A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice

Honggui La; Bo Ding; Gyan P. Mishra; Bo Zhou; Hongmei Yang; Maria Del Rosario Bellizzi; Songbiao Chen; Blake C. Meyers; Zhaohua Peng; Jian Kang Zhu; Guo Liang Wang

doi:10.1073/pnas.1112704108

A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice

Honggui La, Bo Ding, Gyan P. Mishra, Bo Zhou, Hongmei Yang, Maria Del Rosario Bellizzi, Songbiao Chen, Blake C. Meyers, Zhaohua Peng, Jian Kang Zhu, Guo Liang Wang

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84 Scopus citations

Abstract

DNA 5-methylcytosine (5-meC) is an important epigenetic mark for transcriptional gene silencing in many eukaryotes. In Arabidopsis, 5-meC DNA glycosylase/lyases actively remove 5-meC to counter-act transcriptional gene silencing in a locus-specific manner, and have been suggested to maintain the expression of transposons. However, it is unclear whether plant DNA demethylases can promote the transposition of transposons. Here we report the functional characterization of the DNA glycosylase/lyase DNG701 in rice. DNG701 encodes a large (1,812 amino acid residues) DNA glycosylase domain protein. Recombinant DNG701 protein showed 5-meC DNA glycosylase and lyase activities in vitro. Knockout or knockdown of DNG701 in rice plants led to DNA hypermethylation and reduced expression of the retrotransposon Tos17. Tos17 showed less transposition in calli derived from dng701 knockout mutant seeds compared with that in wild-type calli. Overexpression of DNG701 in both rice calli and transgenic plants substantially reduced DNA methylation levels of Tos17 and enhanced its expression. The overexpression also led to more frequent transposition of Tos17 in calli. Our results demonstrate that rice DNG701 is a 5-meC DNA glycosylase/lyase responsible for the demethylation of Tos17 and this DNA demethylase plays a critical role in promoting Tos17 transposition in rice calli.

Original language	English
Pages (from-to)	15498-15503
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	108
Issue number	37
DOIs	https://doi.org/10.1073/pnas.1112704108
State	Published - Sep 13 2011

Keywords

Incision activity
Oryza sativa
Tos17 copy number

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10.1073/pnas.1112704108

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La, H., Ding, B., Mishra, G. P., Zhou, B., Yang, H., Bellizzi, M. D. R., Chen, S., Meyers, B. C., Peng, Z., Zhu, J. K., & Wang, G. L. (2011). A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice. Proceedings of the National Academy of Sciences of the United States of America, 108(37), 15498-15503. https://doi.org/10.1073/pnas.1112704108

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title = "A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice",

abstract = "DNA 5-methylcytosine (5-meC) is an important epigenetic mark for transcriptional gene silencing in many eukaryotes. In Arabidopsis, 5-meC DNA glycosylase/lyases actively remove 5-meC to counter-act transcriptional gene silencing in a locus-specific manner, and have been suggested to maintain the expression of transposons. However, it is unclear whether plant DNA demethylases can promote the transposition of transposons. Here we report the functional characterization of the DNA glycosylase/lyase DNG701 in rice. DNG701 encodes a large (1,812 amino acid residues) DNA glycosylase domain protein. Recombinant DNG701 protein showed 5-meC DNA glycosylase and lyase activities in vitro. Knockout or knockdown of DNG701 in rice plants led to DNA hypermethylation and reduced expression of the retrotransposon Tos17. Tos17 showed less transposition in calli derived from dng701 knockout mutant seeds compared with that in wild-type calli. Overexpression of DNG701 in both rice calli and transgenic plants substantially reduced DNA methylation levels of Tos17 and enhanced its expression. The overexpression also led to more frequent transposition of Tos17 in calli. Our results demonstrate that rice DNG701 is a 5-meC DNA glycosylase/lyase responsible for the demethylation of Tos17 and this DNA demethylase plays a critical role in promoting Tos17 transposition in rice calli.",

keywords = "Incision activity, Oryza sativa, Tos17 copy number",

author = "Honggui La and Bo Ding and Mishra, {Gyan P.} and Bo Zhou and Hongmei Yang and Bellizzi, {Maria Del Rosario} and Songbiao Chen and Meyers, {Blake C.} and Zhaohua Peng and Zhu, {Jian Kang} and Wang, {Guo Liang}",

year = "2011",

month = sep,

day = "13",

doi = "10.1073/pnas.1112704108",

language = "English",

volume = "108",

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La, H, Ding, B, Mishra, GP, Zhou, B, Yang, H, Bellizzi, MDR, Chen, S, Meyers, BC, Peng, Z, Zhu, JK & Wang, GL 2011, 'A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 37, pp. 15498-15503. https://doi.org/10.1073/pnas.1112704108

TY - JOUR

T1 - A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice

AU - La, Honggui

AU - Ding, Bo

AU - Mishra, Gyan P.

AU - Zhou, Bo

AU - Yang, Hongmei

AU - Bellizzi, Maria Del Rosario

AU - Chen, Songbiao

AU - Meyers, Blake C.

AU - Peng, Zhaohua

AU - Zhu, Jian Kang

AU - Wang, Guo Liang

PY - 2011/9/13

Y1 - 2011/9/13

N2 - DNA 5-methylcytosine (5-meC) is an important epigenetic mark for transcriptional gene silencing in many eukaryotes. In Arabidopsis, 5-meC DNA glycosylase/lyases actively remove 5-meC to counter-act transcriptional gene silencing in a locus-specific manner, and have been suggested to maintain the expression of transposons. However, it is unclear whether plant DNA demethylases can promote the transposition of transposons. Here we report the functional characterization of the DNA glycosylase/lyase DNG701 in rice. DNG701 encodes a large (1,812 amino acid residues) DNA glycosylase domain protein. Recombinant DNG701 protein showed 5-meC DNA glycosylase and lyase activities in vitro. Knockout or knockdown of DNG701 in rice plants led to DNA hypermethylation and reduced expression of the retrotransposon Tos17. Tos17 showed less transposition in calli derived from dng701 knockout mutant seeds compared with that in wild-type calli. Overexpression of DNG701 in both rice calli and transgenic plants substantially reduced DNA methylation levels of Tos17 and enhanced its expression. The overexpression also led to more frequent transposition of Tos17 in calli. Our results demonstrate that rice DNG701 is a 5-meC DNA glycosylase/lyase responsible for the demethylation of Tos17 and this DNA demethylase plays a critical role in promoting Tos17 transposition in rice calli.

AB - DNA 5-methylcytosine (5-meC) is an important epigenetic mark for transcriptional gene silencing in many eukaryotes. In Arabidopsis, 5-meC DNA glycosylase/lyases actively remove 5-meC to counter-act transcriptional gene silencing in a locus-specific manner, and have been suggested to maintain the expression of transposons. However, it is unclear whether plant DNA demethylases can promote the transposition of transposons. Here we report the functional characterization of the DNA glycosylase/lyase DNG701 in rice. DNG701 encodes a large (1,812 amino acid residues) DNA glycosylase domain protein. Recombinant DNG701 protein showed 5-meC DNA glycosylase and lyase activities in vitro. Knockout or knockdown of DNG701 in rice plants led to DNA hypermethylation and reduced expression of the retrotransposon Tos17. Tos17 showed less transposition in calli derived from dng701 knockout mutant seeds compared with that in wild-type calli. Overexpression of DNG701 in both rice calli and transgenic plants substantially reduced DNA methylation levels of Tos17 and enhanced its expression. The overexpression also led to more frequent transposition of Tos17 in calli. Our results demonstrate that rice DNG701 is a 5-meC DNA glycosylase/lyase responsible for the demethylation of Tos17 and this DNA demethylase plays a critical role in promoting Tos17 transposition in rice calli.

KW - Incision activity

KW - Oryza sativa

KW - Tos17 copy number

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U2 - 10.1073/pnas.1112704108

DO - 10.1073/pnas.1112704108

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SN - 0027-8424

VL - 108

SP - 15498

EP - 15503

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 37

ER -

A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice

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