Abstract
BackgroundPiwi-interacting RNAs (piRNAs) are a class of short (~26–31-nucleotide) non-protein-coding RNAs expressed in the metazoan germline. The piRNA pathway in arthropods is best understood in the ovary of Drosophila melanogaster, where it acts to silence active transposable elements (TEs). Maternal loading of piRNAs in oocytes is further required for the inheritance of piRNA-mediated transposon defence. However, our understanding of the diversity, evolution and function of the piRNA complement beyond drosophilids is limited. The red flour beetle, Tribolium castaneum, is an emerging model organism separated from Drosophila by ~ 350 million years of evolution that displays a number of features ancestral to arthropods, including short germ embryogenesis. Here, we characterize the maternally deposited and zygotically expressed small RNA and mRNA complements throughout T. castaneum embryogenesis.ResultsWe find that beetle oocytes and embryos of all stages are abundant in heterogeneous ~ 28-nucleotide RNAs. These small RNAs originate from discrete genomic loci enriched in TE sequences and display the molecular signatures of transposon-derived piRNAs. In addition to the maternally loaded primary piRNAs, Tribolium embryos produce secondary piRNAs by the cleavage of zygotically activated TE transcripts via the ping-pong mechanism. The two Tribolium piRNA pathway effector proteins, Tc-Piwi/Aub and Tc-Ago3, are also expressed throughout the soma of early embryos.ConclusionsOur results show that the piRNA pathway in Tribolium is not restricted to the germline, but also operates in the embryo and may act to antagonize zygotically activated transposons. Taken together, these data highlight a functional divergence of the piRNA pathway between insects.
Highlights
Piwi-interacting RNAs are a class of short (~26–31-nucleotide) non-protein-coding RNAs expressed in the metazoan germline
Abundant ~ 28-nt RNAs in T. castaneum embryos display the properties of Piwi-interacting RNAs (piRNAs) Our previous analyses of the abundance and size distribution of small RNA sequencing libraries from T. castaneum oocytes, early embryos before the onset of zygotic transcription (0–5 h), transcriptionally active early blastoderm (8–16 h), differentiating blastoderm (16– 20 h), gastrulation (20–24 h), germband elongation (24– 34 h), fully-extended germband (34–48 h), and late stage development through hatching (2–6 days), revealed that the small RNA population at all developmental stages was dominated by a pool of 26–30-nt long RNAs, peaking at 28 nt [27]
For specific examples of up-regulated transposons targeted by the piRNA pathway in the embryo, we show the small RNA and RNA sequencing data mapped to two piRNA loci encoding transcripts homologous to the LTR retrotransposon gypsy and SARTTc6, a telomeric non-LTR transposon (Fig. 6)
Summary
Piwi-interacting RNAs (piRNAs) are a class of short (~26–31-nucleotide) non-protein-coding RNAs expressed in the metazoan germline. PiRNAs are a class of short non-coding RNAs that associate with the Piwi subfamily of Argonaute proteins and are primarily involved in transcriptional and posttranscriptional silencing of transposable elements (TEs) in the germline of metazoans (reviewed in [1, 2]). Most primary piRNAs derive from longer primary transcripts expressed from specialized, discrete loci in the Drosophila genome known as piRNA clusters, enriched in inactive transposons [3, 7]. PiRNAs and Piwi proteins are components of the maternally deposited pole plasm in the egg, and this deposition is required for the inheritance of the piRNA-mediated transposon response [11,12,13]
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