Abstract
BackgroundMicroRNAs play a vital role in the regulation of gene expression and have been identified in every animal with a sequenced genome examined thus far, except for the placozoan Trichoplax. The genomic repertoires of metazoan microRNAs have become increasingly endorsed as phylogenetic characters and drivers of biological complexity.ResultsIn this study, we report the first investigation of microRNAs in a species from the phylum Ctenophora. We use short RNA sequencing and the assembled genome of the lobate ctenophore Mnemiopsis leidyi to show that this species appears to lack any recognizable microRNAs, as well as the nuclear proteins Drosha and Pasha, which are critical to canonical microRNA biogenesis. This finding represents the first reported case of a metazoan lacking a Drosha protein.ConclusionsRecent phylogenomic analyses suggest that Mnemiopsis may be the earliest branching metazoan lineage. If this is true, then the origins of canonical microRNA biogenesis and microRNA-mediated gene regulation may postdate the last common metazoan ancestor. Alternatively, canonical microRNA functionality may have been lost independently in the lineages leading to both Mnemiopsis and the placozoan Trichoplax, suggesting that microRNA functionality was not critical until much later in metazoan evolution.
Highlights
MicroRNAs play a vital role in the regulation of gene expression and have been identified in every animal with a sequenced genome examined far, except for the placozoan Trichoplax
Since Dicer and Drosha are both members of the ribonuclease III (RNase III) protein family (Figure 2), we focused our analysis on the RNase III protein domain to better characterize the Mnemiopsis Dicer protein and to yield insight into how, through the evolution of this protein family in the Metazoa, the canonical miRNA biogenesis pathway may have emerged
If poriferans are the most basal metazoan clade, Drosha, Pasha and canonical miRNA functionality must have been lost in the Mnemiopsis lineage (Figure 4b)
Summary
MicroRNAs play a vital role in the regulation of gene expression and have been identified in every animal with a sequenced genome examined far, except for the placozoan Trichoplax. MicroRNAs (miRNAs) are a class of small RNA molecules derived from transcribed mRNA hairpin structures and spliced introns [1,2,3] that play a key role in mRNA targeting, leading to the degradation or translational repression of the target transcript. The regulatory functions of miRNAs are essential to many key biological processes in metazoans, including development, cell growth and death, stem cell maintenance, hematopoiesis, and neurogenesis. The hairpin structures in mRNA transcripts that give rise to primary microRNAs (pri-miRNAs) are not unique to miRNAs or. The canonical miRNA biogenesis pathway in metazoans is part of the larger RNA interference (RNAi) pathway, which includes the closely related siRNA pathway (Figure 1). EXON INTRON EXON transcription Pasha pri-miRNA AAAAAAA cleavage. AAAAAAA EXON EXON splicesome mature splicing mRNA EXON pre-miRNA.
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