Abstract
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.
Highlights
Seed germination involves progression from complete metabolic dormancy to a highly active, growing seedling
Differential RNA splicing changes relative transcript isoform abundance during germination The primary aim of our study was to determine the interactions between genome and epigenome during germination
The gene ontology (GO) functional enrichments in each cluster were consistent with previous studies [8,9,10]: light-related and root-related functions were enriched in the cluster of genes with highest expression in the seedling, RNA splicing and histone functions were enriched for genes with high expression in dry seed and genes encoding mitochondrial proteins and RNA-related functions were enriched among the transiently expressed genes (Additional file 2: Figure S1)
Summary
Seed germination involves progression from complete metabolic dormancy to a highly active, growing seedling. Seeds are essential for crop productivity and are an important part of our diet They can remain dormant for years before becoming highly metabolically active as the seed germinates and transitions into a seedling. Microarray-based transcriptomic studies in various plants have described global changes in the cellular messenger RNA (mRNA) population and hormone interactions during seed germination, such as ABA regulation of the germination transcriptome [8,9,10,11,12]. They have enabled network modelling of global transcriptional interactions in seeds (SeedNet) [13]. Alternative splicing expands the repertoire of transcripts derived from a genome: the latest genome annotation of Arabidopsis (Araport11) documents 48,359 transcripts corresponding to 27,655 genes
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