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

Demethylation of transposons can activate the expression of nearby genes and cause imprinted gene expression in the endosperm; this demethylation is hypothesized to lead to expression of transposon small interfering RNAs (siRNAs) that reinforce silencing in the next generation through transfer eithe...

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Autores principales: Gent, Jonathan I, Higgins, Kaitlin M, Swentowsky, Kyle W, Fu, Fang-Fang, Zeng, Yibing, Kim, Dong won, Dawe, R Kelly, Springer, Nathan M, Anderson, Sarah N
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9516051/
https://www.ncbi.nlm.nih.gov/pubmed/35775949
http://dx.doi.org/10.1093/plcell/koac199
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author Gent, Jonathan I
Higgins, Kaitlin M
Swentowsky, Kyle W
Fu, Fang-Fang
Zeng, Yibing
Kim, Dong won
Dawe, R Kelly
Springer, Nathan M
Anderson, Sarah N
author_facet Gent, Jonathan I
Higgins, Kaitlin M
Swentowsky, Kyle W
Fu, Fang-Fang
Zeng, Yibing
Kim, Dong won
Dawe, R Kelly
Springer, Nathan M
Anderson, Sarah N
author_sort Gent, Jonathan I
collection PubMed
description Demethylation of transposons can activate the expression of nearby genes and cause imprinted gene expression in the endosperm; this demethylation is hypothesized to lead to expression of transposon small interfering RNAs (siRNAs) that reinforce silencing in the next generation through transfer either into egg or embryo. Here we describe maize (Zea mays) maternal derepression of r1 (mdr1), which encodes a DNA glycosylase with homology to Arabidopsis thaliana DEMETER and which is partially responsible for demethylation of thousands of regions in endosperm. Instead of promoting siRNA expression in endosperm, MDR1 activity inhibits it. Methylation of most repetitive DNA elements in endosperm is not significantly affected by MDR1, with an exception of Helitrons. While maternally-expressed imprinted genes preferentially overlap with MDR1 demethylated regions, the majority of genes that overlap demethylated regions are not imprinted. Double mutant megagametophytes lacking both MDR1 and its close homolog DNG102 result in early seed failure, and double mutant microgametophytes fail pre-fertilization. These data establish DNA demethylation by glycosylases as essential in maize endosperm and pollen and suggest that neither transposon repression nor genomic imprinting is its main function in endosperm.
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spelling pubmed-95160512022-09-29 The maize gene maternal derepression of r1 encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm Gent, Jonathan I Higgins, Kaitlin M Swentowsky, Kyle W Fu, Fang-Fang Zeng, Yibing Kim, Dong won Dawe, R Kelly Springer, Nathan M Anderson, Sarah N Plant Cell Research Articles Demethylation of transposons can activate the expression of nearby genes and cause imprinted gene expression in the endosperm; this demethylation is hypothesized to lead to expression of transposon small interfering RNAs (siRNAs) that reinforce silencing in the next generation through transfer either into egg or embryo. Here we describe maize (Zea mays) maternal derepression of r1 (mdr1), which encodes a DNA glycosylase with homology to Arabidopsis thaliana DEMETER and which is partially responsible for demethylation of thousands of regions in endosperm. Instead of promoting siRNA expression in endosperm, MDR1 activity inhibits it. Methylation of most repetitive DNA elements in endosperm is not significantly affected by MDR1, with an exception of Helitrons. While maternally-expressed imprinted genes preferentially overlap with MDR1 demethylated regions, the majority of genes that overlap demethylated regions are not imprinted. Double mutant megagametophytes lacking both MDR1 and its close homolog DNG102 result in early seed failure, and double mutant microgametophytes fail pre-fertilization. These data establish DNA demethylation by glycosylases as essential in maize endosperm and pollen and suggest that neither transposon repression nor genomic imprinting is its main function in endosperm. Oxford University Press 2022-07-01 /pmc/articles/PMC9516051/ /pubmed/35775949 http://dx.doi.org/10.1093/plcell/koac199 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Gent, Jonathan I
Higgins, Kaitlin M
Swentowsky, Kyle W
Fu, Fang-Fang
Zeng, Yibing
Kim, Dong won
Dawe, R Kelly
Springer, Nathan M
Anderson, Sarah N
The maize gene maternal derepression of r1 encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm
title The maize gene maternal derepression of r1 encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm
title_full The maize gene maternal derepression of r1 encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm
title_fullStr The maize gene maternal derepression of r1 encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm
title_full_unstemmed The maize gene maternal derepression of r1 encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm
title_short The maize gene maternal derepression of r1 encodes a DNA glycosylase that demethylates DNA and reduces siRNA expression in the endosperm
title_sort maize gene maternal derepression of r1 encodes a dna glycosylase that demethylates dna and reduces sirna expression in the endosperm
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9516051/
https://www.ncbi.nlm.nih.gov/pubmed/35775949
http://dx.doi.org/10.1093/plcell/koac199
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