Background Eukaryotic 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. Results We 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. Conclusions Decondensation 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.

Summary Light regulates major plant developmental transitions by orchestrating a series of nuclear events. This study uncovers the molecular function of the natural variant, TZP (Tandem Zinc-finger-Plus3), as a novel signal integrator of light and photoperiodic pathways in transcriptional nuclear foci. We report that TZP acts as a positive regulator of photoperiodic flowering via physical interactions with the red-light receptor phytochrome B (phyB). We demonstrate that TZP localizes in dynamic nuclear domains regulated by light quality and photoperiod. This study shows that phyB is indispensible not only for localizing TZP to transcriptionally active nuclear photobodies, but also for recruiting TZP on the promoter of the floral inducer FLOWERING LOCUS T (FT). Our findings signify a unique transcriptional regulatory role to the highly enigmatic plant nuclear photobodies, where TZP directly activates FT gene expression and promotes flowering.

Intrinsically disordered proteins can adopt multiple conformations, thereby enabling interaction with a wide variety of partners. They often serve as hubs in protein interaction networks. We have previously shown that the Histone Deacetylase Complex 1 (HDC1) protein from Arabidopsis (Arabidopsis thaliana) interacts with histone deacetylases and quantitatively determines histone acetylation levels, transcriptional activity, and several phenotypes, including abscisic acid sensitivity during germination, vegetative growth rate, and flowering time. HDC1-type proteins are ubiquitous in plants, but they contain no known structural or functional domains. Here, we explored the protein interaction spectrum of HDC1 using a quantitative bimolecular fluorescence complementation assay in tobacco (Nicotiana benthamiana) epidermal cells. In addition to binding histone deacetylases, HDC1 directly interacted with histone H3-binding proteins and corepressor-associated proteins but not with H3 or the corepressors themselves. Surprisingly, HDC1 also was able to interact with variants of the linker histone H1. Truncation of HDC1 to the ancestral core sequence narrowed the spectrum of interactions and of phenotypic outputs but maintained binding to a H3-binding protein and to H1. Thus, HDC1 provides a potential link between H1 and histone-modifying complexes.Regulation of gene transcription underpins plant development and dynamic responses to the environment. Transcription occurs in the context of chromatin, a highly condensed structure in which the DNA is wrapped around nucleosomes composed of histones H2A/B, H3, and H4 and further stabilized by linker histone H1 (Over and Michaels, 2014;Hergeth and Schneider, 2015). Alteration of chromatin structure plays an important part in transcriptional regulation and is achieved through multiprotein complexes that recognize and instigate biochemical modifications of the DNA and/or the histones (Pfluger and Wagner, 2007;Derkacheva et al., 2013). For example, binding of repressors to so-called corepressors recruits histone deacetylases (HDAs) to the gene region (Song et al., 2005). The HDAs in turn interact with histonebinding proteins (Mehdi et al., 2016). Removal of acetyl groups from Lys residues of the core histones leads to chromatin compaction and inhibition of transcription (Kouzarides, 2007;Roudier et al., 2009). Specific recruitment at both 'ends' of the repressive protein complex generates a double lock between DNA and the nucleosome: the repressors recognize certain DNA motifs in the gene promoters, and the histone-binding proteins recognize ('read') certain histone residues and their modifications (Liu et al., 2010). A minimal HDAC complex therefore needs to combine at least three protein functions: repressor binding, histone binding, and catalytic activity. Biochemical studies in yeast (Saccharomyces cerevisiae) and in animal systems have provided evidence for large multiprotein complexes linking a corepressor and a HDA with several histone-binding proteins and a range of associate...