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A Small RNA-Mediated Regulatory Network in Arabidopsis thaliana Demonstrates Connectivity Between phasiRNA Regulatory Modules and Extensive Co-Regulation of Transcription by miRNAs and phasiRNAs.

ABSTRACT: Gene regulation involves the orchestrated action of multiple regulators to fine-tune the expression of genes. Hierarchical interactions and co-regulation among regulators are commonly observed in biological systems, leading to complex regulatory networks. Small RNA (sRNAs) have been shown to be important regulators of gene expression due to their involvement in multiple cellular processes. In plants, microRNA (miRNAs) and phased small interfering RNAs (phasiRNAs) correspond to two well-characterized types of sRNAs involved in the regulation of posttranscriptional gene expression, although information about their targets and interactions with other gene expression regulators is limited. We describe an extended sRNA-mediated regulatory network in Arabidopsis thaliana that provides a reference frame to understand sRNA biogenesis and activity at the genome-wide level. This regulatory network combines a comprehensive evaluation of phasiRNA production and sRNA targets supported by degradome data. The network includes ~17% of genes in the A. thaliana genome, representing ~50% annotated gene ontology (GO) functional categories. Approximately 14% of genes with GO annotations corresponding to regulation of gene expression were found to be under sRNA control. The unbiased bioinformatic approach used to produce the network was able to detect 107 PHAS loci (regions of phasiRNA production), 5,047 active phasiRNAs (~70% of which were non-canonical), and reconstruct 17 regulatory modules resulting from complex regulatory interactions between different sRNA-regulatory pathways. Known regulatory modules like miR173-TAS-PPR/TPR and miR390-TAS3-ARF/F-box were faithfully reconstructed and expanded, illustrating the accuracy and sensitivity of the methods and providing confidence for the validity of findings of previously unrecognized modules. The network presented here includes a 2X increase in the number of identified PHAS loci, a large complement (~70%) of non-canonical phasiRNAs, and the most comprehensive evaluation of sRNA cleavage activity in A. thaliana to date. Structural analysis showed similarities to networks of other biological systems and demonstrated connectivity between phasiRNA regulatory modules with extensive co-regulation of transcripts by miRNAs and phasiRNAs. The described regulatory network provides a reference that will facilitate global analyses of individual plant regulatory programs such as those that control homeostasis, development, and responses to biotic and abiotic environmental changes.

SUBMITTER: Vargas-Asencio JA

PROVIDER: S-EPMC7001039 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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A Small RNA-Mediated Regulatory Network in <i>Arabidopsis thaliana</i> Demonstrates Connectivity Between phasiRNA Regulatory Modules and Extensive Co-Regulation of Transcription by miRNAs and phasiRNAs.

Vargas-Asencio Jose A JA Perry Keith L KL

Frontiers in plant science 20200129

Gene regulation involves the orchestrated action of multiple regulators to fine-tune the expression of genes. Hierarchical interactions and co-regulation among regulators are commonly observed in biological systems, leading to complex regulatory networks. Small RNA (sRNAs) have been shown to be important regulators of gene expression due to their involvement in multiple cellular processes. In plants, microRNA (miRNAs) and phased small interfering RNAs (phasiRNAs) correspond to two well-character ...[more]

PMID: 32082334

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Project description:BackgroundSeed germination involves progression from complete metabolic dormancy to a highly active, growing seedling. Many factors regulate germination and these interact extensively, forming a complex network of inputs that control the seed-to-seedling transition. Our understanding of the direct regulation of gene expression and the dynamic changes in the epigenome and small RNAs during germination is limited. The interactions between genome, transcriptome and epigenome must be revealed in order to identify the regulatory mechanisms that control seed germination.ResultsWe present an integrated analysis of high-resolution RNA sequencing, small RNA sequencing and MethylC sequencing over ten developmental time points in Arabidopsis thaliana seeds, finding extensive transcriptomic and epigenomic transformations associated with seed germination. We identify previously unannotated loci from which messenger RNAs are expressed transiently during germination and find widespread alternative splicing and divergent isoform abundance of genes involved in RNA processing and splicing. We generate the first dynamic transcription factor network model of germination, identifying known and novel regulatory factors. Expression of both microRNA and short interfering RNA loci changes significantly during germination, particularly between the seed and the post-germinative seedling. These are associated with changes in gene expression and large-scale demethylation observed towards the end of germination, as the epigenome transitions from an embryo-like to a vegetative seedling state.ConclusionsThis study reveals the complex dynamics and interactions of the transcriptome and epigenome during seed germination, including the extensive remodelling of the seed DNA methylome from an embryo-like to vegetative-like state during the seed-to-seedling transition. Data are available for exploration in a user-friendly browser at https://jbrowse.latrobe.edu.au/germination_epigenome .

Dataset Information

A Small RNA-Mediated Regulatory Network in Arabidopsis thaliana Demonstrates Connectivity Between phasiRNA Regulatory Modules and Extensive Co-Regulation of Transcription by miRNAs and phasiRNAs.

Publications

A Small RNA-Mediated Regulatory Network in <i>Arabidopsis thaliana</i> Demonstrates Connectivity Between phasiRNA Regulatory Modules and Extensive Co-Regulation of Transcription by miRNAs and phasiRNAs.

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