A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation

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Abstract

Transposons are generally kept silent by epigenetic mechanisms including DNA methylation. Here, we identified a pair of Harbinger transposon- derived proteins (HDPs), HDP1 and HDP2, as anti-silencing factors in Arabidopsis. hdp1 and hdp2 mutants displayed an enhanced silencing of transgenes and some transposons. Phylogenetic analyses revealed that HDP1 and HDP2 were co-domesticated from the Harbinger transposon-encoded transposase and DNA-binding protein, respectively. HDP1 interacts with HDP2 in the nucleus, analogous to their transposon counterparts. Moreover, HDP1 and HDP2 are associated with IDM1, IDM2, IDM3 and MBD7 that constitute a histone acetyltransferase complex functioning in DNA demethylation. HDP2 and the methyl-DNA-binding protein MBD7 share a large set of common genomic binding sites, indicating that they jointly determine the target specificity of the histone acetyltransferase complex. Thus, our data revealed that HDP1 and HDP2 constitute a functional module that has been recruited to a histone acetyltransferase complex to prevent DNA hypermethylation and epigenetic silencing.

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Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis.

Zhengyan Feng, Yanfei Mao, Nanfei Xu … (2014)

The CRISPR (clustered regularly interspaced short palindromic repeat)/Cas (CRISPR-associated) system has emerged as a powerful tool for targeted gene editing in many organisms, including plants. However, all of the reported studies in plants focused on either transient systems or the first generation after the CRISPR/Cas system was stably transformed into plants. In this study we examined several plant generations with seven genes at 12 different target sites to determine the patterns, efficiency, specificity, and heritability of CRISPR/Cas-induced gene mutations or corrections in Arabidopsis. The proportion of plants bearing any mutations (chimeric, heterozygous, biallelic, or homozygous) was 71.2% at T1, 58.3% at T2, and 79.4% at T3 generations. CRISPR/Cas-induced mutations were predominantly 1 bp insertion and short deletions. Gene modifications detected in T1 plants occurred mostly in somatic cells, and consequently there were no T1 plants that were homozygous for a gene modification event. In contrast, ∼22% of T2 plants were found to be homozygous for a modified gene. All homozygotes were stable to the next generation, without any new modifications at the target sites. There was no indication of any off-target mutations by examining the target sites and sequences highly homologous to the target sites and by in-depth whole-genome sequencing. Together our results show that the CRISPR/Cas system is a useful tool for generating versatile and heritable modifications specifically at target genes in plants.

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The origin and behavior of mutable loci in maize.

B. McClintock (1950)

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Active DNA demethylation mediated by DNA glycosylases.

Jian-Kang Zhu (2009)

Active DNA demethylation is involved in many vital developmental and physiological processes of plants and animals. Recent genetic and biochemical studies in Arabidopsis have demonstrated that a subfamily of DNA glycosylases function to promote DNA demethylation through a base excision-repair pathway. These specialized bifunctional DNA glycosylases remove the 5-methylcytosine base and then cleave the DNA backbone at the abasic site, resulting in a gap that is then filled with an unmethylated cytosine nucleotide by as yet unknown DNA polymerase and ligase enzymes. Evidence suggests that active DNA demethylation in mammalian cells is also mediated at least in part by a base excision repair pathway where the AID/Apobec family of deaminases convert 5-methylcytosine to thymine followed by G/T mismatch repair by the DNA glycosylase MBD4 or TDG. This review also discusses other possible mechanisms of active DNA demethylation, how genome DNA methylation status might be sensed to regulate the expression of demethylase genes, and the targeting of demethylases by small RNAs.

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Author and article information

Journal

Journal ID (nlm-ta): Cell Res

Journal ID (iso-abbrev): Cell Res

Title: Cell Research

Publisher: Nature Publishing Group

ISSN (Print): 1001-0602

ISSN (Electronic): 1748-7838

Publication date (Print): February 2017

Publication date (Electronic): 09 December 2016

Publication date PMC-release: 1 February 2017

Volume: 27

Issue: 2

Pages: 226-240

Affiliations

[1 ]Shanghai Center for Plant Stress Biology, Shanghai Institute for Biological Sciences, Chinese Academy of Sciences , China

[2 ]Department of Horticulture and Landscape Architecture, Purdue University , West Lafayette, IN 47907, USA

[3 ]Department of Biochemistry, Purdue University , West Lafayette, IN 47907, USA

[4 ]The State Key Laboratory of Plant Cell and Chromosome Engineering, Center for Agricultural Research Resources, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences , Shijiazhuang, Hebei 050022, China

[5 ]Biotechnology Section, Indian Institute of Rice Research (IIRR) , Hyderabad, India

[6 ]College of Agriculture, Henan University of Science and Technology , Luoyang, Henan 471026, China

Author notes

[* ]E-mail: jkzhu@ 123456purdue.edu

[✝]

These two authors contributed equally to this work.

Article

Publisher Item ID: cr2016147

DOI: 10.1038/cr.2016.147

PMC ID: 5339849

PubMed ID: 27934869

SO-VID: ad8977ca-83d1-4f2b-a0f7-0ade992201af

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This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 4.0 Unported License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/4.0/

History

Date received : 09 October 2016

Date revision received : 17 October 2016

Date accepted : 18 October 2016

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A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation

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Most cited references 29

Multigeneration analysis reveals the inheritance, specificity, and patterns of CRISPR/Cas-induced gene modifications in Arabidopsis.

The origin and behavior of mutable loci in maize.

Active DNA demethylation mediated by DNA glycosylases.

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