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

Handle URI:
http://hdl.handle.net/10754/561871
Title:
A 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in rice
Authors:
La, Honggui; Ding, Bo; Mishra, Gyan Prakash; Zhou, Bo; Yang, Hongmei; Bellizzi, Maria Del Rosario; Chen, Songbiao; Meyers, Blake C.; Peng, Zhaohua; Zhu, Jian-Kang; Wang, Guoliang
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.
KAUST Department:
Center for Desert Agriculture
Publisher:
National Academy of Sciences
Journal:
Proceedings of the National Academy of Sciences of the United States of America
Issue Date:
6-Sep-2011
DOI:
10.1073/pnas.1112704108
PubMed ID:
21896764
PubMed Central ID:
PMC3174586
Type:
Article
ISSN:
00278424
Sponsors:
We thank Drs. Ko Shimamoto and Michael Goodin for providing the pANDA vector and pGDG vector, respectively; Dr. Steven E. Jacobsen for providing the genomic bisulfite sequencing protocol; Dr. Jiming Jiang for providing the centromeric repeat probe; and the Rice Genome Resource Center in Japan for providing the cDNA clones and Tos17 insertion lines. This research is supported by National Institutes of Health Grant R01GM070795 (to J.-K.Z.), and US Department of Agriculture-Cooperative State Research, Education, and Extension Service Grant 2004-05425 and National Science Foundation-Plant Genome Research Program Grants 0321437 and 0701745 (to G.-L.W.).
Additional Links:
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3174586
Appears in Collections:
Articles; Center for Desert Agriculture

Full metadata record

DC FieldValue Language
dc.contributor.authorLa, Hongguien
dc.contributor.authorDing, Boen
dc.contributor.authorMishra, Gyan Prakashen
dc.contributor.authorZhou, Boen
dc.contributor.authorYang, Hongmeien
dc.contributor.authorBellizzi, Maria Del Rosarioen
dc.contributor.authorChen, Songbiaoen
dc.contributor.authorMeyers, Blake C.en
dc.contributor.authorPeng, Zhaohuaen
dc.contributor.authorZhu, Jian-Kangen
dc.contributor.authorWang, Guoliangen
dc.date.accessioned2015-08-03T09:32:56Zen
dc.date.available2015-08-03T09:32:56Zen
dc.date.issued2011-09-06en
dc.identifier.issn00278424en
dc.identifier.pmid21896764en
dc.identifier.doi10.1073/pnas.1112704108en
dc.identifier.urihttp://hdl.handle.net/10754/561871en
dc.description.abstractDNA 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.en
dc.description.sponsorshipWe thank Drs. Ko Shimamoto and Michael Goodin for providing the pANDA vector and pGDG vector, respectively; Dr. Steven E. Jacobsen for providing the genomic bisulfite sequencing protocol; Dr. Jiming Jiang for providing the centromeric repeat probe; and the Rice Genome Resource Center in Japan for providing the cDNA clones and Tos17 insertion lines. This research is supported by National Institutes of Health Grant R01GM070795 (to J.-K.Z.), and US Department of Agriculture-Cooperative State Research, Education, and Extension Service Grant 2004-05425 and National Science Foundation-Plant Genome Research Program Grants 0321437 and 0701745 (to G.-L.W.).en
dc.publisherNational Academy of Sciencesen
dc.relation.urlhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC3174586en
dc.subjectIncision activityen
dc.subjectOryza sativaen
dc.subjectTos17 copy numberen
dc.titleA 5-methylcytosine DNA glycosylase/lyase demethylates the retrotransposon Tos17 and promotes its transposition in riceen
dc.typeArticleen
dc.contributor.departmentCenter for Desert Agricultureen
dc.identifier.journalProceedings of the National Academy of Sciences of the United States of Americaen
dc.identifier.pmcidPMC3174586en
dc.contributor.institutionDepartment of Plant Pathology, Ohio State University, Columbus, OH 43210, United Statesen
dc.contributor.institutionDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, United Statesen
dc.contributor.institutionDepartment of Plant and Soil Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, DE 19711, United Statesen
dc.contributor.institutionDepartment of Biochemistry and Molecular Biology, Mississippi State University, MS 39762, United Statesen
dc.contributor.institutionState Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, Chinaen
kaust.authorZhu, Jian-Kangen

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