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Specialization and Evolution of Endogenous Small RNA Pathways

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Specialization and Evolution of Endogenous Small RNA Pathways REVIEWS Specialization and evolution of endogenous small RNA pathways Elisabeth J. Chapman* and James C. Carrington‡ Abstract | The specificity of RNA silencing is conferred by small RNA guides that are processed from structured RNA or dsRNA. The core components for small RNA biogenesis and effector functions have proliferated and specialized in eukaryotic lineages, resulting in diversified pathways that control expression of endogenous and exogenous genes, invasive elements and viruses, and repeated sequences. Deployment of small RNA pathways for spatiotemporal regulation of the transcriptome has shaped the evolution of eukaryotic genomes and contributed to the complexity of multicellular organisms. Genome expansion in higher plants, animals and other and genome-wide deployment of silencing mechanisms multicellular eukaryotes is partially attributed to an is high, it also includes a broader perspective from other increased capacity for the spatiotemporal control of systems. We focus primarily on endogenous regulatory gene expression that is required for development1,2. pathways, with only brief discussions of antiviral silenc- Throughout evolution, protein components of transcrip- ing mechanisms in cases in which they are of particular tional, post-transcriptional and post-translational regula- relevance to the central topic of this Review. tory pathways have proliferated, expanding the potential for regulatory specificity. Proteins that are involved in Diversity of small RNA pathways transcription, for example, represent as much as 10% Early studies of transgene-induced RNA-silencing of the coding sequence in the genomes of metazoans1. phenomena, particularly in plants, revealed puzzling By contrast, specificity for RNA-mediated silencing- differences in the molecular and epigenetic properties based regulation is conferred by small RNA guides (for that are associated with silencing in distinct individuals3. example, microRNAs (miRNAs), small interfering RNAs In some cases, silencing was associated with DNA (siRNAs) and Piwi-interacting RNAs (piRNAs)) that methylation of promoter regions and transcriptional are generated through distinct biogenesis pathways and repression whereas, in other cases, it was associated function with specialized effector proteins (members with high levels of transcription of targeted loci but low of the Argonaute (AGO)–Piwi family). Therefore, the stability of the resulting transcripts. In retrospect, it is evolution of the RNA-mediated silencing mechanism obvious that many of these differences resulted from the as a regulatory device in multicellular organisms has entry of trigger loci or transcripts into distinct silenc- involved a proliferation of small RNA biogenesis and ing pathways that evolved through proliferation and effector proteins, and the de novo formation, prolifera- specialization of a basic set of modules4,5. The core mech- tion and refinement of small RNA guides. How have the anism, as revealed through pioneering studies in worms, core biogenesis and effector modules proliferated and flies, plants and other eukaryotic models, is triggered by *Department of Biology, specialized to generate diverse regulatory pathways? perfect or near-perfect dsRNA that is processed into Myers Hall, 915 East Third How have new specificities emerged, and how has RNA small RNA duplexes by RNaseIII-like enzymes6–10. The Street, Indiana University, silencing been integrated into regulatory networks? diversity of RNA silencing modules is therefore reflected Bloomington, Indiana 47405, USA. Here, we review the diverse functions of the basic in distinct types of trigger loci, and in biogenesis and ‡Center for Genome Research RNA silencing modules, focusing on three areas in effector factors that form and use distinct classes of and Biocomputing, 3021 ALS, which regulatory proliferation and functional special- small RNA (TABLE 1). Oregon State University, ization has occurred: diversification and specialization Corvallis, Oregon 97331, USA. of small-RNA-processing factors, proliferation and spe- Diversity of small-RNA-generating loci Correspondence to J.C.C. e-mail: carrington@cgrb. cialization of effectors, and de novo evolution of small There are several types of loci that generate functional oregonstate.edu RNA regulators. Although much of the evidence dis- small RNAs. Some form precursor transcripts that doi:10.1038/nrg2179 cussed here refers to plant systems, in which the diversity adopt secondary structures with Dicer substrate activity, 884 | noVEMber 2007 | VOLUME 8 www.nature.com/reviews/genetics © 2007 Nature Publishing Group REVIEWS Table 1 | Classes of small RNA identified in eukaryotes. Class Description Biogenesis and genomic origin Function miRNA MicroRNA Processing of foldback miRNA gene transcripts by members Post-transcriptional regulation of transcripts of the Dicer and RNaseIII-like families from a wide range of genes Primary Small interfering Processing of dsRNA or foldback RNA by members of the Binding to complementary target RNA; guide siRNA RNA Dicer family for initiation of RdRP-dependent secondary siRNA synthesis Secondary Small interfering RdRP activity at silenced loci (Caenorhabditis elegans); Post-transcriptional regulation of transcripts; siRNA RNA processing of RdRP-derived long dsRNA or long foldback formation and maintenance of heterochromatin RNA by members of the Dicer family (Arabidopsis thaliana) tasiRNA Trans-acting miRNA-dependent cleavage and RdRP-dependent conversion Post-transcriptional regulation of transcripts siRNA of TAS gene transcripts to dsRNA, followed by Dicer processing natsiRNA Natural antisense Dicer processing of dsRNA arising from sense- and Post-transcriptional regulation of genes transcript-derived antisense-transcript pairs involved in pathogen defense and stress siRNA responses in plants piRNA Piwi-interacting A biogenesis mechanism is emerging, which is Suppression of transposons and retroelements RNA Argonaute-dependent but Dicer-independent in the germ lines of flies and mammals RdRP, RNA-dependent RNA polymerase. and do not require RNA-dependent RNA polymerase Small RNA from bidirectional transcripts. Transcription (RdRP) or amplification mechanisms. Other loci form from opposing promoters can yield dsRNA (FIG. 1b). For small RNAs after the primary transcripts are processed example, the 5′ untranslated region (UTR) of the human through dsRNA-forming mechanisms that involve LINE1 (L1) element contains promoters that support inter- RdRP activity. Yet other loci yield small RNAs through nal bidirectional transcription, and L1-specific siRNAs non-RdRP-dependent amplification mechanisms. that derive from the putative double-stranded region accumulate in cultured cells. Production of L1-specific miRNA loci. miRNAs, which act as post-transcriptional siRNAs is associated with degradation of L1 transcripts regulators of gene expression, are encoded in the and repression of L1 transposition26. genomes of multicellular eukaryotes and unicellular In plants, natural antisense transcript-derived siRNAs plants. miRNAs arise from primary transcripts with self- (natsiRNAs) arise from overlapping transcripts that complementarity that undergo a multistep maturation are induced by abiotic or biotic stress. In two examples process involving specialized RNaseIII-type enzymes, reported to date, stress-induced transcription results in including Dicer11,12. miRNA genes are most often production of dsRNA from which a specific natsiRNA transcribed by RNA polymerase II (PolII), can form arises by the activity of one or more Dicer-like (DCL) in mono- or polycistronic configurations, and occur in proteins27,28. The natsiRNA then guides repression of the both intronic and exonic sequences13,14. In plants and complementary transcript. In some cases, the activity of animals, miRNAs of similar sequence are grouped into natsiRNA is accompanied by production of other small families, the members of which are sometimes regulated RNAs, triggered from the natsiRNA-guided cleavage of differentially and expressed in tissue-specific patterns15. the target transcript27. Computational analysis of natural antisense tran- siRNAs from inverted and direct repeat sequences. scripts (NATs) and small RNA accumulation patterns Endogenous siRNAs can arise from loci that contain in A. thaliana indicates that NAT pairs are not a major direct or inverted repeats, and from dispersed repetitive contributor to small RNA populations in the absence of elements16. Inverted repeats that yield transcripts with stress29. However, natsiRNA accumulation is strongly near-perfect self-complementarity are common in plant induced following relevant stimuli, and NAT pairs are genomes, and often yield heterogeneous siRNA popula- found at more than 7% of the annotated transcriptional tions that do not require an RdRP17,18 (FIG. 1a). Tandem units in the A. thaliana genome27–29. This suggests that direct repeats, such as those at 5S rRNA loci, and all the potential for small RNA production from NAT classes of transposons and retroelements, also spawn pairs in response to general or specific stimuli might be siRNA populations, but these are frequently depend- underestimated. ent on RdRP activity19. The proportion of total small RNA that derives from repeat sequences in Arabidopsis TAS loci. Trans-acting siRNAs (tasiRNAs) arise in plants thaliana is relatively high, although this overrepresen- from specific TAS loci (FIG. 1c). TAS transcripts are PolII- tation is reduced when the proportion is adjusted to dependent,
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