The DME demethylase regulates sporophyte gene expression, cell proliferation, differentiation, and meristem resurrection

Abstract

The flowering plant life cycle consists of alternating haploid (gametophyte) and diploid (sporophyte) generations, where the sporophytic generation begins with fertilization of haploid gametes. In Arabidopsis, genome-wide DNA demethylation is required for normal development, catalyzed by the DEMETER (DME) DNA demethylase in the gamete companion cells of male and female gametophytes. In the sporophyte, postembryonic growth and development are largely dependent on the activity of numerous stem cell niches, or meristems. Analyzing Arabidopsis plants homozygous for a loss-of-function dme-2 allele, we show that DME influences many aspects of sporophytic growth and development. dme-2 mutants exhibited delayed seed germination, variable root hair growth, aberrant cellular proliferation and differentiation followed by enhanced de novo shoot formation, dysregulation of root quiescence and stomatal precursor cells, and inflorescence meristem (IM) resurrection. We also show that sporophytic DME activity exerts a profound effect on the transcriptome of developing Arabidopsis plants, including discrete groups of regulatory genes that are misregulated in dme-2 mutant tissues, allowing us to potentially link phenotypes to changes in specific gene expression pathways. These results show that DME plays a key role in sporophytic development and suggest that DME-mediated active DNA demethylation may be involved in the maintenance of stem cell activities during the sporophytic life cycle in Arabidopsis.

The maize genematernal derepression of r1encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm

“…In rice ( Oryza sativa ), the DNA glycosylase ROS1a/OsDNG702 is also strictly required for seed development and has a function in pollen fertility, but its importance in pollen may be dependent on the cultivar ( Ono et al, 2012 ; Zhou et al, 2021 ). The Arabidopsis genome also encodes three other glycosylases, which along with demeter mutants, produce subtle phenotypes in a variety of plant tissues ( Pillot et al, 2010 ; Yamamuro et al, 2014 ; Schumann et al, 2017 ; Schumann et al, 2019 ; Khouider et al, 2021 ; Kim et al, 2021 ). Endosperm derived from central cells that lack DEMETER has excessive DNA methylation in thousands of small regions ( Ibarra et al, 2012 ; Park et al, 2016 ).…”

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

“…In Arabidopsis, DEMETER is required for normal development not just in endosperm, but in the pollen vegetative cell and non-reproductive cell types as well (Schoft et al 2011; Borg et al 2021; Khouider et al 2021; Kim et al 2021). In the case of pollen vegetative cell, developmental phenotypes are determined by gene regulation rather than transposon activation.…”

“…In rice, the DNA glycosylase ROS1a/OsDNG702 is also strictly required for seed development and has a function in pollen fertility, but its importance in pollen may be dependent on the cultivar (Ono et al 2012; Zhou et al 2021). The Arabidopsis genome also encodes three other glycosylases, which along with demeter mutants, produce subtle phenotypes in a variety of plant tissues (Pillot et al 2010; Yamamuro et al 2014; Schumann et al 2017; Schumann et al 2019; Khouider et al 2021; Kim et al 2021). Endosperm derived from central cells that lack DEMETER have excessive DNA methylation at thousands of small regions (Ibarra et al 2012; Park et al 2016).…”

CG and CHG Methylation Contribute to the Transcriptional Control of OsPRR37-Output Genes in Rice

“…A specific DNA methylation state is also under the dynamic regulation by de novo methylation, maintenance of methylation, and active demethylation ( Law and Jacobsen, 2010 ; Zhang et al, 2018 ). The function of DNA methylation in plant reproductive cells has been extensively studied, and this knowledge has deepened our understanding of the dynamic DNA methylation patterns during plant development ( Zheng et al, 2019 ; Higo et al, 2020 ; Kim et al, 2021 ; Zhou et al, 2021a ). In addition, DNA methylation reportedly has roles in regulating plant architecture, plant defense against rice black-streaked dwarf virus, and multiple agronomical traits ( Zhang et al, 2015 , 2020 ; Kawakatsu, 2020 ; Xu et al, 2020 ).…”