Genome-wide characterization of long intergenic non-coding RNAs (lincRNAs) provides new insight into viral diseases in honey bees Apis cerana and Apis mellifera

Abstract

BackgroundLong non-coding RNAs (lncRNAs) are a class of RNAs that do not encode proteins. Recently, lncRNAs have gained special attention for their roles in various biological process and diseases.ResultsIn an attempt to identify long intergenic non-coding RNAs (lincRNAs) and their possible involvement in honey bee development and diseases, we analyzed RNA-seq datasets generated from Asian honey bee (Apis cerana) and western honey bee (Apis mellifera). We identified 2470 lincRNAs with an average length of 1011 bp from A. cerana and 1514 lincRNAs with an average length of 790 bp in A. mellifera. Comparative analysis revealed that 5 % of the total lincRNAs derived from both species are unique in each species. Our comparative digital gene expression analysis revealed a high degree of tissue-specific expression among the seven major tissues of honey bee, different from mRNA expression patterns. A total of 863 (57 %) and 464 (18 %) lincRNAs showed tissue-dependent expression in A. mellifera and A. cerana, respectively, most preferentially in ovary and fat body tissues. Importantly, we identified 11 lincRNAs that are specifically regulated upon viral infection in honey bees, and 10 of them appear to play roles during infection with various viruses.ConclusionsThis study provides the first comprehensive set of lincRNAs for honey bees and opens the door to discover lincRNAs associated with biological and hormone signaling pathways as well as various diseases of honey bee.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1868-7) contains supplementary material, which is available to authorized users.

Genome-wide identification of long non-coding RNAs and their regulatory networks involved in Apis mellifera ligustica response to Nosema ceranae infection

“…For example, lncRNA plays pivotal roles in controlling the stressresponse in plants including Populus [80] and wheat [30]. Jayakodi et al identified 15 long intergenic non-coding RNAs (lincRNAs) showing significant differential expression between sacbrood virus (SBV)-infected and uninfected Apis cerana, and further confirmed the expression of 11 lincRNAs using RT-qPCR [38]. In this work, the expression levels of 111 and 146 lncRNAs were observed to significantly alter in N.…”

“…Utilizing transcriptome sequencing, Jayakodi et al [38] identified 1514 long intergenic non-coding RNAs (lincRNAs) in A. mellifera and 2470 lincRNAs in Apis cerana, most of which had a tissue-specific expression pattern. More recently, Chen et al [39] predicted a variety of lncRNAs, miRNAs and mRNAs during the ovary activation, oviposition inhibition and oviposition recovery processes; and they further found 73 differentially expressed genes and 14 differentially expressed lncRNAs (DElncRNAs) located in the QTL region, which may be candidate genes responsible for ovary size and oviposition.…”

Identification and comparison of long non‐coding RNAs in the silk gland between domestic and wild silkworms

“…Although lncRNAs are widely identified in some insect species with the application of RNA‐seq technology (Etebari et al ., ; Jayakodi et al ., ; Jenkins et al ., ; Legeai & Derrien, ; Xiao et al ., ; Chen et al ., ; Wu et al ., ), the information about lncRNAs in the silkworm is relatively rare. A previous study suggested that nine silk gland‐enriched ncRNAs may be involved in the development of silk gland and fibroin synthesis (Li et al ., ).…”

Origin and evolution of the metazoan non-coding regulatory genome: Insights from the sponge Amphimedon queenslandica

“…In mice, many lncRNAs are essential for normal development and survival (Anderson et al, 2016;Goff et al, 2015;Sauvageau et al, 2013). Developmentally expressed lncRNAs have also been identified in C. elegans (Nam and Bartel, 2012), Drosophila and other insects (Brown et al, 2014;Chen et al, 2016a;Jayakodi et al, 2015;Jenkins et al, 2015;Wu et al, 2016;Young et al, 2012), and echinoderms (Mu et al, 2016). In contrast, the systematic investigation of lncRNAs in non-bilaterian metazoans has been lagging behind ( Fig.…”

“…However, lncRNAs are rapidly evolving and exhibit poor primary sequence similarity between species; orthologues are difficult to identify (Ulitsky, 2016), thus precluding a detailed understanding of their functionality in an evolutionary developmental framework. In fact, while the role of lncRNAs in the regulation of developmental gene activity appears to be widespread amongst animals (Bråte et al, 2015;Brown et al, 2014;Chen et al, 2016a;Forouzmand et al, 2016;Gaiti et al, 2015;Jayakodi et al, 2015;Jenkins et al, 2015;Mu et al, 2016;Nam and Bartel, 2012;Necsulea et al, 2014;Pauli et al, 2012;Sauvageau et al, 2013;Tan et al, 2013;Ulitsky et al, 2011;Wu et al, 2016;Young et al, 2012), only a handful of lncRNAs have thus far been shown to function in evolutionarily divergent animals, mostly restricted to bilaterians (Grant et al, 2012;Heard et al, 1999;Migeon et al, 1999;Ulitsky et al, 2011).…”