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

Jin Sup Park, Jennifer M. Frost, Kyunghyuk Park, Hyonhwa Ohr, Guen Tae Park, Seohyun Kim, Hyunjoo Eom, Ilha Lee, Janie Sue Brooks, Robert L. Fischer, Yeonhee Choi

Research output: Contribution to journalArticle

10 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)2078-2083
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number8
DOIs
Publication statusPublished - 2017 Feb 21

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Arabidopsis
Germ Cells
DNA
Genes
Endosperm
DNA Transposable Elements
Transcriptional Regulatory Elements
DNA Glycosylases
Nucleosomes
Conserved Sequence
Cell Lineage
Reporter Genes
Epigenomics
DNA Repair
Reproduction
Ovum
Spermatozoa
Seeds
Transcription Factors
Genome

All Science Journal Classification (ASJC) codes

  • General

Cite this

Park, Jin Sup ; Frost, Jennifer M. ; Park, Kyunghyuk ; Ohr, Hyonhwa ; Park, Guen Tae ; Kim, Seohyun ; Eom, Hyunjoo ; Lee, Ilha ; Brooks, Janie Sue ; Fischer, Robert L. ; Choi, Yeonhee. / Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells in Arabidopsis thaliana. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 8. pp. 2078-2083.
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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.",
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Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells in Arabidopsis thaliana. / Park, Jin Sup; Frost, Jennifer M.; Park, Kyunghyuk; Ohr, Hyonhwa; Park, Guen Tae; Kim, Seohyun; Eom, Hyunjoo; Lee, Ilha; Brooks, Janie Sue; Fischer, Robert L.; Choi, Yeonhee.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 8, 21.02.2017, p. 2078-2083.

Research output: Contribution to journalArticle

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AU - Park, Jin Sup

AU - Frost, Jennifer M.

AU - Park, Kyunghyuk

AU - Ohr, Hyonhwa

AU - Park, Guen Tae

AU - Kim, Seohyun

AU - Eom, Hyunjoo

AU - Lee, Ilha

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AU - Fischer, Robert L.

AU - Choi, Yeonhee

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AB - 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.

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