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.
Highlights
Social organization and division of labor within a honey bee colony is characterized by marked physiological, behavioral and morphological differences between the queen and the workers, especially so in the reproductive system [1]
The complex functionalities of long noncoding RNAs (lncRNA) emergent in recent studies, primarily on mammalian model organisms, and the fact that we identified ESTs representing two putative new lncRNAs expressed in a developmental context that is crucial for establishing reproductive division of labor in a social insect [16], we describe their full length cDNA sequence, obtained through 3959 RACE, and their putative secondary structure
As to further investigate this hypothesis, and in the absence of high resolution functional genomics assays for honey bee lncRNAs, we considered that the intracellular localization of lncov1 could provide further hints and serve as a proxy for functionality because many noncoding RNAs exhibit certain specificity with respect to nuclear or cytoplasmatic localization [36]
Summary
Social organization and division of labor within a honey bee colony is characterized by marked physiological, behavioral and morphological differences between the queen and the workers, especially so in the reproductive system [1]. The contigs consisting of two and five ESTs, respectively, were both over 200 bp in size but lacked an apparent coding potential As these expression tags had not been computationally predicted as genes in the Official Gene set 2.0 for the honey bee [1,17] we originally named them according to the genome scaffold they were located in, already considering that they might represent long noncoding RNAs [16]. Long noncoding RNAs (lncRNAs), a class of noncoding RNAs defined by molecular size (.200 nt), have drawn increased attention during the last decade, as in several of the genome sequencing and annotation projects they came to light as a class of genes that may by far exceed the number of protein coding genes [18] As they show little evolutionary conservation, they cannot be predicted by current genome annotation algorithms. Since lncov is expressed in the context of autophagic cell death we further focused on this gene and analyzed its temporal expression profile in larval worker ovaries, as well as its cellular localization by fluorescence in situ hybridization, so as to gain insights into possible functions
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