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MicroRNAs and essential components of the microRNA processing machinery are not encoded in the genome of the ctenophore Mnemiopsis leidyi - PubMed

  • ️Sun Jan 01 2012

MicroRNAs and essential components of the microRNA processing machinery are not encoded in the genome of the ctenophore Mnemiopsis leidyi

Evan K Maxwell et al. BMC Genomics. 2012.

Abstract

Background: MicroRNAs 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.

Results: In 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.

Conclusions: Recent 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.

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Figures

Figure 1
Figure 1

Metazoan miRNA and siRNA pathways. Representation of standard metazoan models for canonical miRNA biogenesis, mirtron biogenesis, and siRNA processing. The Drosha/Pasha protein complex is specific to canonical miRNA biogenesis and initiates cleavage of the primary miRNA (pri-miRNA) from transcribed mRNAs. Intronic miRNAs (mirtrons) bypass cleavage by Drosha/Pasha, generating precursor miRNAs (pre-miRNAs) via intron splicing of mRNAs. The Dicer and Argonaute proteins are responsible for further processing and transport of miRNAs, in addition to short-interfering RNAs (siRNAs) from exogenous sources, resulting in repression of mRNA targets.

Figure 2
Figure 2

Typical domain architectures of Ribonuclease III and Pasha proteins. Members of the Ribonuclease III (RNase III) protein family all contain RNase III protein domains responsible for binding Mg2+ ions that cleave individual strands of dsRNA. The dsRNA binding domain (dsRBD) is common to most RNase III proteins and Pasha. Other common domains found in RNase III class 3 (Dicer) proteins include PAZ, a domain of unknown function (DUF), and a helicase. Pasha contains only tandem dsRBD domains, a domain architecture relatively common in other dsRNA binding proteins within metazoan proteomes.

Figure 3
Figure 3

Evolution of metazoan RNase III domains.a, Cladogram of isolated RNase III domains from metazoan Dicer and Drosha proteins. Mnemiopsis Dicer protein RNase III domains are labeled in red. Bootstrap support values above 45, based on 1000 bootstrap replicates, are displayed on branches with Bayesian probabilities as indicated. See Additional file 7: Table S1 for information on sequence identifiers. b, Scenario for Drosha evolution. Dicer proteins evolved from a duplicated RNase III domain early in eukaryotic evolution. Drosha proteins evolved from a duplicated Dicer protein early in metazoan evolution. White ‘a’ and ‘b’ labels represent RNase IIIa and RNase IIIb domains of Dicer and Drosha proteins, respectively. Green, yellow, pink and blue domains correspond with the clades shown in a.

Figure 4
Figure 4

Scenarios of the evolutionary implications of canonical miRNA functionality absence inMnemiopsis leidyi. a, Ctenophora (represented by M. leidyi) branching earlier than Porifera (represented by A. queenslandica). In this scenario, miRNA functionality likely emerged after the branching of Ctenophora. b, Porifera branching prior to Ctenophora. In this scenario, miRNA functionality coevolved with the Metazoa and was lost from Mnemiopsis leidyi, along with the biogenesis proteins Drosha and Pasha. Also shown are the closest outgroups to the Metazoa with sequenced genomes (i.e., S. arctica, C. owczarzaki, S. rosetta, and M. brevicollis); see Methods for details on the identification of miRNA pathway proteins in these species.

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