Systematic characterization of small RNAome during zebrafish early developmental stages

Yao, Yuangen; Ma, Lili; Jia, Qiong; Deng, Wankun; Liu, Zexian; Zhang, Yuan‐Wei; Ren, Jian; Xue, Yu; Jia, Haibo

doi:10.1186/1471-2164-15-117

Cited by 22 publications

(32 citation statements)

References 48 publications

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“…For example, a previous study showed that dre-let-7a and dre-miR-22a were among the top five most abundant miRNA families expressed in early zebrafish development. 36 Similarly, with a previous study, dre-let-7 and dre-miR-22a were highly expressed in zebrafish spermatozoa in our results. Also, dre-miR-430b, which facilitates the MZT by the clearance of maternal mRNAs, was identified in this study.…”

Section: Discussionsupporting

confidence: 91%

“…Previous analysis of miRNAs showed that 218 known miRNAs and 25 novel miRNAs were detected during eight distinct stages of early zebrafish development by sRNA-seq technology. 36 Wei et al reported that 198 known miRNAs and 8 novel were identified during zebrafish early development. 37 In this study, we identified 400 novel and 204 known miRNAs.…”

Section: Discussionmentioning

confidence: 99%

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Identification of MicroRNAs in Zebrafish Spermatozoa

et al. 2015

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MicroRNAs (miRNAs) participate in almost all biological processes. Plenty of evidences show that some testis- or spermatozoa-specific miRNAs play crucial roles in the process of gonad and germ cell development. In this study, the spermatozoa miRNA profiles were investigated through a combination of illumina deep sequencing and bioinformatics analysis in zebrafish. Deep sequencing of small RNAs yielded 11,820,680 clean reads. By mapping to the zebrafish genome, we identified 400 novel and 204 known miRNAs that could be grouped into 104 families. Furthermore, we selected the six highest expressions of known miRNAs to detect their expression patterns in different tissues by stem-loop quantitative real-time polymerase chain reaction. We found that among the six miRNAs, dre-miR-202-5p displayed specific and high expression in zebrafish spermatozoa and testis. Fluorescence in situ hybridization analysis indicated that dre-miR-202-5p was predominantly expressed in all kind of germ cells at different spermatogenetic stages, including spermatogonia and spermatozoa, but barely expressed in the germ cells in the ovary. This sex-biased expression pattern suggests that dre-miR-202-5p might be related to spermatogenesis and the functioning of spermatozoa. The identification of miRNAs in zebrafish spermatozoa and germ cells offers new insights into the spermatogenesis and spermatozoa in the teleost and other vertebrates.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Identification of MicroRNAs in Zebrafish Spermatozoa

et al. 2015

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“…The unexpected differences in the RNAi repertoire of bilaterians, cnidarians, ctenophores and sponges uncovered here, suggests that while the last common ancestor of extant animals employed miRNA, piRNA and endo-siRNA systems, these were not integrated into the shared ancestral gene regulatory system. This is in contrast to bilaterians, which in general appear to use a common RNAi system [10][11][12][13][14][15][16]. Following the emergence of these major metazoan RNAi pathways, lineage-specific evolutionary trajectories appear to have resulted in divergent RNAi strategies evolving in each basal metazoan lineage.…”

Section: Discussionmentioning

confidence: 95%

“…There are some marked differences in the miRNA systems of sponges, cnidarians and bilaterians. In contrast to bilaterians, which express a complex repertoire of miRNAs in somatic tissues [10][11][12][13][14][15][16], miRNA expression in cnidarians is consistently dwarfed by piRNAs [2,[17][18][19]. The miRNAs of the cnidarian Nematostella vectensis, while capable of bilaterian-like silencing [20], also regularly silence their targets through extensive base pairing followed by cleavage, as observed in plants, rather than by transcript destabilisation or translational inhibition [19].…”

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confidence: 99%

Diverse RNA interference strategies in early-branching metazoans

Calcino

Taft

Degnan

2018

Preprint

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Background: Micro RNAs (miRNAs) and piwi interacting RNAs (piRNAs), along with the more ancient eukaryotic endogenous small interfering RNAs (endo-siRNAs) constitute the principal components of the RNA interference (RNAi) repertoire of most animals. RNAi in non-bilaterians -sponges, ctenophores, placozoans and cnidarians -appears to be more diverse than that of bilaterians, and includes structurally variable miR-NAs in sponges, an enormous number of piRNAs in cnidarians and the absence of miRNAs in ctenophores and placozoans. Results:Here we identify thousands of endo-siRNAs and piRNAs from the sponge Amphimedon queenslandica, the ctenophore Mnemiopsis leidyi and the cnidarian Nematostella vectensis using a computational approach that clusters mapped small RNA sequences and annotates each cluster based on the read length and relative abundance of the constituent reads. This approach was validated on 11 small RNA libraries in Drosophila melanogaster, demonstrating the successful annotation of RNAi associated loci with properties consistent with previous reports. In the non-bilaterians we uncover seven new miRNAs from Amphimedon and four from Nematostella as well as sub-populations of candidate cis-natural antisense transcript (cis-NAT) endo-siRNAs. In the ctenophore, the absence of miRNAs is confirmed and an abundance of endo-siRNAs is revealed. Analysis of putative piRNA structure suggests that conserved localised secondary structures in primary transcripts may be important for the production of mature piRNAs in Amphimedon and Nematostella, as is also the case for endo-siRNAs. Conclusion:Together, these findings suggest that the last common ancestor of animals did not have the entrained RNAi system that typifies bilaterians. Instead it appears that bilaterians, cnidarians, ctenophores and sponges express unique repertoires and combinations of miRNAs, piRNAs and endo-siRNAs. ABSTRACT 2 BACKGROUND RNA interference (RNAi) evolved prior to the divergence of extant eukaryotic lineages, possibly in response to threats from parasitic double-stranded RNA species such as retroviruses and transposons [1]. In contemporary animals, three independent RNAi systems comprise the bulk of the small RNA (sRNA) repertoire: micro RNAs (miRNAs); Piwi interacting RNAs (piRNAs); and endogenous small interfering RNAs (endo-siRNAs). Amongst non-bilaterian animals -sponges, cnidarians ctenophores and placozoans -miRNAs appear to be lost in latter two lineages, with placozoans and ctenophores also lacking key miRNA biogenic enzymes [2][3][4]. The absence of miRNAs in the sister lineages to the animal kingdom, choanoflagellates, and fungi [2,5,6], suggests the miRNA system has been lost or evolved independently multiple times [7]. Nonetheless, animal miRNAs play fundamental roles in cell type differentiation and maintenance, and their emergence and proliferation is linked to the evolution of complex multicellularity [8]. The prevalence of miRNAs in plants and algae [9] lends further support to the hypothesis that miRNAs may be important regu...

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“…However, a good approximation can be obtained by examining miRNA sequencing data from whole animals at different developmental stages and complementing this with expression data of individual miRNAs. For example, sequencing data from whole embryos or larvae of C. elegans and zebrafish (Kato et al, 2009;Yao et al, 2014) show that a small fraction of miRNAs is highly abundant during at least one developmental stage, whereas the majority seems to be expressed at low levels (Fig. 3).…”

Section: Many Mirnas May Act At the Periphery Of Developmentmentioning

confidence: 99%

A framework for understanding the roles of miRNAs in animal development

2017

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MicroRNAs (miRNAs) contribute to the progressive changes in gene expression that occur during development. The combined loss of all miRNAs results in embryonic lethality in all animals analyzed, illustrating the crucial role that miRNAs play collectively. However, although the loss of some individual miRNAs also results in severe developmental defects, the roles of many other miRNAs have been challenging to uncover. This has been mostly attributed to their proposed function as tuners of gene expression or providers of robustness. Here, we present a view of miRNAs in the context of development as a hierarchical and canalized series of gene regulatory networks. In this scheme, only a fraction of embryonic miRNAs act at the top of this hierarchy, with their loss resulting in broad developmental defects, whereas most other miRNAs are expressed with high cellular specificity and play roles at the periphery of development, affecting the terminal features of specialized cells. This view could help to shed new light on our understanding of miRNA function in development, disease and evolution.

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Systematic characterization of small RNAome during zebrafish early developmental stages

Cited by 22 publications

References 48 publications

Identification of MicroRNAs in Zebrafish Spermatozoa

Identification of MicroRNAs in Zebrafish Spermatozoa

Diverse RNA interference strategies in early-branching metazoans

A framework for understanding the roles of miRNAs in animal development

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