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Proc Natl Acad Sci U S A. 2017 Feb 21;114(8):2078-2083. doi: 10.1073/pnas.1620592114. Epub 2017 Jan 27.

Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells in Arabidopsis thaliana.

Author information

1
Department of Biological Sciences, Seoul National University, Seoul 151-747, Korea.
2
Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720.
3
Department of Science, Seoul Foreign School, Seoul 120-823, Korea.
4
Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720; rfischer@berkeley.edu yhc@snu.ac.kr.
5
Department of Biological Sciences, Seoul National University, Seoul 151-747, Korea; rfischer@berkeley.edu yhc@snu.ac.kr.
6
Plant Genomics and Breeding Institute, Seoul 151-921, Korea.

Abstract

The DEMETER (DME) DNA glycosylase initiates active DNA demethylation via the base-excision repair pathway and is vital for reproduction in Arabidopsis thaliana DME-mediated DNA demethylation is preferentially targeted to small, AT-rich, and nucleosome-depleted euchromatic transposable elements, influencing expression of adjacent genes and leading to imprinting in the endosperm. In the female gametophyte, DME expression and subsequent genome-wide DNA demethylation are confined to the companion cell of the egg, the central cell. Here, we show that, in the male gametophyte, DME expression is limited to the companion cell of sperm, the vegetative cell, and to a narrow window of time: immediately after separation of the companion cell lineage from the germline. We define transcriptional regulatory elements of DME using reporter genes, showing that a small region, which surprisingly lies within the DME gene, controls its expression in male and female companion cells. DME expression from this minimal promoter is sufficient to rescue seed abortion and the aberrant DNA methylome associated with the null dme-2 mutation. Within this minimal promoter, we found short, conserved enhancer sequences necessary for the transcriptional activities of DME and combined predicted binding motifs with published transcription factor binding coordinates to produce a list of candidate upstream pathway members in the genetic circuitry controlling DNA demethylation in gamete companion cells. These data show how DNA demethylation is regulated to facilitate endosperm gene imprinting and potential transgenerational epigenetic regulation, without subjecting the germline to potentially deleterious transposable element demethylation.

KEYWORDS:

DNA demethylation; DNA enhancer elements; cell-specific transcription; central cell; vegetative cell

PMID:
28130550
PMCID:
PMC5338364
DOI:
10.1073/pnas.1620592114
[Indexed for MEDLINE]
Free PMC Article

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