scholarly journals Diversification of small RNA amplification mechanisms for targeting transposon-related sequences in ciliates

2019 ◽  
Vol 116 (29) ◽  
pp. 14639-14644 ◽  
Author(s):  
Masatoshi Mutazono ◽  
Tomoko Noto ◽  
Kazufumi Mochizuki
Keyword(s):  
Transposable Elements ◽  
Small Rna ◽  
Signal Amplification ◽  
Small Rnas ◽  
Ciliated Protozoa ◽  
Rna Amplification ◽  
Somatic Nucleus ◽  
Dna Elimination ◽  
Internal Eliminated Sequences ◽  
Rna Biogenesis

The silencing of repetitive transposable elements (TEs) is ensured by signal amplification of the initial small RNA trigger, which occurs at distinct steps of TE silencing in different eukaryotes. How such a variety of secondary small RNA biogenesis mechanisms has evolved has not been thoroughly elucidated. Ciliated protozoa perform small RNA-directed programmed DNA elimination of thousands of TE-related internal eliminated sequences (IESs) in the newly developed somatic nucleus. In the ciliate Paramecium, secondary small RNAs are produced after the excision of IESs. In this study, we show that in another ciliate, Tetrahymena, secondary small RNAs accumulate at least a few hours before their derived IESs are excised. We also demonstrate that DNA excision is dispensable for their biogenesis in this ciliate. Therefore, unlike in Paramecium, small RNA amplification occurs before IES excision in Tetrahymena. This study reveals the remarkable diversity of secondary small RNA biogenesis mechanisms, even among ciliates with similar DNA elimination processes, and thus raises the possibility that the evolution of TE-targeting small RNA amplification can be traced by investigating the DNA elimination mechanisms of ciliates.

scholarly journals Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

2021 ◽  
Author(s):  
Jaemyung Choi ◽  
David Bruce Lyons ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Small Rna ◽  
Histone H3 ◽  
Histone H1 ◽  
Dna Methyltransferases ◽  
Flowering Plants ◽  
Genomic Sequences ◽  
Rna Molecules ◽  
Rna Biogenesis

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically required for small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

scholarly journals Analysis of RDR1/RDR2/RDR6-independent small RNAs in Arabidopsis thaliana improves MIRNA annotations and reveals novel siRNA loci

2017 ◽  
Author(s):  
Seth Polydore ◽  
Michael J. Axtell
Keyword(s):  
Gene Expression ◽  
Arabidopsis Thaliana ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Seq ◽  
Triple Mutant ◽  
Physiological Mechanisms ◽  
Protein Coding ◽  
Regulate Gene Expression ◽  
Rna Biogenesis

SummaryPlant small RNAs regulate key physiological mechanisms through post-transcriptional and transcriptional silencing of gene expression. sRNAs fall into two major categories: those that are reliant on RNA Dependent RNA Polymerases (RDRs) for biogenesis and those that aren’t. Known RDR-dependent sRNAs include phased and repeat-associated short interfering RNAs, while known RDR-independent sRNAs are primarily microRNAs and other hairpin-derived sRNAs. In this study, we produced and analyzed small RNA-seq libraries from rdr1/rdr2/rdr6 triple mutant plants. Only a small fraction of all sRNA loci were RDR1/RDR2/RDR6-independent; most of these were microRNA loci or associated with predicted hairpin precursors. We found 58 previously annotated microRNA loci that were reliant on RDR1, −2, or −6 function, casting doubt on their classification. We also found 38 RDR1/2/6-independent small RNA loci that are not MIRNAs or otherwise hairpin-derived, and did not fit into other known paradigms for small RNA biogenesis. These 38 small RNA-producing loci have novel biogenesis mechanisms, and are frequently located in the vicinity of protein-coding genes. Altogether, our analysis suggest that these 38 loci represent one or more new types of small RNAs in Arabidopsis thaliana.Significance StatementSmall RNAs regulate gene expression in plants and are produced through a variety of previously-described mechanisms. Here, we examine a set of previously undiscovered small RNA-producing loci that are produced by novel mechanisms.

scholarly journals Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis

2020 ◽  
Author(s):  
Meetali Singh ◽  
Eric Cornes ◽  
Blaise Li ◽  
Piergiuseppe Quarato ◽  
Loan Bourdon ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Embryonic Development ◽  
Rna Polymerase ◽  
Codon Usage ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Dependent Rna Polymerase ◽  
Coding Sequences ◽  
Germ Granules ◽  
Rna Biogenesis

In the Caenorhabditis elegans germline, thousands of mRNAs are concomitantly expressed with antisense 22G-RNAs, which are loaded into the Argonaute CSR-1. Despite their essential functions for animal fertility and embryonic development, how CSR-1 22G-RNAs are produced remains unknown. Here, we show that CSR-1 slicer activity is primarily involved in triggering the synthesis of small RNAs on the coding sequences of germline mRNAs and post-transcriptionally regulates a fraction of targets. CSR-1-cleaved mRNAs prime the RNA-dependent RNA polymerase, EGO-1, to synthesize 22G-RNAs in phase with ribosome translation in the cytoplasm, in contrast to other 22G-RNAs mostly synthesized in germ granules. Moreover, codon optimality and efficient translation antagonize CSR-1 slicing and 22G-RNAs biogenesis. We propose that codon usage differences encoded into mRNA sequences might be a conserved strategy in eukaryotes to regulate small RNA biogenesis and Argonaute targeting.

scholarly journals A miniature inverted-repeat transposable element, AddIn-MITE, located inside a WD40 gene is conserved in Andropogoneae grasses

PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e6080
Author(s):  
Clicia Grativol ◽  
Flavia Thiebaut ◽  
Sara Sangi ◽  
Patricia Montessoro ◽  
Walaci da Silva Santos ◽  
...  
Keyword(s):  
Transposable Elements ◽  
Transposable Element ◽  
Small Rna ◽  
Genome Assembly ◽  
Inverted Repeat ◽  
Small Rnas ◽  
Distribution Patterns ◽  
Plant Genomes ◽  
Sugarcane Genome

Miniature inverted-repeat transposable elements (MITEs) have been associated with genic regions in plant genomes and may play important roles in the regulation of nearby genes via recruitment of small RNAs (sRNA) to the MITEs loci. We identified eight families of MITEs in the sugarcane genome assembly with MITE-Hunter pipeline. These sequences were found to be upstream, downstream or inserted into 67 genic regions in the genome. The position of the most abundant MITE (Stowaway-like) in genic regions, which we call AddIn-MITE, was confirmed in a WD40 gene. The analysis of four monocot species showed conservation of the AddIn-MITE sequence, with a large number of copies in their genomes. We also investigated the conservation of the AddIn-MITE’ position in the WD40 genes from sorghum, maize and, in sugarcane cultivars and wild Saccharum species. In all analyzed plants, AddIn-MITE has located in WD40 intronic region. Furthermore, the role of AddIn-MITE-related sRNA in WD40 genic region was investigated. We found sRNAs preferentially mapped to the AddIn-MITE than to other regions in the WD40 gene in sugarcane. In addition, the analysis of the small RNA distribution patterns in the WD40 gene and the structure of AddIn-MITE, suggests that the MITE region is a proto-miRNA locus in sugarcane. Together, these data provide insights into the AddIn-MITE role in Andropogoneae grasses.

scholarly journals Histone H1 prevents non-CG methylation-mediated small RNA biogenesis in Arabidopsis heterochromatin

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Jaemyung Choi ◽  
David B Lyons ◽  
Daniel Zilberman
Keyword(s):  
Dna Methylation ◽  
Transposable Elements ◽  
Small Rna ◽  
Histone H3 ◽  
Histone H1 ◽  
Dna Methyltransferases ◽  
Flowering Plants ◽  
Genomic Sequences ◽  
Rna Molecules ◽  
Rna Biogenesis

Flowering plants utilize small RNA molecules to guide DNA methyltransferases to genomic sequences. This RNA-directed DNA methylation (RdDM) pathway preferentially targets euchromatic transposable elements. However, RdDM is thought to be recruited by methylation of histone H3 at lysine 9 (H3K9me), a hallmark of heterochromatin. How RdDM is targeted to euchromatin despite an affinity for H3K9me is unclear. Here we show that loss of histone H1 enhances heterochromatic RdDM, preferentially at nucleosome linker DNA. Surprisingly, this does not require SHH1, the RdDM component that binds H3K9me. Furthermore, H3K9me is dispensable for RdDM, as is CG DNA methylation. Instead, we find that non-CG methylation is specifically associated with small RNA biogenesis, and without H1 small RNA production quantitatively expands to non-CG methylated loci. Our results demonstrate that H1 enforces the separation of euchromatic and heterochromatic DNA methylation pathways by excluding the small RNA-generating branch of RdDM from non-CG methylated heterochromatin.

scholarly journals RNA-mediated nucleosome depletion is required for elimination of transposon-derived DNA.

2022 ◽  
Author(s):  
Aditi Singh ◽  
Xyrus X. Maurer-Alcalá ◽  
Therese Solberg ◽  
Silvan Gisler ◽  
Michael Ignarski ◽  
...  
Keyword(s):  
Transposable Elements ◽  
Chromatin Remodeling ◽  
Dna Cleavage ◽  
Small Rnas ◽  
Heterochromatin Formation ◽  
Dna Accessibility ◽  
Dna Elimination ◽  
Nucleosome Density ◽  
Somatic Genome ◽  
Genomic Regions

Small RNAs are known to mediate silencing of transposable elements and other genomic loci, increasing nucleosome density and preventing undesirable gene expression. Post-zygotic development of the Paramecium somatic genome requires elimination of thousands of transposon remnants (IESs) and transposable elements that are scattered throughout the germline genome (Garnier et al. 2004). The elimination process is guided by Piwi-associated small RNAs and leads to precise cleavage at IES boundaries (Bouhouche et al. 2011; Furrer et al. 2017). Previous research suggests that small RNAs induce heterochromatin formation within IESs, which, in turn, is required for DNA elimination (Liu et al. 2007). Here we show that IES recognition and precise excision is facilitated by recruitment of a homolog of a chromatin remodeler ISWI, which depletes target genomic regions of nucleosomes, making the chromatin accessible for DNA cleavage. ISWI knockdown in Paramecium leads to pronounced inhibition of DNA elimination. Furthermore, nucleosome profiling indicates that ISWI is required for IES elimination in nucleosome-dense genomic regions, while other IESs do not require small RNAs or ISWI for excision. ISWI silencing notably also reduces DNA elimination precision, resulting in aberrant excision at alternative IES boundaries. In summary, we demonstrate that chromatin remodeling that increases DNA accessibility together with small RNAs are necessary for efficient and precise DNA elimination in Paramecium.

scholarly journals Whats, hows and whys of programmed DNA elimination in Tetrahymena

Open Biology ◽  
2017 ◽  
Vol 7 (10) ◽  
pp. 170172 ◽  
Author(s):  
Tomoko Noto ◽  
Kazufumi Mochizuki
Keyword(s):  
Small Rna ◽  
Small Rnas ◽  
Feedback Loop ◽  
Tetrahymena Thermophila ◽  
Repetitive Sequences ◽  
Genome Comparison ◽  
High Similarity ◽  
Dna Elimination ◽  
Elimination Mechanism ◽  
Key Questions

Programmed genome rearrangements in ciliates provide fascinating examples of flexible epigenetic genome regulations and important insights into the interaction between transposable elements (TEs) and host genomes. DNA elimination in Tetrahymena thermophila removes approximately 12 000 internal eliminated sequences (IESs), which correspond to one-third of the genome, when the somatic macronucleus (MAC) differentiates from the germline micronucleus (MIC). More than half of the IESs, many of which show high similarity to TEs, are targeted for elimination in cis by the small RNA-mediated genome comparison of the MIC to the MAC. Other IESs are targeted for elimination in trans by the same small RNAs through repetitive sequences. Furthermore, the small RNA–heterochromatin feedback loop ensures robust DNA elimination. Here, we review an updated picture of the DNA elimination mechanism, discuss the physiological and evolutionary roles of DNA elimination, and outline the key questions that remain unanswered.

scholarly journals High-Level Accumulation of Exogenous Small RNAs Not Affecting Endogenous Small RNA Biogenesis and Function in Plants

2014 ◽  
Vol 13 (5) ◽  
pp. 1017-1023
Author(s):  
Wan-xia SHEN ◽  
Neil A Smith ◽  
Chang-yong ZHOU ◽  
Ming-bo WANG
Keyword(s):  
Small Rna ◽  
Small Rnas ◽  
Rna Biogenesis ◽  
High Level ◽  
And Function

scholarly journals Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis

2020 ◽  
Author(s):  
Germano Cecere ◽  
Meetali Singh ◽  
Eric Cornes ◽  
Blaise Li ◽  
Piergiuseppe Quarato ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Embryonic Development ◽  
Rna Polymerase ◽  
Codon Usage ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Dependent Rna Polymerase ◽  
Coding Sequences ◽  
Germ Granules ◽  
Rna Biogenesis

Abstract In the Caenorhabditis elegans germline, thousands of mRNAs are concomitantly expressed with antisense 22G-RNAs, which are loaded into the Argonaute CSR-1. Despite their essential functions for animal fertility and embryonic development, how CSR-1 22G-RNAs are produced remains unknown. Here, we show that CSR-1 slicer activity is primarily involved in triggering the synthesis of small RNAs on the coding sequences of germline mRNAs and post-transcriptionally regulates a fraction of targets. CSR-1-cleaved mRNAs prime the RNA-dependent RNA polymerase, EGO-1, to synthesize 22G-RNAs in phase with ribosome translation in the cytoplasm, in contrast to other 22G-RNAs mostly synthesized in germ granules. Moreover, codon optimality and efficient translation antagonize CSR-1 slicing and 22G-RNAs biogenesis. We propose that codon usage differences encoded into mRNA sequences might be a conserved strategy in eukaryotes to regulate small RNA biogenesis and Argonaute targeting.

scholarly journals Fidelity in RNA-based recognition of transposable elements

2018 ◽  
Vol 373 (1762) ◽  
pp. 20180168 ◽  
Author(s):  
Ilaria Ugolini ◽  
Mario Halic
Keyword(s):  
Transposable Elements ◽  
Small Rna ◽  
Small Rnas ◽  
Rna Degradation ◽  
Current Data ◽  
Theme Issue ◽  
Rna Pathways ◽  
Transposon Insertions

Genomes are under constant threat of invasion by transposable elements and other genomic parasites. How can host genomes recognize these elements and target them for degradation? This requires a system that is highly adaptable, and at the same time highly specific. Current data suggest that perturbation of transcription patterns by transposon insertions could be detected by the RNAi surveillance pathway. Multiple transposon insertions might generate sufficient amounts of primal small RNAs to initiate generation of secondary small RNAs and silencing. At the same time primal small RNAs need to be constantly degraded to reduce the level of noise small RNAs below the threshold required for initiation of silencing. Failure in RNA degradation results in loss of fidelity of small RNA pathways and silencing of ectopic targets. This article is part of the theme issue ‘5′ and 3′ modifications controlling RNA degradation’.

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