Deep experimental profiling of microRNA diversity, deployment, and evolution across the Drosophila genus (original) (raw)
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Large-Scale Annotation and Evolution Analysis of MiRNA in Insects
Genome Biology and Evolution
Insects are among the most diverse and successful groups of animals and exhibit great morphological diversity and complexity. The innovation of wings and metamorphosis are some examples of the fascinating biological evolution of insects. Most microRNAs (miRNAs) contribute to canalization by conferring robustness to gene networks and thus increase the heritability of important phenotypes. Though previous studies have demonstrated how miRNAs regulate important phenotypes, little is still known about miRNA evolution in insects. Here, we used both small RNA-seq data and homology searching methods to annotate the miRNA repertoires of 152 arthropod species, including 135 insects and 17 noninsect arthropods. We identified 16,212 miRNA genes, and classified them into highly conserved (62), insect-conserved (90), and lineage-specific (354) miRNA families. The phylogenetic relationship of miRNA binary presence/absence dynamics implies that homoplastic loss of conserved miRNA families tends to...
New MicroRNAs in Drosophila—Birth, Death and Cycles of Adaptive Evolution
PLoS Genetics, 2014
The origin and evolution of new microRNAs (miRNAs) is important because they can impact the transcriptome broadly. As miRNAs can potentially emerge constantly and rapidly, their rates of birth and evolution have been extensively debated. However, most new miRNAs identified appear not to be biologically significant. After an extensive search, we identified 12 new miRNAs that emerged de novo in Drosophila melanogaster in the last 4 million years (Myrs) and have been evolving adaptively. Unexpectedly, even though they are adaptively evolving at birth, more than 94% of such new miRNAs disappear over time. They provide selective advantages, but only for a transient evolutionary period. After 30 Myrs, all surviving miRNAs make the transition from the adaptive phase of rapid evolution to the conservative phase of slow evolution, apparently becoming integrated into the transcriptional network. During this transition, the expression shifts from being tissue-specific, predominantly in testes and larval brain/gonads/imaginal discs, to a broader distribution in many other tissues. Interestingly, a measurable fraction (20-30%) of these conservatively evolving miRNAs experience ''evolutionary rejuvenation'' and begin to evolve rapidly again. These rejuvenated miRNAs then start another cycle of adaptiveconservative evolution. In conclusion, the selective advantages driving evolution of miRNAs are themselves evolving, and sometimes changing direction, which highlights the regulatory roles of miRNAs.
Genome …, 2011
Since the initial annotation of miRNAs from cloned short RNAs by the Ambros, Tuschl, and Bartel groups in 2001, more than a hundred studies have sought to identify additional miRNAs in various species. We report here a meta-analysis of short RNA data from Drosophila melanogaster, aggregating published libraries with 76 data sets that we generated for the modENCODE project. In total, we began with more than 1 billion raw reads from 187 libraries comprising diverse developmental stages, specific tissue- and cell-types, mutant conditions, and/or Argonaute immunoprecipitations. We elucidated several features of known miRNA loci, including multiple phased byproducts of cropping and dicing, abundant alternative 5′ termini of certain miRNAs, frequent 3′ untemplated additions, and potential editing events. We also identified 49 novel genomic locations of miRNA production, and 61 additional candidate loci with limited evidence for miRNA biogenesis. Although these loci broaden the Drosophila miRNA catalog, this work supports the notion that a restricted set of cellular transcripts is competent to be specifically processed by the Drosha/Dicer-1 pathway. Unexpectedly, we detected miRNA production from coding and untranslated regions of mRNAs and found the phenomenon of miRNA production from the antisense strand of known loci to be common. Altogether, this study lays a comprehensive foundation for the study of miRNA diversity and evolution in a complex animal model.
Functional shifts in insect microRNA evolution
Genome Biology and Evolution, 2010
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 highthroughput 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.
Bioinformatics, 2008
Background: MicroRNAs (miRNAs) are small, noncoding RNA molecules that act as posttranscriptional regulators of gene expression. Studies concerning transcriptional regulation of miRNAs have so far concentrated on those located within the intergenic region of the genome and the search for putative promoters, thus leaving open the question of the existence of possible regulatory elements common to all miRNAs including those located in introns of protein coding genes. Results: In this study, we initially searched for motifs occurring in the area 1000 bp upstream from all miRNAs independent of their genomic location. We discovered a previously unknown sequence motif GANNNNGA that displayed a conserved distribution in the nematode worms Caenorhabditis elegans and Caenorhabditis briggsae. This motif had a peak occurrence at 500 bp upstream, with a sharp drop-off toward the miRNA start site. Further analysis indicated that this motif was locally restricted and not enriched 1000-5000 bp upstream or 0-2000 bp downstream of the miRNA start site. In addition, this motif was observed to be most abundant in the upstream sequences of two important miRNAs, mir-1 and mir-124. This abundance was also conserved in phylogenetically distant species including human and mouse. Conclusion: The results show that the motif GANNNNGA is conserved close to miRNA precursor start sites, suggesting that it may be involved in miRNA sequence recognition or regulation. This data provides important knowledge for the identification and computational prediction of miRNA sequences.
Molecular Biology and Evolution, 2020
A striking feature of micro-RNAs is that they are often clustered in the genomes of animals. The functional and evolutionary consequences of this clustering remain obscure. Here, we investigated a micro-RNA cluster miR-6/5/4/286/3/309 that is conserved across drosophilid lineages. Small RNA sequencing revealed expression of this micro-RNA cluster in Drosophila melanogaster leg discs, and conditional overexpression of the whole cluster resulted in leg appendage shortening. Transgenic overexpression lines expressing different combinations of micro-RNA cluster members were also constructed. Expression of individual micro-RNAs from the cluster resulted in a normal wild-type phenotype, but either the expression of several ancient micro-RNAs together (miR-5/4/286/3/309) or more recently evolved clustered micro-RNAs (miR-6-1/2/3) can recapitulate the phenotypes generated by the whole-cluster overexpression. Screening of transgenic fly lines revealed downregulation of leg-patterning gene ca...
Diversity of miRNAs, siRNAs, and piRNAs across 25 Drosophila cell lines
Genome research, 2014
We expanded the knowledge base for Drosophila cell line transcriptomes by deeply sequencing their small RNAs. In total, we analyzed more than 1 billion raw reads from 53 libraries across 25 cell lines. We verify reproducibility of biological replicate data sets, determine common and distinct aspects of miRNA expression across cell lines, and infer the global impact of miRNAs on cell line transcriptomes. We next characterize their commonalities and differences in endo-siRNA populations. Interestingly, most cell lines exhibit enhanced TE-siRNA production relative to tissues, suggesting this as a common aspect of cell immortalization. We also broadly extend annotations of cis-NAT-siRNA loci, identifying ones with common expression across diverse cells and tissues, as well as cell-restricted loci. Finally, we characterize small RNAs in a set of ovary-derived cell lines, including somatic cells (OSS and OSC) and a mixed germline/somatic cell population (fGS/OSS) that exhibits ping-pong p...
The microRNA toolkit of insects
Scientific Reports, 2016
Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth. Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. Previously, miRNA evolution had been linked to morphological complexity, but astonishing variation in the currently available miRNA complements of insects made this link unclear. To address this issue, we sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. Our analyses show that the variation of insect miRNAs is an artefact mainly resulting from poor sampling and inaccurate miRNA annotation, and that insects share a conserved microRNA toolkit of 65 families exhibiting very low variation. For example, the evolutionary shift toward a complete metamorphosis was accompanied only by the acquisition of three and the loss of one miRNA families.
2019
A striking feature of microRNAs is that they are often clustered in the genomes of animals. The functional and evolutionary consequences of this clustering remain obscure. Here, we investigated a microRNA cluster miR-6/5/4/286/3/309 that is conserved across drosophilid lineages. Small RNA sequencing revealed expression of this microRNA cluster in Drosophila melanogaster leg discs, and conditional overexpression of the whole cluster resulted in leg appendage shortening. Transgenic overexpression lines expressing different combinations of microRNA cluster members were also constructed. Expression of individual microRNAs from the cluster resulted in a normal wild-type phenotype, but either the expression of several ancient microRNAs together (miR-5/4/286/3/309) or more recently evolved clustered microRNAs (miR-6-1/2/3) can recapitulate the phenotypes generated by the whole-cluster overexpression. Screening of transgenic fly lines revealed down-regulation of leg patterning gene cassette...