AtHDA6 functions as an H3K18ac eraser to maintain pericentromeric CHG methylation in Arabidopsis thaliana

Qianwen Wang; Xiucong Bao; Shengjie Chen; Huan Zhong; Yaqin Liu; Li Zhang; Yiji Xia; Friedrich Kragler; Ming Luo; Xiang David Li; Hon Ming Lam; Shoudong Zhang

doi:10.1093/nar/gkab706

AtHDA6 functions as an H3K18ac eraser to maintain pericentromeric CHG methylation in Arabidopsis thaliana

Qianwen Wang, Xiucong Bao, Shengjie Chen, Huan Zhong, Yaqin Liu, Li Zhang, Yiji Xia, Friedrich Kragler, Ming Luo^*, Xiang David Li^*, Hon Ming Lam^*, Shoudong Zhang^*

^*Corresponding author for this work

Research output: Contribution to journal › Journal article › peer-review

7 Citations (Scopus)

Abstract

Pericentromeric DNA, consisting of high-copy-number tandem repeats and transposable elements, is normally silenced through DNA methylation and histone modifications to maintain chromosomal integrity and stability. Although histone deacetylase 6 (HDA6) has been known to participate in pericentromeric silencing, the mechanism is still yet unclear. Here, using whole genome bisulfite sequencing (WGBS) and chromatin immunoprecipitation-sequencing (ChIP-Seq), we mapped the genome-wide patterns of differential DNA methylation and histone H3 lysine 18 acetylation (H3K18ac) in wild-type and hda6 mutant strains. Results show pericentromeric CHG hypomethylation in hda6 mutants was mediated by DNA demethylases, not by DNA methyltransferases as previously thought. DNA demethylases can recognize H3K18ac mark and then be recruited to the chromatin. Using biochemical assays, we found that HDA6 could function as an 'eraser' enzyme for H3K18ac mark to prevent DNA demethylation. Oxford Nanopore Technology Direct RNA Sequencing (ONT DRS) also revealed that hda6 mutants with H3K18ac accumulation and CHG hypomethylation were shown to have transcriptionally active pericentromeric DNA.

Original language	English
Pages (from-to)	9755-9767
Number of pages	13
Journal	Nucleic Acids Research
Volume	49
Issue number	17
Early online date	17 Aug 2021
DOIs	https://doi.org/10.1093/nar/gkab706
Publication status	Published - 27 Sept 2021

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Genetics

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10.1093/nar/gkab706

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@article{7d1776c0a960440ca9b78f91a82a6235,

title = "AtHDA6 functions as an H3K18ac eraser to maintain pericentromeric CHG methylation in Arabidopsis thaliana",

abstract = "Pericentromeric DNA, consisting of high-copy-number tandem repeats and transposable elements, is normally silenced through DNA methylation and histone modifications to maintain chromosomal integrity and stability. Although histone deacetylase 6 (HDA6) has been known to participate in pericentromeric silencing, the mechanism is still yet unclear. Here, using whole genome bisulfite sequencing (WGBS) and chromatin immunoprecipitation-sequencing (ChIP-Seq), we mapped the genome-wide patterns of differential DNA methylation and histone H3 lysine 18 acetylation (H3K18ac) in wild-type and hda6 mutant strains. Results show pericentromeric CHG hypomethylation in hda6 mutants was mediated by DNA demethylases, not by DNA methyltransferases as previously thought. DNA demethylases can recognize H3K18ac mark and then be recruited to the chromatin. Using biochemical assays, we found that HDA6 could function as an 'eraser' enzyme for H3K18ac mark to prevent DNA demethylation. Oxford Nanopore Technology Direct RNA Sequencing (ONT DRS) also revealed that hda6 mutants with H3K18ac accumulation and CHG hypomethylation were shown to have transcriptionally active pericentromeric DNA.",

author = "Qianwen Wang and Xiucong Bao and Shengjie Chen and Huan Zhong and Yaqin Liu and Li Zhang and Yiji Xia and Friedrich Kragler and Ming Luo and Li, {Xiang David} and Lam, {Hon Ming} and Shoudong Zhang",

note = "Funding information: Hong Kong Research Grants Council Area of Excellence Scheme [AoE/M-403/16 to H.-M.L., Y.X., AoE/P-705/16 to X.D.L.]; Key-Areas Research and Development Program of Guangdong Province [2020B020220004 to M.L.]; Youth Innovation Promotion Association; Chinese Academy of Sciences [2017399 to M.L.]; Science and Technology Program of Guangzhou [202002030097 to M.L.]; National Natural Science Foundation of China [91753203, 91753130 to X.D.L.]; Excellent Young Scientists Fund of China (Hong Kong and Macau) [21922708 to X.D.L.]; Hong Kong Research Grants Council (RGC) Collaborative Research Fund [CRF C7029-15G, C7017-18G to X.D.L.]; General Research Fund [GRF 17121120, 17126618, 17125917 to X.D.L.]; Lo Kwee-Seong Biomedical Research Fund (to H.-M.L.); CUHK direct grant [CUHK4053383, CUHK4053442 to S.Z.]; European Research Council [ERCsyg PLAMORF 810131 to F.K.). Funding for open access charge: Hong Kong Research Grants Council Area of Excellence Scheme [AoE/M-403/16]. Publisher Copyright: {\textcopyright} The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.",

year = "2021",

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doi = "10.1093/nar/gkab706",

language = "English",

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T1 - AtHDA6 functions as an H3K18ac eraser to maintain pericentromeric CHG methylation in Arabidopsis thaliana

AU - Wang, Qianwen

AU - Bao, Xiucong

AU - Chen, Shengjie

AU - Zhong, Huan

AU - Liu, Yaqin

AU - Zhang, Li

AU - Xia, Yiji

AU - Kragler, Friedrich

AU - Luo, Ming

AU - Li, Xiang David

AU - Lam, Hon Ming

AU - Zhang, Shoudong

N1 - Funding information: Hong Kong Research Grants Council Area of Excellence Scheme [AoE/M-403/16 to H.-M.L., Y.X., AoE/P-705/16 to X.D.L.]; Key-Areas Research and Development Program of Guangdong Province [2020B020220004 to M.L.]; Youth Innovation Promotion Association; Chinese Academy of Sciences [2017399 to M.L.]; Science and Technology Program of Guangzhou [202002030097 to M.L.]; National Natural Science Foundation of China [91753203, 91753130 to X.D.L.]; Excellent Young Scientists Fund of China (Hong Kong and Macau) [21922708 to X.D.L.]; Hong Kong Research Grants Council (RGC) Collaborative Research Fund [CRF C7029-15G, C7017-18G to X.D.L.]; General Research Fund [GRF 17121120, 17126618, 17125917 to X.D.L.]; Lo Kwee-Seong Biomedical Research Fund (to H.-M.L.); CUHK direct grant [CUHK4053383, CUHK4053442 to S.Z.]; European Research Council [ERCsyg PLAMORF 810131 to F.K.). Funding for open access charge: Hong Kong Research Grants Council Area of Excellence Scheme [AoE/M-403/16]. Publisher Copyright: © The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.

PY - 2021/9/27

Y1 - 2021/9/27

N2 - Pericentromeric DNA, consisting of high-copy-number tandem repeats and transposable elements, is normally silenced through DNA methylation and histone modifications to maintain chromosomal integrity and stability. Although histone deacetylase 6 (HDA6) has been known to participate in pericentromeric silencing, the mechanism is still yet unclear. Here, using whole genome bisulfite sequencing (WGBS) and chromatin immunoprecipitation-sequencing (ChIP-Seq), we mapped the genome-wide patterns of differential DNA methylation and histone H3 lysine 18 acetylation (H3K18ac) in wild-type and hda6 mutant strains. Results show pericentromeric CHG hypomethylation in hda6 mutants was mediated by DNA demethylases, not by DNA methyltransferases as previously thought. DNA demethylases can recognize H3K18ac mark and then be recruited to the chromatin. Using biochemical assays, we found that HDA6 could function as an 'eraser' enzyme for H3K18ac mark to prevent DNA demethylation. Oxford Nanopore Technology Direct RNA Sequencing (ONT DRS) also revealed that hda6 mutants with H3K18ac accumulation and CHG hypomethylation were shown to have transcriptionally active pericentromeric DNA.

AB - Pericentromeric DNA, consisting of high-copy-number tandem repeats and transposable elements, is normally silenced through DNA methylation and histone modifications to maintain chromosomal integrity and stability. Although histone deacetylase 6 (HDA6) has been known to participate in pericentromeric silencing, the mechanism is still yet unclear. Here, using whole genome bisulfite sequencing (WGBS) and chromatin immunoprecipitation-sequencing (ChIP-Seq), we mapped the genome-wide patterns of differential DNA methylation and histone H3 lysine 18 acetylation (H3K18ac) in wild-type and hda6 mutant strains. Results show pericentromeric CHG hypomethylation in hda6 mutants was mediated by DNA demethylases, not by DNA methyltransferases as previously thought. DNA demethylases can recognize H3K18ac mark and then be recruited to the chromatin. Using biochemical assays, we found that HDA6 could function as an 'eraser' enzyme for H3K18ac mark to prevent DNA demethylation. Oxford Nanopore Technology Direct RNA Sequencing (ONT DRS) also revealed that hda6 mutants with H3K18ac accumulation and CHG hypomethylation were shown to have transcriptionally active pericentromeric DNA.

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DO - 10.1093/nar/gkab706

M3 - Journal article

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AN - SCOPUS:85117360784

SN - 0305-1048

VL - 49

SP - 9755

EP - 9767

JO - Nucleic Acids Research

JF - Nucleic Acids Research

IS - 17

ER -

AtHDA6 functions as an H3K18ac eraser to maintain pericentromeric CHG methylation in Arabidopsis thaliana

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