Fast-evolving microRNAs are highly expressed in the early embryo of <i>Drosophila virilis</i>

Ninova, Maria; Ronshaugen, Matthew; Griffiths-Jones, Sam

doi:10.1261/rna.041657.113

Cited by 41 publications

(72 citation statements)

References 76 publications

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“…The evolution of the pan-Drosophilid mir-309/3/286/4/5/6-1,2,3 (i.e., mir-306 6) cluster was recently examined by Griffiths-Jones and colleagues, and our analysis agrees with theirs for the species analyzed (Ninova et al 2014). We extended this analysis by identifying proto-mir-309 clusters in two ant species, for which none of the resident miRNAs had been previously annotated (Fig.…”

Section: Acquisition Of Multiple Seed Family Classes In the Eight Memsupporting

confidence: 88%

Diverse modes of evolutionary emergence and flux of conserved microRNA clusters

Mohammed

Siepel

Lai

2014

RNA

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Many animal miRNA loci reside in genomic clusters that generate multicistronic primary-miRNA transcripts. While clusters that contain copies of the same miRNA hairpin are clearly products of local duplications, the evolutionary provenance of clusters with disparate members is less clear. Recently, it was proposed that essentially all such clusters in Drosophila derived from de novo formation of miRNA-like hairpins within existing miRNA transcripts, and that the maintenance of multiple miRNAs in such clusters was due to evolutionary hitchhiking on a major cluster member. However, this model seems at odds with the fact that many such miRNA clusters are composed of well-conserved miRNAs. In an effort to trace the birth and expansion of miRNA clusters that are presently well-conserved across Drosophilids, we analyzed a broad swath of metazoan species, with particular emphasis on arthropod evolution. Beyond duplication and de novo birth, we highlight a diversity of modes that contribute to miRNA evolution, including neofunctionalization of miRNA copies, fissioning of locally duplicated miRNA clusters, miRNA deletion, and miRNA cluster expansion via the acquisition and/or neofunctionalization of miRNA copies from elsewhere in the genome. In particular, we suggest that miRNA clustering by acquisition represents an expedient strategy to bring cohorts of target genes under coordinate control by miRNAs that had already been individually selected for regulatory impact on the transcriptome.

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Section: Acquisition Of Multiple Seed Family Classes In the Eight Memsupporting

confidence: 88%

Diverse modes of evolutionary emergence and flux of conserved microRNA clusters

Mohammed

Siepel

Lai

2014

RNA

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“…It has been shown in Drosophila that the miR-309 cluster could promote mRNA turnover during the maternal-to-zygotic transition and, thus, lead to reduced survival and delayed larval development (18). Here, our results have demonstrated that miR-309 acts to initiate ovarian development appropriately in the mosquito A. aegypti.…”

Section: Discussionsupporting

confidence: 61%

“…Recently, a fast-evolving miRNA cluster mir-309∼6 has been identified, which is undergoing particularly dynamic evolutionary events within the arthropod lineage, including duplication, gain, and/or loss of miRNA members within it (18). In Drosophila, this miRNA cluster is preferentially expressed in eggs and promotes mRNA turnover during the maternal-to-zygotic transition (19).…”

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confidence: 99%

“…In Drosophila, this miRNA cluster is preferentially expressed in eggs and promotes mRNA turnover during the maternal-to-zygotic transition (19). Interestingly, miR-309, a member of this miRNA cluster, persists and duplicates in a lineage-specific manner against the background of loss of many other miRNA cluster members in the mosquito A. aegypti (18). Generally, fast-evolving genes/miRNAs could drive adaptive evolution with respect to lineage-specific physiology and contribute to species divergence.…”

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confidence: 99%

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microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti

Zhang

Zhao

Roy

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

102

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Obligatory blood-triggered reproductive strategy is an evolutionary adaptation of mosquitoes for rapid egg development. It contributes to the vectorial capacity of these insects. Therefore, understanding the molecular mechanisms underlying reproductive processes is of particular importance. Here, we report that microRNA-309 (miR-309) plays a critical role in mosquito reproduction. A spatiotemporal expression profile of miR-309 displayed its blood feeding-dependent onset and ovary-specific manifestation in female Aedes aegypti mosquitoes. Antagomir silencing of miR-309 impaired ovarian development and resulted in nonsynchronized follicle growth. Furthermore, the genetic disruption of miR-309 by CRISPR/Cas9 system led to the developmental failure of primary follicle formation. Examination of genomic responses to miR-309 depletion revealed that several pathways associated with ovarian development are down-regulated. Comparative analysis of genes obtained from the high-throughput RNA sequencing of ovarian tissue from the miR-309 antagomirsilenced mosquitoes with those from the in silico computation target prediction identified that the gene-encoding SIX homeobox 4 protein (SIX4) is a putative target of miR-309. Reporter assay and RNA immunoprecipitation confirmed that SIX4 is a direct target of miR-309. RNA interference of SIX4 was able to rescue phenotypic manifestations caused by miR-309 depletion. Thus, miR-309 plays a critical role in mosquito reproduction by targeting SIX4 in the ovary and serves as a regulatory switch permitting a stage-specific degradation of the ovarian SIX4 mRNA. In turn, this microRNA (miRNA)-targeted degradation is required for appropriate initiation of a blood feeding-triggered phase of ovarian development, highlighting involvement of this miRNA in mosquito reproduction.Homeobox protein gene | microRNA | CRISPR/Cas9 | ovary | fast evolution T ransmission of mosquito-borne diseases brings enormous human suffering, with more than 1 million deaths worldwide annually. The yellow fever mosquito Aedes aegypti has reemerged as one of the most dangerous vectors of human diseases, transmitting Dengue fever, Yellow fever, Chikungunya, and Zika virus (1-4). Because of the lack of effective vaccines and increasing drug resistance in pathogens, biological control is considered one of the most promising strategies for preventing disease transmission. In particular, female hematophagous mosquitoes rely on acquisition of blood to initiate a series of physiological events promoting egg development (5, 6). Therefore, understanding the molecular mechanisms underlying ovarian activation is of great significance for the development of effective approaches to control mosquito-borne diseases (7,8).MicroRNAs (miRNAs) are small noncoding RNAs that regulate gene expression at the posttranscriptional level through translational repression or mRNA decay (9). Hence, miRNAs play significant roles in governing multiple functions in animals and plants via integrating sophisticated miRNA-mRNA regulatory networks (10, 11...

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“…In addition, the most abundant microRNAs in the beetle oocyte belong to two clusters: mir-279e 2944c and mir-3889 3843. These are diverged homologs of the Drosophila mir-309 6 and mir-994 318 (Ninova et al 2014), whose maternal deposition in Drosophila is modest. The maternal microRNA complement of T. castaneum also contains a number of lineage-specific microRNAs, including the members of the massively duplicated 40 miRNA gene cluster on the X Chromosome, albeit at lower concentrations (Supplemental Table 2).…”

Section: Resultsmentioning

confidence: 99%

MicroRNA evolution, expression, and function during short germband development in Tribolium castaneum

2015

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MicroRNAs are well-established players in the development of multicellular animals. Most of our understanding of microRNA function in arthropod development comes from studies in Drosophila. Despite their advantages as model systems, the long germband embryogenesis of fruit flies is an evolutionary derived state restricted to several holometabolous insect lineages. MicroRNA evolution and expression across development in animals exhibiting the ancestral and more widespread short germband mode of embryogenesis has not been characterized. We sequenced small RNA libraries of oocytes and successive intervals covering the embryonic development of the short germband model organism, Tribolium castaneum. We analyzed the evolution and temporal expression of the microRNA complement and sequenced libraries of total RNA to investigate the relationships with microRNA target expression. We show microRNA maternal loading and sequence-specific 3 ′ end nontemplate oligoadenylation of maternally deposited microRNAs that is conserved between Tribolium and Drosophila. We further uncover large clusters encoding multiple paralogs from several Tribolium-specific microRNA families expressed during a narrow interval of time immediately after the activation of zygotic transcription. These novel microRNAs, together with several early expressed conserved microRNAs, target a significant number of maternally deposited transcripts. Comparison with Drosophila shows that microRNA-mediated maternal transcript targeting is a conserved process in insects, but the number and sequences of microRNAs involved have diverged. The expression of fast-evolving and species-specific microRNAs in the early blastoderm of T. castaneum is consistent with previous findings in Drosophila and shows that the unique permissiveness for microRNA innovation at this stage is a conserved phenomenon.

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

Cited by 41 publications

References 76 publications

Diverse modes of evolutionary emergence and flux of conserved microRNA clusters

Diverse modes of evolutionary emergence and flux of conserved microRNA clusters

microRNA-309 targets the Homeobox gene SIX4 and controls ovarian development in the mosquito Aedes aegypti

MicroRNA evolution, expression, and function during short germband development in Tribolium castaneum

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