Functional Shifts in Insect microRNA Evolution

Abstract

MicroRNAs (miRNAs) are short endogenous RNA molecules that regulate gene expression at the posttranscriptional level and have been shown to play critical roles during animal development. The identification and comparison of miRNAs in metazoan species are therefore paramount for our understanding of the evolution of body plans. We have characterized 203 miRNAs from the red flour beetle Tribolium castaneum by deep sequencing of small RNA libraries. We can conclude, from a single study, that the Tribolium miRNA set is at least 15% larger than that in the model insect Drosophila melanogaster (despite tens of high-throughput sequencing experiments in the latter). The rate of birth and death of miRNAs is high in insects. Only one-third of the Tribolium miRNA sequences are conserved in D. melanogaster, and at least 18 Tribolium miRNAs are conserved in vertebrates but lost in Drosophila. More than one-fifth of miRNAs that are conserved between Tribolium and Drosophila exhibit changes in the transcription, genomic organization, and processing patterns that lead to predicted functional shifts. For example, 13% of conserved miRNAs exhibit seed shifting, and we describe arm-switching events in 11% of orthologous pairs. These shifts fundamentally change the predicted targets and therefore function of orthologous miRNAs. In general, Tribolium miRNAs are more representative of the insect ancestor than Drosophila miRNAs and are more conserved in vertebrates.

Identification, expression, and molecular evolution of microRNAs in the “living fossil” Triops cancriformis (tadpole shrimp)

“…These results suggest that the miRNAs in each cluster are transcribed from the same transcriptional unit. Next, we compared the compositions of the T. cancriformis miRNA clusters with those of the arthropod D. melanogaster and Tribolium castaneum clusters (Marco et al 2010(Marco et al , 2013. Of the 11 miRNAs clusters of T. cancriformis, the compositions of four (tcf-miR-2a-2/2a/13/2b/ 71, tcf-miR-305/275, tcf-miR-92a/92b, tcf-let-7/miR-100) were (partly) conserved relative to those of D. melanogaster, whereas the compositions of five clusters (tcf-miR-2a-2/2a/ 13/2b/71, tcf-miR-2788/193, tcf-miR-305/275, tcf-miR-92a/ 92b, and tcf-let-7/miR-100) were (partly) conserved relative to those of Tribolium castaneum.…”

Fast-evolving microRNAs are highly expressed in the early embryo of Drosophila virilis

“…We found evidence of expression for 117 of the 131 computationally predicted homologs of D. melanogaster microRNAs. In addition, using a conservative pipeline for microRNA annotation previously established in our lab (Marco et al 2010), we identified 13 candidate novel microRNAs unique to the virilis-repleta group (Supplemental Fig. S2).…”

“…Some D. melanogaster microRNAs are members of widely conserved animal microRNA families; however, a substantial fraction of its microRNA complement is lineage-or speciesspecific. For example, fruit flies (Diptera) and beetles (Coleoptera) diverged ∼300 mya (Wiegmann et al 2009) and share only one-third of their microRNA gene set, with the remaining microRNAs emerging after their split (Marco et al 2010).…”

Evolution of the Mir-155 Family and Possible Targets in Cancers and the Immune System

“…Zero means that mature sequences are produced at equal levels from both arms (Marco et al, 2010). Targets were predicted by miRDB (Wienholds et al, 2005), and "-" indicate there was no data available (WangToomey et al, 2011;Zhi-Yong et al, 2011;CorstenPapageorgiou et al, 2012;MattiskeSuetani et al, 2012).…”

“…To quantify the relative amount of mature miRNA products from each arm of the same miRNAhairpin precursor, we performed the ''relative arm usage'' measure as reported (Marco et al, 2010). The quantity of relative arm usage was calculated as follows: Relative arm usage=log 2 (N 5 '/N 3 '); where N 5 ' is the number of reads mapped to the 5' arm of the hairpin precursor and N3' the number of reads from the 3' arm.…”