Dataset Information

Differential Odour Coding of Isotopomers in the Honeybee Brain.

ABSTRACT: The shape recognition model of olfaction maintains that odorant reception probes physicochemical properties such as size, shape, electric charge, and hydrophobicity of the ligand. Recently, insects were shown to distinguish common from deuterated isotopomers of the same odorant, suggesting the involvement of other molecular properties to odorant reception. Via two-photon functional microscopy we investigated how common and deuterated isoforms of natural odorants are coded within the honeybee brain. Our results provide evidence that (i) different isotopomers generate different neuronal activation maps, (ii) isotopomer sensitivity is a general mechanism common to multiple odorant receptors, and (iii) isotopomer specificity is highly consistent across individuals. This indicates that honeybee's olfactory system discriminates between isotopomers of the same odorant, suggesting that other features, such as molecular vibrations, may contribute to odour signal transduction.

SUBMITTER: Paoli M

PROVIDER: S-EPMC4762004 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Differential Odour Coding of Isotopomers in the Honeybee Brain.

Paoli Marco M Anesi Andrea A Antolini Renzo R Guella Graziano G Vallortigara Giorgio G Haase Albrecht A

Scientific reports 20160222

The shape recognition model of olfaction maintains that odorant reception probes physicochemical properties such as size, shape, electric charge, and hydrophobicity of the ligand. Recently, insects were shown to distinguish common from deuterated isotopomers of the same odorant, suggesting the involvement of other molecular properties to odorant reception. Via two-photon functional microscopy we investigated how common and deuterated isoforms of natural odorants are coded within the honeybee bra ...[more]

PMID: 26899989

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Project description:Learning and memory-related skills that honeybees use for navigation, foraging and other activities are associated with a central region of the brain, the mushroom bodies, which are relatively more developed in workers than in queens. During larval period, however, the differential feeding offered to prospective queens promotes faster brain development and higher expression of several neurogenic genes (ataxin-2, cryptocephal, dachshund, Eph Receptor, fax, shot, krüppel homolog-1 and tetraspanin 5D). It seems that in some point during pupation there happens a shift in this trend. In fact, queen’s brain experiences net cell death rates while worker’s brain is favored by higher rates of cell proliferation, resulting in caste specific brains. Here we report on transcriptomic results which might represent the molecular underpinnings of the differential brain development between castes. Genome-wide expression analyses using oligonucleotide microarray approach show an opposite pattern to that observed during larval development, with workers’ brain with higher transcription levels of 324 genes (e.g., mesencephalic astrocyte derived neurotrophic factor, minibrain, signal peptide peptidase, and tumbleweed, all associated to neurogenic events or cell death prevention). This suggests that somehow the respective gene products promote differential development of honeybee brain. MANF, for example, a gene superexpressed in workers’ brain, encodes a protein with a domain homologous to SAP Ku70 C-terminal domain. Since this molecule is an inhibitor of apoptotic protein Bax, MANF is a candidate to act as an anti-apoptotic factor during worker brain development (extensive cell death events characterize queens’ pupal brain). Minibrain encodes a protein-kinase involved in regulating cell division during post-embryonic neurogenesis, and is another candidate to participate in the mechanism responsible for the reversing the brain size/body volume rate between queens and workers. Moreover, we assessed by RT-qPCR the transcription profile of the ecdysone receptor (which mediates ecdysteroid action and is probably involved in differential brain cell death/proliferation between castes) variants A and B in three time points during pupal development. Our results suggest the existence of a hormone/receptor threshold above which (hormone excess), in queens, it would be triggered more cell death than proliferation events, which through the differential participation of effector genes, would lead to the morphological differences between adult queens’ and workers’ brain.

Project description:The differential feeding regimes experienced by the queen and worker larvae of the honeybee Apis mellifera shape a complex endocrine response cascade that ultimately gives rise to differences in brain morphologies. Brain development analyzed at the morphological level from the third (L3) through fifth (L5) larval instars revealed an asynchrony between queens and workers. In the feeding phase of the last larval instar (L5F), two well-formed structures, pedunculi and calyces, are identifiable in the mushroom bodies of queens, both of which are not present in workers until a later phase (spinning phase, L5S). Genome-wide expression analyses and normalized transcript expression experiments monitoring specific genes revealed that this differential brain development starts earlier, during L3. Analyzing brains from L3 through L5S1 larvae, we identified 21 genes with caste-specific transcription patterns (e.g., APC-4, GlcAT-P, fax, kr-h1 and shot), which encode proteins that are potentially involved in the development of brain tissues through controlling the cell proliferation rate (APC4, kr-h1) and fasciculation (GlcAT-P, fax, and shot). Shot, whose expression is known to be required for axon extension and cell proliferation, was found to be transcribed at significantly higher levels in L4 queens compared with worker larvae. Moreover, the protein encoded by this gene was immunolocalized to the cytoplasm of cells near the antennal lobe neuropiles and proximal to the Kenyon cells in the brains of L4 queens. In conclusion, during the larval period, the brains of queens are larger and develop more rapidly than workers' brains, which represents a developmental heterochrony reflecting the effect of the differential feeding regime of the two castes on nervous system development. Furthermore, this differential development is characterized by caste-specific transcriptional profiles of a set of genes, thus pointing to a link between differential nutrition and differential neurogenesis via genes that control cell proliferation and fasciculation.

Project description:Background and aims: The Asian honeybee (Apis cerana) and the European honeybee (Apis mellifera) are reproductively isolated. Previous studies reported that exchanging the larval food between the two species, known as nutritional crossbreeding, resulted in obvious changes in morphology, physiology and behavior. This study explored the molecular mechanisms underlying the honeybee nutritional crossbreeding. Methods: This study used full nutritional crossbreeding technology to rear A. cerana queens by feeding them with an A. mellifera royal jelly-based diet in an incubator. The body color and the expression of certain genes, microRNA, lncRNA, and circRNA among nutritional crossbred A. cerana queens (NQ), and control A. cerana queens (CQ) were compared. The biological functions of two target genes, TPH1 and KMO, were verified using RNA interference. Results: Our results showed that the NQ's body color turned yellow compared to the black control queens. Whole transcriptome sequencing results showed that a total of 1484, 311, 92, and 169 DEGs, DElncRNAs, DEmiRNAs, and DEcircRNAs, respectively, were identified in NQ and CQ, in which seven DEGs were enriched for three key pathways (tryptophan, tyrosine, and dopamine) involved in melanin synthesis. Interestingly, eight DElncRNAs and three DEmiRNAs were enriched into the key pathways regulating the above key DEGs. No circRNAs were enriched into these key pathways. Knocking down two key genes (KMO and TPH1) resulted in altered body color, suggesting that feeding NQ's an RNAi-based diet significantly downregulated the expression of TPH1 and KMO in 4-day-old larvae, which confirmed the function of key DEGs in the regulation of honeybee body color. Conclusion: These findings reveal that the larval diets from A. mellifera could change the body color of A. cerana, perhaps by altering the expression of non-coding RNAs and related key genes. This study serves as a model of epigenetic regulation in insect body color induced by environmental factors.

Dataset Information

Differential Odour Coding of Isotopomers in the Honeybee Brain.

Publications

Differential Odour Coding of Isotopomers in the Honeybee Brain.

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