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Boundary Formation is an Inherent Property of Mobile Small RNA Gradients

ABSTRACT: Small RNAs recently emerged as a new class of mobile instructive signals in development. Here, we investigate their mechanism of action and show that the gradients formed by mobile small RNAs generate sharply defined domains of target gene expression. By modulating the source of artificial miRNAs we show that boundary formation is an inherent property of the small RNA gradient itself. The threshold-based readout of such gradients is highly sensitive to small RNA levels at the source, allowing plasticity in the positioning of a target gene expression boundary. In addition to generating sharp expression domains of their immediate targets, the readouts of opposing small RNA gradients enable formation of stable and uniformly positioned developmental boundaries. These novel patterning properties of small RNAs are reminiscent of those of morphogens in animal systems. However, their exceptionally high specificity, direct mode of action, and the fully intrinsic nature of their gradients, distinguish mobile small RNAs from classical morphogens. Our findings present mobile small RNAs and their targets as highly portable and evolutionarily-tractable regulatory modules through which to create pattern in development and beyond.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE94720 | GEO | 2017/12/01

SECONDARY ACCESSION(S): PRJNA373843

REPOSITORIES: GEO

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Arabidopsis thaliana

Project description:Boundary Formation is an Inherent Property of Mobile Small RNA Gradients

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small RNAs sequences from grafted Arabidopsis thaliana and Nicotiana benthamiana tissues

Project description:A silencing signal in plants with an RNA specificity determinant moves through plasmodesmata and the phloem. To identify the mobile RNA we grafted Arabidopsis thaliana shoots to roots that would be a recipient for the silencing signal. Using high throughput sequencing as a sensitive detection method and mutants to block small RNA (sRNA) biogenesis in either source or recipient tissue, we detected endogenous and transgene specific sRNA that moved across the graft union. Surprisingly we found that the mobile endogenous sRNAs account for a substantial proportion of the sRNA in roots and we provide evidence that 24nt mobile sRNAs direct epigenetic modifications in the genome of the recipient cells. Mobile sRNA thus represents a mechanism for transmitting the specification of epigenetic modification and could affect genome defence and responses to external stimuli that have persistent effects in plants. Keywords: Small RNA Analysis, Epigenetics

2010-03-24 | GSE20663 | GEO

small RNAs sequences from grafted Arabidopsis thaliana and Nicotiana benthamiana tissues

2010-03-24 | E-GEOD-20663 | biostudies-arrayexpress

Mobile PEAR transcription factors integrate hormone and miRNA cues to prime cambial growth

Project description:In addition to apical growth, plants undergo radial growth to increase girth, a particularly prominent feature in trees. During both apical and radial growth the phytohormones auxin and cytokinins form symmetries that govern further growth patterns. But whereas the gene regulatory networks interpreting the hormonal fields during apical growth are well established, such networks are not known for the radial growth. We show here that the initiation of radial growth occurs around early protophloem sieve element (PSE) cell files of the root procambial tissue in Arabidopsis. In this domain cytokinin signalling promotes expression of a pair of novel mobile transcription factors, PHLOEM EARLY DOF (PEAR1, PEAR2) and their four homologs (OBP2, DOF6, TMO6 and HCA2), collectively called PEAR proteins. The PEAR proteins form a short-range concentration gradient peaking at PSE and activating gene expression that promotes radial growth. The expression and function of PEAR proteins are antagonized by well-established polarity transcription factors, HD-ZIP III, whose expression is concentrated in the more internal domain of radially non-dividing procambial cells by the function of auxin and mobile miR165/166. The PEAR proteins locally promote transcription of their inhibitory HD-ZIP III genes, thereby establishing a negative feedback loop that forms a sharp boundary demarking the zone of cell divisions. Taken together, we have established a network, in which the PEAR - HD-ZIP III module integrates the spatial information of the hormonal domains and miRNA gradients during root procambial development, to provide a pre-pattern with actively dividing and more quiescent zones, thus priming radial growth.

2018-11-09 | GSE115183 | GEO

HELZ2: a new, interferon-regulated, human 3’-5’ exoribonuclease of the RNB family is expressed from a non-canonical initiation codon

Project description:Proteins containing a RNB domain, originally identified in E. coli RNase II, are widely present throughout the tree of life. Many RNB proteins are endowed with 3’-5’ exoribonucleolytic activity but some have lost catalytic function during evolution. Database searches identified a new RNB domain containing protein in human: HELZ2. Analysis of genomic and expression data with evolutionary information suggested that the human HELZ2 protein is produced from an unforeseen non-canonical initiation codon in Hominidae. This unusual property was confirmed experimentally, extending the human protein by 247 residues. Human HELZ2 was further shown to be an active ribonuclease despite the substitution of a key residue in its catalytic center. HELZ2 harbors also two RNA helicase domains and several zinc-fingers and its expression is induced by interferon treatment. We demonstrate that HELZ2 is able to degrade structured RNAs through the coordinated ATP-dependent displacement of duplex RNA mediated by its RNA helicase domains and its 3’-5’ ribonucleolytic action. The expression characteristics and biochemical properties of HELZ2 support a role for this factor in response to viruses and/or mobile elements.

2023-08-18 | PXD040351 | Pride

miRNA mobility is a highly regulated process in plants

Project description:Small RNAs regulate many important developmental processes by targeting key regulators, such as transcription factor families, for posttranscriptional repression. Although originally assumed to function cell-autonomously, several instances of small RNAs serving as short-range mobile signals have now been reported. The recognition that small RNAs can move from cell-to-cell has broadened our thinking on how these molecules are utilized during development, serving as positional, morphogen-like, signals. However, major questions regarding the properties and function of mobile small RNAs during plant development remain. For example, is miRNA movement a developmentally regulated process? What factors are important for miRNA mobility? In order to address questions regarding the properties of miRNAs mobility, our group has developed a reporter system to assay non-cell-autonomous miRNA activity. In this system an artificial miRNA (MIR-GFP) is expressed from tissue-specific promoters and assayed for its capacity to silence a ubiquitously-expressed, cell-autonomous, nuclear-localized GFP reporter (p35S:3xNLS-GFP). Here we report that miRNA movement is a regulated process, and that competence to move is developmentally determined. In select tissue contexts, miRNAs show differential or directional movement, indicating miRNA mobility to be regulated independently from other signalling molecules.

2017-12-01 | GSE102236 | GEO

Bisulfite-Seq and RNA-seq in rootstock of Arabidopsis thaliana grafts

Project description:RNA silencing is a mechanism for regulating gene expression at the transcriptional and post-transcriptional levels. Its functions include regulating endogenous gene expression and protecting the cell against viruses and invading transposable elements (TEs). A key component of the mechanism is small RNAs (sRNAs) of 21-24 nucleotides (nt) in length, which direct the silencing machinery in a sequence specific manner to target nucleic acids. sRNAs of 24 nt are involved in methylation of cytosine residues of target loci in three sequence contexts (CG, CHG and CHH), referred to as RNA-directed DNA methylation (RdDM). We previously demonstrated that 24 nt sRNAs are mobile from shoot to root in Arabidopsis thaliana. In this study we demonstrated that methylation of thousands of loci in root tissues is dependent upon mobile sRNAs from the shoot. Furthermore, we found that mobile sRNA-dependent DNA methylation occurs predominantly in non-CG contexts. These findings were made using base-resolution next generation sequencing approaches and genome wide analyses. Specific classes of short TEs are the predominant targets of mobile sRNA-dependent DNA methylation; classes typically found in gene-rich euchromatic regions. Mobile sRNA-regulated genes were also identified. Mechanistically, we demonstrate that mobile sRNA-dependent non-CG methylation is largely independent of the CMT2/3 RdDM pathway but dependent upon the DRM1/DRM2 RdDM pathway. This is in contrast to non-mobile sRNA-dependent DNA methylation, which predominantly depends upon the CMT2/3 RdDM pathway. These data are complementary to the small RNA sequencing data from Arabidopsis root grafts described in Molnar et al (Science, 2010 May 14;328(5980):872-5).

2016-01-04 | E-MTAB-3473 | biostudies-arrayexpress

Essential role of Cp190 in physical and regulatory boundary formation in Drosophila

Project description:Animal genomes fold into contact domains defined by enhanced internal contact frequencies with debated functions in establishing independent gene regulatory domains. A large fraction of contact domains in mammals are formed by stalling of chromosomal loop-extruding cohesin by CTCF at domain boundaries. 90% of domain boundaries in Drosophila form CTCF-independently, and other proteins were proposed to form chromosomal loops with dual functions of segregating promoters from inappropriate regulatory elements and connecting distal regulatory elements to their correct targets. Here, we genetically ablate the ubiquitous boundary-associated factor Cp190 and assess impacts on genome folding and transcriptional regulation in embryos. Our results reveal that Cp190 is a major factor required for contact domain boundary formation and gene insulation in Drosophila.

2022-05-30 | PXD027795 | Pride

Opposite Imp/Syp temporal gradients govern birth time-dependent neuronal fates

Project description:Generating diverse neurons involves spatially distinct neural stem cells that show age dependent developmental fates. Drosophila neuroblasts produce long, diverse yet stereotyped series of distinct neurons, called lineages. We searched for novel temporal factors that could pattern such extended lineages by RNA-sequencing of specific neuroblasts at various developmental times. We found that two RNA-binding proteins, Imp and Syp, display opposing high-to-low and low-to-high temporal gradients with distinct dynamics in specific lineages. Manipulating Imp/Syp levels in mushroom body neuroblasts revealed opposing roles in the specification of early and late temporal fates, primarily via regulation of Chinmo translation. This study implicates the opposing Imp/Syp gradients as temporal morphogens that encode stem cell age and govern birth time-dependent offspring cell fate through post-transcriptional regulation of temporal dentity genes.

2015-10-21 | GSE71103 | GEO

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