Abstract
Regulation of cytosine methylation in the plant genome is of pivotal in determining the epigenetic states of chromosome regions. Relative tolerance of plant to deficiency in cytosine methylation provides unparalleled opportunities to study the mechanism for regulation of cytosine methylation. The Decrease in DNA Methylation 1 (DDM1) of Arabidopsis thaliana is one of the best characterized plant epigenetic regulators that are necessary for maintenance of cytosine methylation in genomic DNA. Although cytosine methylation could affect various aspects of plant growth and development including those related to agricultural importance, orthologs of DDM1 in plants other than Arabidopsis has not been studied in detail. In this study, we identified two rice genes with similarity to Arabidopsis DDM1 and designated them OsDDM1a and OsDDM1b. Both of the rice DDM1 homologs are transcribed during development and their amino acid sequences are 93 % identical to each other. Transgenic rice lines expressing the OsDDM1a cDNA in the antisense orientation exhibited genomic DNA hypomethylation. In those lines, repeated sequences were more severely affected than a single copy sequence as is the case in Arabidopsis ddm1 mutants. Transcripts derived from endogenous transposon-related loci were up-regulated in the antisense OsDDM1 lines, opening a possibility to identify and utilize potentially active transposons for rice functional genomics.
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References
Brzeski J, Jerzmanowski A (2003) Deficient in DNA Methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J Biol Chem 278:823–828
Cheng Z, Dong F, Langdon T, Ouyang S, Buell CR, Gu M, Blattner FR, Jiang J (2002) Functional rice centromeres are marked by a satellite repeat and a centromere-specific retrotransposon. Plant Cell 14:1691–1704
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
Dennis K, Fan T, Geiman T, Yan Q, Muegge K (2001) Lsh, a member of the SNF2 family, is required for genome-wide methylation. Genes Dev 15:2940–2944
Finnegan EJ, Peacock J, Dennis E (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci USA 93:8449–8454
Habu Y, Mathieu O, Tariq M, Probst AV, Smathajitt C, Zhu T, Paszkowski J (2006) Epigenetic regulation of transcription in intermediate heterochromatin. EMBO Rep 7:1279–1284
Hirochika H (2001) Contribution of the Tos17 retrotransposon to rice functional genomics. Curr Opin Plant Biol 4:118–122
Hirochika H, Fukuchi A, Kikuchi F (1992) Retrotransposon families in rice. Mol Gen Genet 233:209–216
Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci USA 93:7783–7788
Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12:357–369
Huang J, Zhang K, Shen Y, Huang Z, Li M, Tang D, Gu M, Chang Z (2009) Identification of a high frequency transposon induced by tissue culture, nDaiZ, a member of the hAT family in rice. Genomics 93:274–281
Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94–97
Johnson L, Cao X, Jacobsen S (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12:1360
Kakutani T, Jeddeloh J, Flowers S, Munakata K, Richards E (1996) Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci USA 93:12406–12411
Kankel MW, Ramsey DE, Stokes TL, Flowers SK, Haag JR, Jeddeloh JA, Riddle NC, Verbsky ML, Richards EJ (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–1122
Kouzminova EA, Selker EU (2001) dim-2 encodes a DNA methyltransferase responsible for all known cytosine methylation in Neurospora. EMBO J 20:4309–4323
Kurata N, Nagamura Y, Yamamoto K, Harushima Y, Sue WuJ, Antonio BA, Shomura A, Shimizu T, Lin S-Y, Inoue T, Fukuda A, Shimano T, Kuboki Y, Toyama T, Miyamoto Y, Kirihara T, Hayasaka K, Miyao A, Monna L, Zhong HS, Tamura Y, Wang Z-X, Momma T, Umehara Y, Yano M, Sasaki T, Minobe Y (1994) A 300 kilobase interval genetic map of rice including 883 expressed sequences. Nat Genet 8:365–372
Li E, Bestor TH, Jaenisch R (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915–926
Lindroth AM, Cao X, Jackson JP, Zilberman D, McCallum CM, Henikoff S, Jacobsen SE (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080
Lippman Z, May B, Yordan C, Singer T, Martienssen R (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1:E67
Lippman Z, Gendrel A-V, Black M, Vaughn MA, Dedhia N, McCombie WR, Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V, Martienssen R (2004) Roles of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476
Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214
Miura A, Kato M, Watanabe K, Kawabe A, Kotani H, Kakutani T (2004) Genomic localization of endogenous mobile CACTA family transposons in natural variants of Arabidopsis thaliana. Mol Genet Genomics 270:524–532
Naito K, Cho E, Tang G, Campbell MA, Yano K, Okumoto Y, Tanisaka T, Wessler SR (2006) Dramatic amplification of a rice transposable element during recent domestication. Proc Natl Acad Sci USA 103:17620–17625
Ronemus MJ, Galbiati M, Ticknor C, Chen J, Dellaporta SL (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science 273:654–657
Sato Y, Antonio B, Namiki N, Motoyama R, Sugimoto K, Takehisa H, Minami H, Kamatsuki K, Kusaba M, Hirochika H, Nagamura Y (2011) Field transcriptome revealed critical developmental and physiological transitions involved in the expression of growth potential in japonica rice. BMC Plant Biol 11:10
Saze H, Scheid OM, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34:65–69
Singer T, Yordan C, Martienssen RA (2001) Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev 15:591–602
Steimer A, Amedeo P, Afsar K, Fransz P, Mittelsten Scheid O, Paszkowski J (2000) Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12:1165–1178
Takaiwa F, Kikuchi S, Ohno K (1990) The complete nucleotide sequence of the intergenic spacer between 25S and 17S rDNAs in rice. Plant Mol Biol 15:933–935
Toki S (1997) Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Mol Biol Rep 15:16–21
Tsugane K, Maekawa M, Takagi K, Takahara H, Qian Q, Eun CH, Iida S (2006) An active DNA transposon nDart causing leaf variegation and mutable dwarfism and its related elements in rice. Plant J 45:46–57
Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:423–426
Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928
Walbot V (2000) Saturation mutagenesis using maize transposons. Curr Opin Plant Biol 3:103–107
Acknowledgments
We thank Y. Iguchi, K. Munakata, A. Terui, K. Hioki, and M. Arai for technical assistance. Special thanks to S. Iida for comments on the manuscript, H. Hirochika, H. Ohtsubo, F. Takaiwa, and S. Tsuchimoto for rice DNA clones and sequences used for probes. This work was supported by Grant-in-Aid for Creative Scientific Research 14GS0321 to TK and for Scientific Research (C) 24580016 to YH.
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Communicated by S. Hohmann.
H. Higo and M. Tahir contributed equally to this work.
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Higo, H., Tahir, M., Takashima, K. et al. DDM1 (Decrease in DNA Methylation) genes in rice (Oryza sativa). Mol Genet Genomics 287, 785–792 (2012). https://doi.org/10.1007/s00438-012-0717-5
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DOI: https://doi.org/10.1007/s00438-012-0717-5