Epigenetic reprogramming rewires transcription during the alternation of generations in Arabidopsis

Abstract

Alternation between morphologically distinct haploid and diploid life forms is a defining feature of most plant and algal life cycles, yet the underlying molecular mechanisms that govern these transitions remain unclear. Here, we explore the dynamic relationship between chromatin accessibility and epigenetic modifications during life form transitions in Arabidopsis. The diploid-to-haploid life form transition is governed by the loss of H3K9me2 and DNA demethylation of transposon-associated cis-regulatory elements. This event is associated with dramatic changes in chromatin accessibility and transcriptional reprogramming. In contrast, the global loss of H3K27me3 in the haploid form shapes a chromatin accessibility landscape that is poised to re-initiate the transition back to diploid life after fertilization. Hence, distinct epigenetic reprogramming events rewire transcription through major reorganization of the regulatory epigenome to guide the alternation of generations in flowering plants.

The epigenetic origin of life history transitions in plants and algae

“…As a result, the loss of constitutive heterochromatin identity in the VN re-activates a handful of TEs that stimulate the production of epigenetically activated small RNAs (easiRNAs) (Slotkin et al 2009;Calarco et al 2012;Borges et al 2018;Wang et al 2020). Strikingly, a large proportion of the genomic regions targeted for demethylation by DME specifically gain chromatin accessibility in the VN (Borg et al 2021b). This occurs within regions that not only stimulate easiRNA production but that also lie in the vicinity of VN-specific protein-coding genes, which importantly are silenced with DNA-H3K9 methylation in the sporophyte (Borg et al 2021b).…”

“…Strikingly, several H3K27me3-marked genes in the sporophyte also include master regulators of embryogenesis like BABY BOOM (BBM) and LEAFY COTYLEDON 1 (LEC1) (Horstman et al 2017;Khanday et al 2019). In sperm, the loss of H3K27me3 as these loci coincides with increased chromatin accessibility and accumulation of active H3K4me3 modifications at promoter regions, which occurs in a pattern that predicts gene expression during earliest phases of embryogenesis (Borg et al 2020(Borg et al , 2021b.…”

“…In contrast, paternally derived histones are passively diluted over several rounds of DNA replication in the endosperm (Ingouff et al 2007), which might provide a longer window for histone-based imprints to act. Interestingly, unlike MEGs, many PEG loci are also transcriptionally primed with open chromatin and H3K4me3 in sperm (Borg et al 2020(Borg et al , 2021b, providing correlative evidence for how paternal chromatin potentially impacts gene expression after fertilization. Mechanistically, preconfigured accessible chromatin could help elicit the binding of maternally derived TFs or perhaps already signifies a paternal contribution of pre-bound TFs at fertilization.…”

Taking the Wheel – de novo DNA Methylation as a Driving Force of Plant Embryonic Development

“…On the one hand, DNA methylation can be conservatively inherited through cell divisions, ensuring epigenetic memory of their cellular predecessors and can be heritable across generations (Schmitz et al, 2013;Iwasaki and Paszkowski, 2014). On the other hand, differences in methylation profiles can be found even between cells of the same origin separated by only a few divisions, such as different cells of a plant gametophyte, as shown for Arabidopsis and rice (Ibarra et al, 2012;Park et al, 2016;Han et al, 2019;Borg et al, 2021). Perhaps the most dramatic feature of epigenetics is 'epigenetic reprogramming, ' a term used to describe a process in which epigenetic marks of a previous developmental stage or cellular form are erased and a novel epigenetic pattern is established de novo.…”

The maize gene maternal derepression of r1 (mdr1) encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in endosperm

“…Even though endosperm DMRs have little mCHH, it is possible that siRNAs produced by endosperm demethylation could direct other chromatin modifications or function posttranscriptionally (Parent et al 2021). In Arabidopsis, demethylation of heterochromatin in pollen vegetative cells corresponds to production of 21 and 22nt siRNAs from LTR retrotransposons (Creasey et al 2014;McCue et al 2015;Borg et al 2021). Since the preference for DMRs is to be near euchromatin, where they have the potential to overlap RdDM regions, we separated endosperm DMRs into two groups, euchromatin DMRs, which were within 2 Kb of euchromatin (10142 regions), and heterochromatin DMRs, which were not (10014 regions).…”