Epigenetic Regulation of the Rice Retrotransposon Tos17

Overview

Journal Mol Genet Genomics

Specialty Genetics

Date 2006 Jul 6

PMID 16821043

Citations 48

Authors

Chaoyang Cheng

Masaaki Daigen

Hirohiko Hirochika

Affiliations

Soon will be listed here.

Abstract

Transposable elements are major components of plant genomes. Their activity seems to be epigenetically regulated by gene silencing systems. Here we report epigenetic variation in the retrotransposon Tos17 activity in rice varieties. Of the two copies of Tos17 present in chromosome 7 (Tos17 (chr.7)) and chromosome 10 (Tos17 (chr.10)), Tos17 (chr.7) is strongly activated by tissue culture in most varieties including Nipponbare except for Moritawase, despite the identity of the DNA sequences in Moritawase and Nipponbare. Tos17 (chr.7) activity correlated with its methylation status, and Tos17 (chr.7 )in Moritawase was heavily methylated and activated by treatment of 5-azacytidine (5-azaC), a DNA methylation inhibitor. Although the original copies of Tos17 are methylated to some extent in all varieties examined, the transposed copies in calli mostly are not methylated. When plants were regenerated from calli, the degree of methylation of the Tos17 DNA increased gradually with the growth of plants, and a significant progress of DNA methylation occurred in the next generation after a completed reproductive cycle. With increasing DNA methylation, the transcription of transposed and original Tos17 copies driven by its own as well as by a flanking gene promoter were suppressed. We conclude that Tos17 DNA methylation controls the transpositional activity of Tos17, and modulates the activity of neighboring genes. Based on the analysis of the inactive Tos17 (chr.10), we propose that another mechanism, called transcriptional interference, is involved in the control of Tos17 activity.

Citing Articles

Epigenetic regulation of organ-specific functions in Mikania micrantha and Mikania cordata: insights from DNA methylation and siRNA integration.

Sang Y, Ma Y, Wang R, Wang Z, Wang T, Su Y BMC Plant Biol. 2024; 24(1):1142.

PMID: 39609688 PMC: 11605950. DOI: 10.1186/s12870-024-05858-z.

Insights into plant regeneration: cellular pathways and DNA methylation dynamics.

Lee S, Park Y, Rhee J, Chu H, Frost J, Choi Y Plant Cell Rep. 2024; 43(5):120.

PMID: 38634973 PMC: 11026228. DOI: 10.1007/s00299-024-03216-9.

Blessing or curse: how the epigenetic resolution of host-transposable element conflicts shapes their evolutionary dynamics.

Huang Y, Lee Y Proc Biol Sci. 2024; 291(2020):20232775.

PMID: 38593848 PMC: 11003778. DOI: 10.1098/rspb.2023.2775.

A review of the pangenome: how it affects our understanding of genomic variation, selection and breeding in domestic animals?.

Gong Y, Li Y, Liu X, Ma Y, Jiang L J Anim Sci Biotechnol. 2023; 14(1):73.

PMID: 37143156 PMC: 10161434. DOI: 10.1186/s40104-023-00860-1.

Transposable element finder (TEF): finding active transposable elements from next generation sequencing data.

Miyao A, Yamanouchi U BMC Bioinformatics. 2022; 23(1):500.

PMID: 36418944 PMC: 9682801. DOI: 10.1186/s12859-022-05011-3.

References

Yamazaki M, Tsugawa H, Miyao A, Yano M, Wu J, Yamamoto S . The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets. Mol Genet Genomics. 2001; 265(2):336-44. DOI: 10.1007/s004380000421. View

Kashkush K, Feldman M, Levy A . Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet. 2002; 33(1):102-6. DOI: 10.1038/ng1063. View

McCLINTOCK B . The significance of responses of the genome to challenge. Science. 1984; 226(4676):792-801. DOI: 10.1126/science.15739260. View

Kanno T, Huettel B, Mette M, Aufsatz W, Jaligot E, Daxinger L . Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet. 2005; 37(7):761-5. DOI: 10.1038/ng1580. View

Takeda S, Sugimoto K, Otsuki H, Hirochika H . Transcriptional activation of the tobacco retrotransposon Tto1 by wounding and methyl jasmonate. Plant Mol Biol. 1998; 36(3):365-76. DOI: 10.1023/a:1005911413528. View

Kikuchi K, Terauchi K, Wada M, Hirano H . The plant MITE mPing is mobilized in anther culture. Nature. 2003; 421(6919):167-70. DOI: 10.1038/nature01218. View

Sugimoto K, Takeda S, Hirochika H . MYB-related transcription factor NtMYB2 induced by wounding and elicitors is a regulator of the tobacco retrotransposon Tto1 and defense-related genes. Plant Cell. 2001; 12(12):2511-2528. PMC: 102234. DOI: 10.1105/tpc.12.12.2511. View

Adhya S, Gottesman M . Promoter occlusion: transcription through a promoter may inhibit its activity. Cell. 1982; 29(3):939-44. DOI: 10.1016/0092-8674(82)90456-1. View

Lindroth A, Cao X, Jackson J, Zilberman D, McCALLUM C, Henikoff S . Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science. 2001; 292(5524):2077-80. DOI: 10.1126/science.1059745. View

10.

Hirochika H, Guiderdoni E, An G, Hsing Y, Eun M, Han C . Rice mutant resources for gene discovery. Plant Mol Biol. 2004; 54(3):325-34. DOI: 10.1023/B:PLAN.0000036368.74758.66. View

11.

Nakazaki T, Okumoto Y, Horibata A, Yamahira S, Teraishi M, Nishida H . Mobilization of a transposon in the rice genome. Nature. 2003; 421(6919):170-2. DOI: 10.1038/nature01219. View

12.

Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T . Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature. 2001; 411(6834):212-4. DOI: 10.1038/35075612. View

13.

Martienssen R, Colot V . DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science. 2001; 293(5532):1070-4. DOI: 10.1126/science.293.5532.1070. View

14.

McCarthy E, Liu J, Lizhi G, McDonald J . Long terminal repeat retrotransposons of Oryza sativa. Genome Biol. 2002; 3(10):RESEARCH0053. PMC: 134482. DOI: 10.1186/gb-2002-3-10-research0053. View

15.

Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M . Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A. 1996; 93(15):7783-8. PMC: 38825. DOI: 10.1073/pnas.93.15.7783. View

16.

Jiang N, Bao Z, Zhang X, Hirochika H, Eddy S, McCouch S . An active DNA transposon family in rice. Nature. 2003; 421(6919):163-7. DOI: 10.1038/nature01214. View

17.

Feschotte C, Jiang N, Wessler S . Plant transposable elements: where genetics meets genomics. Nat Rev Genet. 2002; 3(5):329-41. DOI: 10.1038/nrg793. View

18.

Komatsu M, Shimamoto K, Kyozuka J . Two-step regulation and continuous retrotransposition of the rice LINE-type retrotransposon Karma. Plant Cell. 2003; 15(8):1934-44. PMC: 167180. DOI: 10.1105/tpc.011809. View

19.

Kiger A, Gigliotti S, Fuller M . Developmental genetics of the essential Drosophila nucleoporin nup154: allelic differences due to an outward-directed promoter in the P-element 3' end. Genetics. 1999; 153(2):799-812. PMC: 1460801. DOI: 10.1093/genetics/153.2.799. View

20.

Meyers B, Tingey S, Morgante M . Abundance, distribution, and transcriptional activity of repetitive elements in the maize genome. Genome Res. 2001; 11(10):1660-76. PMC: 311155. DOI: 10.1101/gr.188201. View