched to 'F', failed to activate the sNPFR. This discovery will now allow us to investigate the function of sNPY and its cognate receptor in fire ant biology.

Project description:BACKGROUND: Insect neuropeptides are involved in diverse physiological functions and can be released as neurotransmitters or neuromodulators acting within the central nervous system, and as circulating neurohormones in insect hemolymph. The insect short neuropeptide F (sNPF) peptides, related to the vertebrate neuropeptide Y (NPY) peptides, have been implicated in the regulation of food intake and body size, and play a gonadotropic role in the ovaries of some insect species. Recently the sNPF peptides were localized in the brain of larval and adult Drosophila. However, the location of the sNPF receptor, a G protein-coupled receptor (GPCR), has not yet been investigated in brains of any adult insect. To elucidate the sites of action of the sNPF peptide(s), the sNPF receptor tissue expression and cellular localization were analyzed in queens of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera), an invasive social insect. RESULTS: In the queen brains and subesophageal ganglion about 164 cells distributed in distinctive cell clusters (C1-C9 and C12) or as individual cells (C10, C11) were immuno-positive for the sNPF receptor. Most of these neurons are located in or near important sensory neuropils including the mushroom bodies, the antennal lobes, the central complex, and in different parts of the protocerebrum, as well as in the subesophageal ganglion. The localization of the sNPF receptor broadly links the receptor signaling pathway with circuits regulating learning and feeding behaviors. In ovaries from mated queens, the detection of sNPF receptor signal at the posterior end of oocytes in mid-oogenesis stage suggests that the sNPF signaling pathway may regulate processes at the oocyte pole. CONCLUSIONS: The analysis of sNPF receptor immunolocalization shows that the sNPF signaling cascade may be involved in diverse functions, and the sNPF peptide(s) may act in the brain as neurotransmitter(s) or neuromodulator(s), and in the ovaries as neurohormone(s). To our knowledge, this is the first report of the cellular localization of a sNPF receptor on the brain and ovaries of adult insects.

Project description:Purpose: We aimed to provide a basis for the adaptive mechanism and a rich resource for the discovery and identification of novel genes involved in the cold and heat stress response in Solenopsis invicta. retinal transcriptome profiling (RNA-seq) to microarray and quantitative reverse transcription polymerase chain reaction (qRT–PCR) methods and to evaluate protocols for optimal high-throughput data analysis Methods: Solenopsis invicta was reared at lab condition, and incubated at 4 different temperature for 24h (10, 20, 30 and 40℃). RNA was extracted using Trizol reagent and Illumina sequencing was performed at Macrogen. Illumina short reads were quality-filtered and Illumina-based de novo transcriptome assembly was performed. Differential Gene Expression Analysis was studied for different tempearture conditions. Results: Totally 99,085 unigenes was obtained which at least 19,154 were annotated with gene descriptions, gene ontology terms, and metabolic pathways. 86 GO functional sub-groups and 23 EggNOG terms resulted. DEGs with log2FC≥10 were screened and were compared at different temperatures. We found 203, 48 and 66 specific DEGs co-regulated at 10, 20 and 40℃, respectively compare with 30℃. Comparing transcriptome profiles for differential gene expression resulted various DE proteins and genes, including cytochrome P450, NADH dehydrogenase subunit 1, cuticle protein and HSP which have previously been reported to be involved in cold and high temperature resistance. GO analysis revealed that antioxidant activity up-regulated under high temperature stress. Conclusions: we compared the transcriptomes of S. invicta under high- and low-temperature stresses using RNA-Seq technology based on the high-throughput sequencing. Comparative transcriptome analysis identified many genes and a large number of changes were discovered in metabolic pathway through the GO and KEGG enrichment analysis. Our data will facilitate further molecular investigations and genomic research. Many high- and low-temperature significantly up-regulated genes were first identified in this study. These newly found genes may be important and necessary to RIFA overwintering and its behavior for adaptation in new environment as well as quarantine area.

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Differences in sNPF receptor-expressing neurons in brains of fire ant (Solenopsis invicta Buren) worker subcastes: indicators for division of labor and nutritional status?

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