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Sequence and structural properties of circular RNAs in the brain of nurse and forager honeybees (Apis mellifera).

ABSTRACT: BACKGROUND:The honeybee (Apis mellifera) represents a model organism for social insects displaying behavioral plasticity. This is reflected by an age-dependent task allocation. The most protruding tasks are performed by young nurse bees and older forager bees that take care of the brood inside the hive and collect food from outside the hive, respectively. The molecular mechanism leading to the transition from nurse bees to foragers is currently under intense research. Circular RNAs, however, were not considered in this context so far. As of today, this group of non-coding RNAs was only known to exist in two other insects, Drosophila melanogaster and Bombyx mori. Here we complement the state of circular RNA research with the first characterization in a social insect. RESULTS:We identified numerous circular RNAs in the brain of A. mellifera nurse bees and forager bees using RNA-Seq with exonuclease enrichment. Presence and circularity were verified for the most abundant representatives. Back-splicing in honeybee occurs further towards the end of transcripts and in transcripts with a high number of exons. The occurrence of circularized exons is correlated with length and CpG-content of their flanking introns. The latter coincides with increased DNA-methylation in the respective loci. For two prominent circular RNAs the abundance in worker bee brains was quantified in TaqMan assays. In line with previous findings of circular RNAs in Drosophila, circAmrsmep2 accumulates with increasing age of the insect. In contrast, the levels of circAmrad appear age-independent and correlate with the bee's task. Its parental gene is related to amnesia-resistant memory. CONCLUSIONS:We provide the first characterization of circRNAs in a social insect. Many of the RNAs identified here show homologies to circular RNAs found in Drosophila and Bombyx, indicating that circular RNAs are a common feature among insects. We find that exon circularization is correlated to DNA-methylation at the flanking introns. The levels of circAmrad suggest a task-dependent abundance that is decoupled from age. Moreover, a GO term analysis shows an enrichment of task-related functions. We conclude that circular RNAs could be relevant for task allocation in honeybee and should be investigated further in this context.

SUBMITTER: Tholken C

PROVIDER: S-EPMC6347836 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Sequence and structural properties of circular RNAs in the brain of nurse and forager honeybees (Apis mellifera).

Thölken Clemens C Thamm Markus M Erbacher Christoph C Lechner Marcus M

BMC genomics 20190125 1

<h4>Background</h4>The honeybee (Apis mellifera) represents a model organism for social insects displaying behavioral plasticity. This is reflected by an age-dependent task allocation. The most protruding tasks are performed by young nurse bees and older forager bees that take care of the brood inside the hive and collect food from outside the hive, respectively. The molecular mechanism leading to the transition from nurse bees to foragers is currently under intense research. Circular RNAs, howe ...[more]

PMID: 30683059

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Project description:The honeybee brain is comprised of a nervous system that sufficiently regulates this life transition. Knowledge about how protein phosphorylation functions in regards to the neurobiological activities in the honeybee brain to drive the age-specific labor division is still lacking. Protein phosphorylation, the most common post-translational modification (PTM), is a key switch for rapid on-off control of signaling cascades that regulate cell differentiation and development, enzyme activity and metabolic maintenance in living cells. A fundamental mechanism for regulating signaling network and protein activity is the covalent PTM of serine (Ser), threonine (Thr), and tyrosine (Tyr) residues with phosphate. Fortunately, because of advances in phosphopeptide enrichment and improvements in mass spectrometry (MS) instrumentation and methods, phosphoproteomics has enabled large-scale identification of protein phosphorylation sites and phosphorylation networks in biological samples. Although the proteome has been mapped in the brain of nurse and forager bees, knowledge about age-specific effects of phosphorylation regulation on proteins in the honeybee brain is still lacking. Moreover, information in regards to the honeybee phosphoproteome is also very limited. Only very recently, in-depth phosphoproteomics analyses of protein phosphorylation networks in the hypopharyngealgland of the honeybee have been reported. Although the phosphoproteome analyses during the development of brood and salivary glands has been reported, only very limited proteins were phosphorylated and phosphorylation sites of those phosphoproteins were not assigned. Therefore, a comprehensive characterization of phosphoproteomics and changes in the brains of nurse and forager bees is key to understand the phosphorylation events underlying age-specific physiology to achieve the completion of biological missions in this well-organized social community of the honeybee. Honeybee (A. m. ligustica) colonies used for sampling were raised at the apiary of the Institute of Apicultural Research, Chinese Academy of Agricultural Science, Beijing. Newly emerged (<12 h after emergence) worker bees were marked on their thoraxes and placed back into the colonies to develop and then the marked nurse and forager bees were collected on days 10 and 20, respectively. There were 150 bees sampled from each of the five colonies which have queens at the same age. In brief, for each time point, worker bees were sampled from five colonies, and pooled all samples for further analysis. This procedure was repeated three times, so that we finally ended up with three independent biological replicates per time point, each consisting of 150 honeybees. Then their brains were dissected, and the brain samples were pooled and stored at −80 °C for further analysis. All the colonies were managed with almost identical population, food, and brood during the nectar flow of chaste berry (Vitexnegundo L.) in June.

Dataset Information

Sequence and structural properties of circular RNAs in the brain of nurse and forager honeybees (Apis mellifera).

Publications

Sequence and structural properties of circular RNAs in the brain of nurse and forager honeybees (Apis mellifera).

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