Targeted disruption of an orthologue of DOMAINS REARRANGED METHYLASE 2, OsDRM2, impairs the growth of rice plants by abnormal DNA methylation

Plant Journal

Volumn 71, Issue 1, 2012, Pages 85-98

  Moritoh, Satoru ^a,b   Eun, Chang Ho ^a,c   Ono, Akemi ^a,d   Asao, Hisayo ^a   Okano, Yosuke ^a,e   Yamaguchi, Katsushi ^a   Shimatani, Zenpei ^a,f   Koizumi, Amane ^b   Terada, Rie ^a,f  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c GREGOR MENDEL INSTITUTE OF MOLECULAR PLANT BIOLOGY   (Austria)

^d NAGOYA UNIVERSITY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f MEIJO UNIVERSITY   (Japan)

Author keywords

development; DNA methylation; DOMAINS REARRANGED METHYLASE 1 2 (DRM1 2); gene targeting (GT); homologous recombination (HR); rice (Oryza sativa)

Indexed keywords

DEVELOPMENT; DNA METHYLATION; GENE TARGETING; HOMOLOGOUS RECOMBINATION; RICE (ORYZA SATIVA);

GENES; GENETIC ENGINEERING; METHYLATION; PLANTS (BOTANY); RNA;

ALKYLATION;

METHYLTRANSFERASE; PLANT DNA; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; DNA METHYLATION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RETROPOSON; RICE;

ARABIDOPSIS; CLONING, MOLECULAR; DNA METHYLATION; DNA, PLANT; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENETIC COMPLEMENTATION TEST; METHYLTRANSFERASES; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PLANT PROTEINS; RETROELEMENTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ORYZA SATIVA;

EID: 84862580050     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04974.x     Document Type: Article

References (68)

1. Akama, K., and, Kashihara, M., (1996) Plant nuclear tRNA Met genes ubiquitously interrupted by introns. Plant Mol. Biol. 32, 427-434.
2. Alleman, M., Sidorenko, L., McGinnis, K., Seshadri, V., Dorweiler, J.E., White, J., Sikkink, K., and, Chandler, V.L., (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature, 442, 295-298. (Pubitemid 44114903)
3. Bartee, L., Malagnac, F., and, Bender, J., (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15, 1753-1758. (Pubitemid 32905632)
4. Cao, X., and, Jacobsen, S.E., (2002a) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12, 1138-1144. (Pubitemid 34766938)
5. Cao, X., and, Jacobsen, S.E., (2002b) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methytransferse genes. Proc. Natl Acad. Sci. USA, 99, 16491-16498. (Pubitemid 35470998)
6. Cao, X., Springer, N.M., Muszynski, M.G., Phillips, R.L., Kaeppler, S., and, Jacobsen, S.E., (2000) Conserved plant genes with similarity to mammalian de novo methyltransferases. Proc. Natl Acad. Sci. USA, 97, 4979-4984. (Pubitemid 30238668)
7. Cao, X., Aufsatz, W., Zilberman, D., Mette, M.F., Huang, M.S., Matzke, M., and, Jacobsen, S.E., (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13, 2212-2217. (Pubitemid 38024949)
8. Chan, S.W., Zilberman, D., Xie, Z., Johansen, L.K., Carrington, J.C., and, Jacobsen, S.E., (2004) RNA silencing genes control de novo DNA methylation. Science, 303, 1336. (Pubitemid 38269419)
9. Chan, S.W., Henderson, I.R., Zhang, X., Shah, G., Chien, J.S., and, Jacobsen, S.E., (2006) RNAi, DRD1, and histone methylation actively target developmentally important non-CG methylation in Arabidopsis. PLoS Genet. 2, e83.
10. Chen, H., Samadder, P.P., Tanaka, Y., et al. (2008) OsRecQ1, a QDE-3 homologue in rice, is required for RNA silencing induced by particle bombardment for inverted repeat DNA, but not for double-stranded RNA. Plant J. 56, 274-286.
11. Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M., and, Jacobsen, S., (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature, 452, 215-219. (Pubitemid 351380251)
12. Erhard, K.F. Jr, Stonaker, J.L., Parkinson, S.E., Lim, J.P., Hale, C.J., and, Hollick, J.B., (2009) RNA polymerase IV functions in paramutation in Zea mays. Science, 323, 1201-1205.
13. Finnegan, E.J., and, Dennis, E.S., (1993) Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana. Nucleic Acids Res. 21, 2383-2388. (Pubitemid 23180815)
14. Finnegan, E.J., Peacock, W.J., and, Dennis, E.S., (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl Acad. Sci. USA, 93, 8849-8854.
15. Garcia-Aguilar, M., Michaud, C., Leblanc, O., and, Grimanelli, D., (2010) Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell, 22, 3249-3267.
16. Goto, S., Mano, S., Nakamori, C., and, Nishimura, M., (2011) Arabidopsis ABERRANT PEROXISOME MORPHOLOGY9 is a peroxin that recruits the PEX1-PEX6 complex to peroxisomes. Plant Cell, 23, 1573-1587.
17. Greenberg, M.V., Ausin, I., Chan, S.W., et al. (2011) Identification of genes required for de novo DNA methylation in Arabidopsis. Epigenetics, 6, 344-354.
18. Gutiérrez-Marcos, J.F., Costa, L.M., Dal Prà, M., Scholten, S., Kranz, E., Perez, P., and, Dickinson, H.G., (2006) Epigentic asymmetry of imprinted genes in plant gametes. Nat. Genet. 38, 876-878. (Pubitemid 44141654)
19. He, G., Zhu, X., Elling, A.A., et al. (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell, 22, 17-33.
20. He, X.J., Chen, T., and, Zhu, J.K., (2011) Regulation and function of DNA methylation in plants and animals. Cell Res. 21, 442-465.
21. Henderson, I.R., and, Jacobsen, S.E., (2008) Tandem repeats upstream of the Arabidopsis endogenous SDC recruit non-CG methylation and initiate siRNA spreading. Genes Dev. 22, 1597-1606. (Pubitemid 351846840)
22. International Rice Genome Sequencing Project. (2005) The map-based sequence of the rice genome. Nature, 436, 793-800.
23. Jacobsen, S.E., and, Meyerowitz, E.M., (1997) Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science, 277, 1100-1103. (Pubitemid 27371632)
24. Jacobsen, S.E., Sakai, H., Finnegan, E.J., Cao, X., and, Meyerowitz, E.M., (2000) Ectopic hypermethylation of flower-specific genes in Arabidopsis. Curr. Biol. 10, 179-186. (Pubitemid 30146782)
25. Jeddeloh, J.A., Stokes, T.L., and, Richards, E.J., (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat. Genet. 22, 94-97. (Pubitemid 29214813)
26. Kakutani, T., Jeddeloh, J.A., Flowers, S.K., Munakata, K., and, Richards, E.J., (1996) Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc. Natl Acad. Sci. USA, 93, 12406-12411. (Pubitemid 26367156)
27. Kankel, M.W., Ramsey, D.E., Stokes, T.L., Flowers, S.K., Haag, J.R., Jeddeloh, J.A., Riddle, N.C., Verbsky, M.L., and, Richards, E.J., (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics, 163, 1109-1122. (Pubitemid 36417951)
28. Kumekawa, N., Ohmido, N., Fukui, K., Ohtsubo, E., and, Ohtsubo, H., (2001) A new gypsy-type retrotransposon, RIRE7: preferential insertion into the tandem repeat sequence TrsD in pericentromeric heterochromatin regions of rice chromosomes. Mol. Genet. Genomics, 265, 480-488.
29. Kurihara, Y., Matsui, A., Kawashima, M., et al. (2008) Identification of the candidate genes regulated by RNA-directed DNA methylation. Biochem. Biophys. Res. Commun. 376, 553-557.
30. Law, J., and, Jacobsen, S.E., (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204-220.
31. Li, X., Wang, X., He, K., et al. (2008) High-resolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation, and gene expression. Plant Cell, 20, 259-276. (Pubitemid 352844011)
32. Lindroth, A.M., Cao, X., Jackson, J.P., Zilberman, D., McCallum, C.M., Henikoff, S., and, Jacobsen, S.E., (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science, 292, 2077-2080. (Pubitemid 32691574)
33. Lister, R., O'Malley, R.C., Tonti-Filippini, J., Gregory, B.D., Berry, C.C., Millar, A.H., and, Ecker, J.R., (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell, 133, 523-536.
34. Lu, C., Tej, S.S., Luo, S., Haudenschild, C.D., Meyers, B.C., and, Green, P.J., (2005) Elucidation of the small RNA component of the transcriptome. Science, 309, 1567-1569. (Pubitemid 41266483)
35. Mathieu, O., Reinders, J., Caikovski, M., Smathajitt, C., and, Paszkowski, J., (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell, 130, 851-862. (Pubitemid 47334929)
36. Matzke, M., Kanno, T., Daxinger, L., Huettel, B., and, Matzke, A.M.J., (2009) RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21, 367-376.
37. Miki, D., and, Shimamoto, K., (2008) De novo DNA methylation induced by siRNA targeted to endogenous transcribed sequences is gene-specific and OsMet1-independent in rice. Plant J. 56, 539-549.
38. Moritoh, S., Miki, D., Akiyama, M., Kawahara, M., Izawa, T., Maki, H., and, Shimamoto, K., (2005) RNAi-mediated silencing of OsGEN-L (OsGEN-like), a new member of the RAD2/XPG nuclease family, causes male sterility by defect of microspore development in rice. Plant Cell Physiol. 46, 699-715. (Pubitemid 40793817)
39. Moritoh, S., Tanaka, K.F., Jouhou, H., Ikenaka, K., and, Koizumi, A., (2010) Organotypic tissue culture of adult rodent retina followed by particle-mediated acute gene transfer in vitro. PLoS ONE, 5, e12917.
40. Nagaki, K., Neumann, P., Zhang, D., Ouyang, S., Buell, C.R., Cheng, Z., and, Jiang, J., (2004) Structure, divergence, and distribution of the CRR cetromeric retrotransposon family in rice. Mol. Biol. Evol. 22, 845-855. (Pubitemid 40471399)
41. Nakagawa, T., Kurose, T., Hino, T., et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J. Biosci. Bioeng. 104, 34-41. (Pubitemid 47223816)
42. Nakashima, A., Chen, L., Thao, N.P., et al. (2008) RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell, 20, 2265-2279. (Pubitemid 352844524)
43. Naumann, U., Daxinger, L., Kanno, T., Eun, C., Long, Q., Lorkovic, Z.J., Matzke, M., and, Matzke, A.J.M., (2011) Genetic evidence that DNA methyltransferase DRM2 has a direct catalytic role in RNA-directed DNA methylation in Arabidopsis thaliana. Genetics, 187, 977-979.
44. Neumann, P., Yan, H., and, Jiang, J., (2007) The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference. Genetics, 176, 749-761. (Pubitemid 46961082)
45. Nobuta, K., Venu, R.C., Lu, C., et al. (2007) An expression atlas of rice mRNAs and small RNAs. Nat. Biotechnol. 25, 473-477. (Pubitemid 46572851)
46. Okano, M., Bell, D.W., Haber, D.A., and, Li, E., (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell, 99, 247-257. (Pubitemid 29519904)
47. Okano, Y., Miki, D., and, Shimamoto, K., (2008) Small interfering RNA (siRNA) targeting of endogenous promoters induces DNA methylation, but not necessarily gene silencing, in rice. Plant J. 53, 65-77. (Pubitemid 350265240)
48. Onodera, Y., Haag, J.R., Ream, T., Nunes, P.C., Pontes, O., and, Pikaard, C.S., (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell, 120, 613-622. (Pubitemid 40343074)
49. Radchuk, V.V., Sreenivasulu, N., Radchuk, R.I., Wobjus, U., and, Weschke, W., (2005) The methylation cycle and its possible functions in barley endosperm development. Plant Mol. Biol. 59, 289-307. (Pubitemid 41500490)
50. Rival, A., Jaligot, E., Beulè, T., Dussert, S., and, Verdeil, J.L., (2000) Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Rep. 19, 684-690. (Pubitemid 30427548)
51. Ronemus, M.J., Galbiati, M., Ticknor, C., Chen, J., and, Dellaporta, S.L., (1996) Demethylation-induced developmental pleiotropy in Arabidopsis. Science, 273, 654-657. (Pubitemid 26262120)
52. Saze, H., and, Kakutani, T., (2007) Heritable epigenetic mutation of a transposon-flanked Arabidopsis gene due to lack of the chromatin-remodeling factor DDM1. EMBO J. 26, 3641-3652. (Pubitemid 47236873)
53. Saze, H., Scheid, O.M., and, Paszkowski, J., (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat. Genet. 34, 65-69. (Pubitemid 36548792)
54. Sharma, R., Singh, R.K.M., Malik, G., Deveshwar, P., Tyagi, A.K., Kapoor, S., and, Kapoor, M., (2009) Rice cytosine DNA methyltransferases-gene expression profiling during reproductive development and abiotic stress. FEBS J. 276, 6301-6311.
55. Sidorenko, L., Dorweiler, J.E., Cigan, A.M., et al. (2009) A dominant mutation in mediator of paramutation2, one of three-second-largest subunits of a plant-specific RNA polymerase, disrupts multiple siRNA silencing processes. PLoS Genet. 5, e1000725.
56. Soppe, W.J., Jacobsen, S.E., Alonso-Blanco, C., Jackson, J.P., Kakutani, T., Koornneef, M., and, Peeters, A.J.M., (2000) The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol. Cell, 6, 791-802.
57. Springer, N.M., and, Kaeppler, S.M., (2005) Evolutionary divergence of monocot and dicot methyl-CpG-binding domain proteins. Plant Physiol. 138, 92-104. (Pubitemid 43138110)
58. Stokes, T.L., Kunkel, B.N., and, Richards, E.J., (2002) Epigenetic variation in Arabidopsis disease resistance. Genes Dev. 16, 171-182. (Pubitemid 34075810)
59. Tarutani, Y., Shiba, H., Iwano, M., Kakizaki, T., Suzuki, G., Watanabe, M., Isogai, A., and, Takayama, S., (2010) Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature, 466, 983-987.
60. Terada, R., Urawa, H., Inagaki, Y., Tsugane, K., and, Iida, S., (2002) Efficient gene targeting by homologous recombination in rice. Nat. Biotechnol. 20, 1030-1034.
61. Terada, R., Asao, H., and, Iida, S., (2004) A large-scale Agrobacterium-mediated transformation procedure with a strong positive-negative selection for gene targeting in rice (Oryza sativa L.). Plant Cell Rep. 22, 653-659. (Pubitemid 38641487)
62. Terada, R., Johzuka-Hisatomi, Y., Saitoh, M., Asao, H., and, Iida, S., (2007) Gene targeting by homologous recombination as a biotechnological tool for rice functional genomics. Plant Physiol. 144, 846-856. (Pubitemid 46944748)
63. Wada, Y., Ohya, H., Yamaguchi, Y., Koizumi, N., and, Sano, H., (2003) Preferential de novo methylation of cytosine residues in non-CpG sequences by a Domains Rearranged DNA Methyltransferase from Tobacco plants. J. Biol. Chem. 278, 42386-42393. (Pubitemid 37310509)
64. Yamauchi, T., Moritoh, S., Johzuka-Hisatomi, Y., Ono, A., Terada, R., Nakamura, I., and, Iida, S., (2008) Alternative splicing of the rice OsMET1 genes encoding maintenance DNA methyltransferase. J. Plant Physiol. 165, 1774-1782.
65. Yamauchi, T., Johzuka-Hisatomi, Y., Fukada-Tanaka, S., Terada, R., Nakamura, I., and, Iida, S., (2009) Homologous recombination-mediated knock-in targeting of the MET1a gene for a maintenance DNA methyltransferase reproducibly reveals dosage-dependent spatiotemporal gene expression in rice. Plant J. 60, 386-396.
66. Zhang, H., and, Zhu, J.K., (2011) RNA-directed DNA methylation. Curr. Opin. Plant Biol. 14, 142-147.
67. Zhang, X., Yazaki, J., Sundaresan, A., et al. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell, 126, 1189-1201. (Pubitemid 44380289)
68. Zilberman, D., Gehring, M., Tran, R.K., Ballinger, T., and, Henikoff, S., (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39, 61-69. (Pubitemid 46026502)