Extensive transcriptomic and epigenomic remodelling occurs during Arabidopsis thaliana germination

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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1302-3) contains supplementary material, which is available to authorized users.

Replication‐coupled histone H3.1 deposition determines nucleosome composition and heterochromatin dynamics during Arabidopsis seedling development

“…To explain the increase in H3.1 occupancy specifically at heterochromatin, we can envisage that after a genome‐wide incorporation during S‐phase, H3.1 is exchanged to H3.3 either in a transcription‐dependent manner at the genic regions analyzed here or globally in euchromatin as described previously during the transition from cell proliferation to differentiation in the root (Otero et al ., ). Interestingly, most H3.1‐encoding genes are not expressed in the dry seed (Kawakatsu et al ., ; Narsai et al ., ), in agreement with absence of replicative activity (Barroco et al ., ) pointing towards a peculiar H3.1 : H3.3 balance in the dry seed that might favor chromatin decondensation during germination. Furthermore, the resumption of replication activity after germination renders this developmental time window particularly suitable to decipher changes in chromatin and nuclear organization linked to DNA replication coupled histone deposition.…”

Gibberellin response in the embryo epidermis regulates germination uniformity in response to seed priming

“…Underpinning the transition from seed to seedling is a sequence of dynamic molecular events which unfold with the germinating embryo. These dynamic gene expression and epigenetic changes have been characterized previously on a genome-wide scale (Dekkers et al, 2013;Nakabayashi et al, 2005;Narsai et al, 2017).…”

“…This transition into a seedling is principally driven by cell expansion, rather than cell division (Bassel et al, 2014;Sliwinska et al, 2009). This discrete induction of growth following the initiation of the germination program is promoted by GA (Groot and Karssen, 1987;Koornneef and Van der Veen, 1980) and its induction of gene expression associated with cell wall remodelling proteins which facilitate cell growth (Dekkers et al, 2013;Nakabayashi et al, 2005;Narsai et al, 2017). These cell expansion-associated genes may be considered the downstream targets of the germination process in light of the central role they play in the regulation of embryo growth (Bassel, 2016).…”

Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming?

“…Wild-type sperm has low CHH methylation (Calarco et al, 2012), indicating that the paternal genome must gain methylation after fertilization. Recent studies from soybean and Arabidopsis have shown that CHH methylation increases during embryogenesis (Kawakatsu et al, 2017;Lin et al, 2017;Narsai et al, 2017). In mature Arabidopsis embryos, CHH methylation approaches 100% at individual cytosines, whereas in other tissues, including younger embryos, individual CHH sites are c. 20% methylated (Bouyer et al, 2017).…”

“…In mature Arabidopsis embryos, CHH methylation approaches 100% at individual cytosines, whereas in other tissues, including younger embryos, individual CHH sites are c. 20% methylated (Bouyer et al, 2017). Methylation decreases upon seed germination, likely through a passive mechanism (Bouyer et al, 2017;Kawakatsu et al, 2017;Lin et al, 2017;Narsai et al, 2017). It is unknown whether the increased CHH methylation in developing embryos is functional: mutation of the de novo methyltransferases DRM2 and CMT2 prevents CHH methylation but without obvious effects on seed development or germination, although it is unclear how comprehensively phenotypes have been assessed.…”