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Proc. Natl. Acad. Sci. USA, Published online before print January 27, 2017 | doi: 10.1073/pnas.1620592114 Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells in Arabidopsis thaliana

Abstract

Jin-Sup Park^a,1, Jennifer M. Frost^b,1, Kyunghyuk Park^a, Hyonhwa Ohr^a, Guen Tae Park^a, Seohyun Kim^a, Hyunjoo Eom^a, Ilha Lee^a, Janie S. Brooks^c, Robert L. Fischer^b,2, and Yeonhee Choi^a,d,2^aDepartment of Biological Sciences, Seoul National University, Seoul 151-747, Korea;
^bDepartment of Plant and Microbial Biology, University of California, Berkeley, CA 94720;
^cDepartment of Science, Seoul Foreign School, Seoul 120-823, Korea;
^dPlant 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.

DNA demethylation, central cell, vegetative cell, cell-specific transcription, DNA enhancer elements
¹J.-S.P. and J.M.F. contributed equally to this work.
²To whom correspondence may be addressed.

Author contributions: J.-S.P., J.M.F., I.L., R.L.F., and Y.C. designed research; J.-S.P., J.M.F., K.P., H.O., G.T.P., S.K., and H.E. performed research; J.-S.P., J.M.F., J.S.B., R.L.F., and Y.C. analyzed data; and J.-S.P., J.M.F., J.S.B., R.L.F., and Y.C. wrote the paper.

논문정보

형식Research article
게재일2017년 01월 (BRIC 등록일 2017-02-03)
연구진국내(교신)+국외 연구진
분야 생명과학 > 식물학

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