Sequence and Expression Characteristics of Long Noncoding RNAs in Honey Bee Caste Development – Potential Novel Regulators for Transgressive Ovary Size

Abstract

Division of labor in social insect colonies relies on a strong reproductive bias that favors queens. Although the ecological and evolutionary success attained through caste systems is well sketched out in terms of ultimate causes, the molecular and cellular underpinnings driving the development of caste phenotypes are still far from understood. Recent genomics approaches on honey bee developmental biology revealed a set of genes that are differentially expressed genes in larval ovaries and associated with transgressive ovary size in queens and massive cell death in workers. Amongst these, two contigs called special attention, both being over 200 bp in size and lacking apparent coding potential. Herein, we obtained their full cDNA sequences. These and their secondary structure characteristics placed in evidence that they are bona fide long noncoding RNAs (lncRNA) differentially expressed in larval ovaries, thus named lncov1 and lncov2. Genomically, both map within a previously identified QTL on chromosome 11, associated with transgressive ovary size in honey bee workers. As lncov1 was over-expressed in worker ovaries we focused on this gene. Real-time qPCR analysis on larval worker ovaries evidenced an expression peak coinciding with the onset of autophagic cell death. Cellular localization analysis through fluorescence in situ hybridization revealed perinuclear spots resembling omega speckles known to regulate trafficking of RNA-binding proteins. With only four lncRNAs known so far in honey bees, two expressed in the ovaries, these findings open a novel perspective on regulatory factors acting in the fine tuning of developmental processes underlying phenotypic plasticity related to social life histories.

Eusocial insects as emerging models for behavioural epigenetics

“…2a). Although there has not yet been a comprehensive identification of long ncRNAs in any eusocial insect, two long ncRNAs were recently characterized in the honeybee in association with worker ovary size 91 . These preliminary findings suggest that the classes of short and long ncRNAs might constitute yet another layer of epigenetic regulation of caste identity in eusocial insects.…”

RNA-Seq reveals that mitochondrial genes and long non-coding RNAs may play important roles in the bivoltine generations of the non-social Neotropical bee Tetrapedia diversipes

“…These transcripts have recently emerged as critical elements in many genetic regulatory mechanisms including epigenetic regulation DNA imprinting, control of cell pluripotency, transcriptional silencing, and co-activation, among others (Rinn and Chang 2012;Kung et al 2013). In honey bees, for instance, one specific lncRNA, lncov-1, was shown to be associated with programmed cell death in the larval worker ovary (Humann et al 2013).…”

Progress and prospects of noncoding RNAs in insects

“…Moreover, both lncov1 and lncov2 specifically expressed in the ovaries of the honeybees (Sawata et al 2002(Sawata et al , 2004Kiya et al 2008;Tadano et al 2009). Overexpression of lncov1 in the ovaries regulates transgressive ovary size of worker bees (Humann et al 2013). Insect lncRNAs are also reportedly associated with fecundity in N. lugens (Xiao et al 2015) and insecticide resistance (Zhu et al 2017).…”