Abstract

BackgroundEukaryotic genomes are partitioned into euchromatic and heterochromatic domains to regulate gene expression and other fundamental cellular processes. However, chromatin is dynamic during growth and development and must be properly re-established after its decondensation. Small interfering RNAs (siRNAs) promote heterochromatin formation, but little is known about how chromatin regulates siRNA expression.ResultsWe demonstrate that thousands of transposable elements (TEs) produce exceptionally high levels of siRNAs in Arabidopsis thaliana embryos. TEs generate siRNAs throughout embryogenesis according to two distinct patterns depending on whether they are located in euchromatic or heterochromatic regions of the genome. siRNA precursors are transcribed in embryos, and siRNAs are required to direct the re-establishment of DNA methylation on TEs from which they are derived in the new generation. Decondensed chromatin also permits the production of 24-nt siRNAs from heterochromatic TEs during post-embryogenesis, and siRNA production from bipartite-classified TEs is controlled by their chromatin states.ConclusionsDecondensation of heterochromatin in response to developmental, and perhaps environmental, cues promotes the transcription and function of siRNAs in plants. Our results indicate that chromatin-mediated siRNA transcription provides a cell-autonomous homeostatic control mechanism to help reconstitute pre-existing chromatin states during growth and development including those that ensure silencing of TEs in the future germ line.

Highlights

  • Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains to regulate gene expression and other fundamental cellular processes

  • Our results indicate that chromatin-mediated small interfering RNAs (siRNAs) transcription provides a cell-autonomous homeostatic control mechanism to help reconstitute pre-existing chromatin states during growth and development including those that ensure silencing of transposable elements (TEs) in the future germ line

  • We previously focused on the ~ 21-nt microRNA class of small RNAs involved in post-transcriptional regulation [39], but noticed that the vast majority of TE-derived small RNAs were 24nt long and highly enriched in embryos compared to floral bud or leaf tissues (Fig. 1b and Additional file 2: Figure S1A)

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Summary

Introduction

Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains to regulate gene expression and other fundamental cellular processes. Small interfering RNAs (siRNAs) promote heterochromatin formation, but little is known about how chromatin regulates siRNA expression. Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains [1, 2]. Heterochromatin formation is promoted by various pathways including those affecting covalent modifications of histones, which package DNA into nucleosomes, as well as cytosine methylation [5,6,7]. Little is known about how heterochromatin-promoting pathways respond to labile chromatin states shortly after fertilization to help reestablish euchromatic and heterochromatic states

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