Unveiling the Impact of the Genomic Architecture on the Evolution of Vertebrate microRNAs (original) (raw)
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microRNAs (miRNAs) are an abundant class of ~22 nucleotide (nt) regulatory RNAs that are pervasive in higher eukaryotic genomes. In order to fully understand their prominence in genomes, it is necessary to elucidate the molecular mechanisms that can diversify miRNA activities. In this review, we describe some of the many strategies that allow novel miRNA functions to emerge, with particular emphasis on how miRNA genes evolve in animals. These mechanisms include changes in their sequence, processing, or expression pattern; acquisition of miRNA* functionality or antisense processing; and de novo gene birth. The facility and versatility of miRNAs to evolve and change likely underlies how they have become dominant constituents of higher genomes.
The evolution of animal microRNA function
Current Opinion in Genetics & Development, 2007
MicroRNAs (miRNAs) are a large class of small RNAs that function as negative gene regulators in eukaryotes. They regulate diverse biological processes, and bioinformatics data indicate that each miRNA can control hundreds of gene targets, underscoring the potential influence of miRNAs on almost every genetic pathway. In addition to the roles in ontogeny, recent evidence has suggested the possibility that miRNAs have huge impacts on animal phylogeny. The dramatically expanding repertoire of miRNAs and their targets appears to be associated with major body-plan innovations as well as the emergence of phenotypic variation in closely related species. Research in the area of miRNA phylogenetic conservation and diversity suggests that miRNAs play important roles in animal evolution, by driving phenotypic variation during development.
Host gene constraints and genomic context impact the expression and evolution of human microRNAs
Nature Communications, 2016
Increasing evidence has shown that recent miRNAs tend to emerge within coding genes. Here we conjecture that human miRNA evolution is tightly influenced by the genomic context, especially by host genes. Our findings show a preferential emergence of intragenic miRNAs within old genes. We found that miRNAs within old host genes are significantly more broadly expressed than those within young ones. Young miRNAs within old genes are more broadly expressed than their intergenic counterparts, suggesting that young miRNAs have an initial advantage by residing in old genes, and benefit from their hosts' expression control and from the exposure to diverse cellular contexts and target genes. Our results demonstrate that host genes may provide stronger expression constraints to intragenic miRNAs in the long run. We also report associated functional implications, highlighting the genomic context and host genes as driving factors for the expression and evolution of human miRNAs.
Annual Review of Genetics, 2015
Although microRNAs (miRNAs) are among the most intensively studied molecules of the past 20 years, determining what is and what is not a miRNA has not been straightforward. Here, we present a uniform system for the annotation and nomenclature of miRNA genes. We show that fewer than a third of the 1,881 human miRBase entries, and only approximately 16% of the 7,095 metazoan miRBase entries, are robustly supported as miRNA genes. Furthermore, we show that the human repertoire of miRNAs has been shaped by periods of intense miRNA innovation, and that mature gene products show a very different tempo and mode of sequence evolution than star products. We establish a new open access database-MirGeneDB (http://mirgenedb.org)-to catalog this set of robustly supported miRNAs, which complements the efforts of miRBase, but differs from it by annotating the mature versus star products, and by imposing an evolutionary hierarchy upon this curated and consistently named repertoire.
The Expansion of Animal MicroRNA Families Revisited
Life (Basel, Switzerland), 2015
MicroRNAs are important regulatory small RNAs in many eukaryotes. Due to their small size and simple structure, they are readily innovated de novo. Throughout the evolution of animals, the emergence of novel microRNA families traces key morphological innovations. Here, we use a computational approach based on homology search and parsimony-based presence/absence analysis to draw a comprehensive picture of microRNA evolution in 159 animal species. We confirm previous observations regarding bursts of innovations accompanying the three rounds of genome duplications in vertebrate evolution and in the early evolution of placental mammals. With a much better resolution for the invertebrate lineage compared to large-scale studies, we observe additional bursts of innovation, e.g., in Rhabditoidea. More importantly, we see clear evidence that loss of microRNA families is not an uncommon phenomenon. The Enoplea may serve as a second dramatic example beyond the tunicates. The large-scale analys...
Evolution and genomic organization of muscle microRNAs in fish genomes
BMC Evolutionary Biology, 2014
Background: MicroRNAs (miRNAs) are small non-coding RNA molecules with an important role upon post-transcriptional regulation. These molecules have been shown essential for several cellular processes in vertebrates, including muscle biology. Many miRNAs were described as exclusively or highly expressed in skeletal and/or cardiac muscle. However, knowledge on the genomic organization and evolution of muscle miRNAs has been unveiled in a reduced number of vertebrates and mostly only reflects their organization in mammals, whereas fish genomes remain largely uncharted. The main goal of this study was to elucidate particular features in the genomic organization and the putative evolutionary history of muscle miRNAs through a genome-wide comparative analysis of cartilaginous and bony fish genomes.
Well-Annotated microRNAomes Do Not Evidence Pervasive miRNA Loss
Genome biology and evolution, 2018
microRNAs are conserved noncoding regulatory factors implicated in diverse physiological and developmental processes in multicellular organisms, as causal macroevolutionary agents and for phylogeny inference. However, the conservation and phylogenetic utility of microRNAs has been questioned on evidence of pervasive loss. Here, we show that apparent widespread losses are, largely, an artefact of poorly sampled and annotated microRNAomes. Using a curated data set of animal microRNAomes, we reject the view that miRNA families are never lost, but they are rarely lost (92% are never lost). A small number of families account for a majority of losses (1.7% of families account for >45% losses), and losses are associated with lineages exhibiting phenotypic simplification. Phylogenetic analyses based on the presence/absence of microRNA families among animal lineages, and based on microRNA sequences among Osteichthyes, demonstrate the power of these small data sets in phylogenetic inferenc...