เอพิเจเนติก-การควบคุมเหนือลำดับดีเอ็นเอ

Authors

  • โชติกา หยกทองวัฒนา ภาควิชาชีวเคมี คณะวิทยาศาสตร์ มหาวิทยาลัยเกษตรศาสตร์ กรุงเทพฯ 10900

DOI:

https://doi.org/10.14456/tjg.2011.6

Keywords:

epigenetic, DNA methylation, histone methylation, histone acetylation, chromatin remodeling

Abstract

Epigenetic refer to changes of gene expression without any change of the underlying DNA sequences. There are various mechanisms that plants utilize to control gene expression. The main regulation mechanisms are DNA methylation, histone modifications such as histone methylation, histone acetylation and changes of chromatin structure or chromatin remodeling. The alteration of gene expression influences plant growth, development and reproduction. In this review, regulation of gene expression via main epigenetic mechanisms and proteins involved in the epigenetic regulation will be described.

References

Agius, F., Kapoor, A. and Zhu, J.K. 2006. Role of the Arabidopsis DNAglycosylase/lyase ROS1 in active DNA demethylation. Proc Natl Acad Sci USA 103: 11796–11801.

Bakshi, R., Prakash, T., Dash, D. and Brahmachari, V. 2004. In silico characterization of the INO80 subfamily of SWI2/SNF2 chromatin remodeling proteins. Biochem Biophys Res Commun 320: 197–204.

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: 1753-8.

Baulcombe, D.C. 2007. Molecular biology: Amplified silencing. Science 315: 199–200.

Baumbusch, L.O., Thorstensen, T., Krauss, V., Fischer, A., Naumann, K., Assalkhou, R., Schulz, I., Reuter, G. and Aalen, R.B. 2001. The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res 29: 4319–4333.

Bender, J. 2004. DNA methylation and epigenetics. Annu Rev Plant Biol 55: 41–68.

Bender, J. and Fink, G.R. 1995. Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83: 725–734.

Benhamed, M., Bertrand, C., Servet, C. and Zhou, D.X. 2006. Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18: 2893–2903.

Bernstein, B.E., Meissner, A. and Lander, E.S. 2007. The mammalian epigenome. Cell 128: 669–681.

Bird, A. 2007. Perception of epigenetics. Nature 447: 396–398.

Boyer, L.A., Latek, R.R. and Peterson, C.L. 2004. The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol 5: 158–163.

Brodersen, P. and Voinnet, O. 2006. The diversity of RNA silencing pathways in plants. Trends Genet 22: 268–280.

Buhler, M. and Gasser, S.M. 2009. Silent chromatin at the middle and ends: lessons from yeasts. EMBO J. 28: 2149–2161.

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 DNA methyltransferases. Proc Natl Acad Sci USA 97: 4979–4984.

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.

Cao, X. and Jacobsen, S.E. 2002b. Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99 Suppl 4: 16491–16498.

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.

Chandler, V.L. 2007. Paramutation: from maize to mice. Cell 128: 641–645.

Chen, T. and Li, E. 2004. Structure and function of eukaryotic DNA methyltransferases. Curr. Top. Dev. Biol. 60: 55–89.

Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B., Jacobsen, S.E. and Fischer, R.L. 2002. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110: 33–42.

Dang, W.W. and Bartholomew, B. 2007. Domain architecture of the catalytic subunit in the ISW2-nucleosome complex Mol Cell Biol. 27: 8306–8317.

de la Cruz, X., Lois, S., Sanchez-Molina, S. and Martinez-Balbas, M.A. 2005. Do protein motifs read the histone code? Bioessays 27: 164–175.

Deng, W., Liu, C., Pei, Y., Deng, X., Niu, L. and Cao, X. 2007. Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLC in Arabidopsis. Plant Physiol. 143: 1660–1668.

Earley, K., Lawrence, R.J., Pontes, O., Reuther, R., Enciso, A.J., Silva, M., Neves, N., Gross, M., Viegas, W. and Pikaard, C.S. 2006. Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev 20: 1283–1293.

Ebbs, M.L. and Bender, J. 2006. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166–1176.

Eberharter, A. and Becker, P.B. 2004. ATP-dependent nucleosome remodelling: factors and functions. J Cell Sci 117: 3707–3711.

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: 8449-8454.

Finnegan, E.J. and Kovac, K.A. 2000. Plant DNA methyltransferases. Plant Mol Biol. 43: 189–201.

Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B. and Fischer, R.L. 2006. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124: 495–506.

Girton, J.R. and Johansen, K.M. 2008. Chromatin structure and the regulation of gene expression: the lessons of PEV in Drosophila. Adv. Genet. 61: 1–43.

Goll, M.G. and Bestor, T.H. 2005. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481–514.

Gong, Z., Morales-Ruiz, T., Ariza, R.R., Roldan-Arjona, T., David, L. and Zhu, J.K. 2002. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111: 803–814.

Grewal, S.I. and Jia, S. 2007. Heterochromatin revisited. Nat Rev Genet 8: 35–46.Hall, J.A. and Georgel, P.T. 2007. CHD proteins: a diverse family with strong ties. Biochem Cell Biol 85: 463–476.

Hassan, A.H., Awad, S., Al-Natour, Z., Othman, S., Mustafa, F. and Rizvi, T.A. 2007. Selective recognition of acetylated histones by bromodomains in transcriptional co-activators. Biochem J 402: 125–133.

Henikoff, S. and Comai, L. 1998. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307-318.

Horton, J.R., Elgar, S.J., Khan, S.I., Zhang, X., Wade, P.A. and Cheng, X. 2007. Structure of the SANT Domain from the Xenopus Chromatin Remodeling Factor ISWI. Proteins 67: 1198–1202.

Jackson, J.P., Lindroth, A.M., Cao, X. and Jacobsen, S.E. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560.

Jackson, J.P., Johnson, L., Jasencakova, Z., Zhang, X., PerezBurgos, L., Singh, P.B., Cheng, X., Schubert, I., Jenuwein, T. and Jacobsen, S.E. 2004. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308–315.

Jarillo, J.A., Pineiro, M., Cubas, P. and Martinez-Zapater, J.M. 2009. Chromatin remodeling in plant development. Int. J. Dev.Biol. 53: 1581–1596.

Jasencakova, Z., Soppe, W.J., Meister, A., Gernand, D., Turner, B.M. and Schubert, I. 2003. Histone modifications in Arabidopsis- high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33: 471–480.

Jenuwein, T. and Allis, C.D. 2001. Translating the histone code. Science 293: 1074–1080.

Kankel, M.W., Ramsey, D.E., Stokes, T.L., Flowers, S.K., Haag, J.R. and Jeddeloh, J.A. 2003. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163: 1109–1122.

Kim, J.-M., To, T.K., Nishioka, T. and Seki, M. 2010. Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ. 33: 604–611.

Kinoshita, T., Miura, A., Choi, Y., Kinoshita, Y., Cao, X., Jacobsen, S.E., Fischer, R.L. and Kakutani, T. 2004. One-way control of FWA imprinting in Arabidopsis endosperm

by DNA methylation. Science 303: 521–523.

Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128: 693–705.

Kunert, N. and Brehm, A. 2009. Novel Mi-2 related ATP-dependent chromatin remodelers. Epigenetics 4: 209–211.

Lee, K.K. and Workman, J.L. 2007. Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev Mol Cell Biol 8: 284–295.

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.

Malagnac, F., Bartee, .L and Bender, J. 2002. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. Embo J 21: 6842–6852.

Marfella, C.G.A. and Imbalzano, A.N. 2007. The Chd family of chromatin remodelers. Mutat Res 618: 30–40.

Morales-Ruiz, T., Ortega-Galisteo, A.P., Ponferrada-Marin, M.I., Martinez-Macias, M.I., Ariza, R.R. and Roldan-Arjona, T. 2006. DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases. Proc Natl Acad Sci USA 103: 6853–6858.

Mujtaba, S., Zeng, L. and Zhou, M.M. 2007. Structure and acetyl-lysine recognition of the bromodomain. Oncogene 26: 5521–557.

Murfett, J., Wang, X.J., Hagen, G. and Guilfoyle, T.J. 2001. Identification of Arabidopsis histone deacetylase HDA6 mutants that affect transgene expression. Plant Cell 13: 1047–1061.

Mylne, J.S., Nap, J.P. and Bisseling, T. 2007. The SWI/SNF chromatin remodeling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress. Plant J. 51: 874–885.

Nakayama, J., Rice, J.C., Strahl, B.D., Allis, C.D. and Grewal, S.I. 2001. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110–113.

Napoli, C., Lemieux, C., and Jorgensen, R. 1990. Introduction of a chimeric chalcone synthase gene into petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2: 279–289.

Narlikar, G.J., Fan, H.Y. and Kingston, R.E. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108: 475–487.

Naumann, K., Fischer, A., Hofmann, I., Krauss, V., Phalke, S., Irmler, K., Hause, G., Aurich, A.C., Dorn, R., Jenuwein, T. and Reuter, G. 2005. Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. Embo J 24: 1418–1429.

O'Carroll, D., Scherthan, H., Peters, A.H., Opravil, S., Haynes, A.R., Laible, G., Rea, S., Schmid, M., Lebersorger, A., Jerratsch, M., Sattler, .L, Mattei, M.G., Denny, P., Brown, S.D., Schweizer, D. and Jenuwein, T. 2000. Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Mol Cell Biol 20: 9423–9433.

Pandey, R., Muller, A., Napoli, C.A., Selinger, D.A., Pikaard, C.S., Richards, E.J., Bender, J., Mount, D.W. and Jorgensen, R.A. 2002. Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30: 5036–5055.

Pavlopoulou, A. and Kossida, S. 2007. Plant cytosine-5 DNA methyltransferases: structure, function, and molecular evolution. Genomics 90: 530–541.

Penterman, J., Zilberman, D., Huh, J.H., Ballinger, T., Henikoff, S. and Fischer, R.L. 2007. DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci USA 104: 6752–6757.

Peters, A.H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S. and Schofer, C. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107: 323–337.

Probst, A.V., Fransz, P.F., Paszkowski, J. and Scheid, O.M. 2003. Two means of transcriptional reactivation within heterochromatin. Plant J 33: 743–749.

Probst, A.V., Fagard, M., Proux, F., Mourrain, P., Boutet,

S., Earley, K., Lawrence, R.J., Pikaard, C.S., Murfett, J., Furner, I., Vaucheret, H. and Mittelsten Scheid, O. 2004. Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16: 1021–1034.

Qian, C. and Zhou, M.M. 2006. SET domain protein lysine methyltransferases: Structure, specificity and catalysis. Cell Mol Life Sci 63: 2755–2763.

Rea, S., Eisenhaber, F., O'Carroll, D., Strahl, B.D., Sun, Z.W., Schmid, M., Opravil, S., Mechtler, K., Ponting, C.P., Allis, C.D. and Jenuwein, T. 2000. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593–599.

Reyes, J.C. 2006. Chromatin modifiers that control plant development. Curr Opin Plant Biol 9: 21–27.

Ronemus, M.J., Galbiati, M., Ticknor, C., Chen, J. and

Dellaporta, S.L. 1996. Demethylation induced developmental pleiotropy in Arabidopsis. Science 273: 654–657.

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.

Selker, E.U., Tountas, N.A., Cross, S.H., Margolin, B.S., Murphy, J.G., Bird, A.P. and Freitag, M. 2003. The methylated component of the Neurospora crassa genome. Nature 422: 893–897.

Shahbazian, M.D. and Grunstein, M. 2007. Functions of site-specific histone acetylation and deacetylation. Annu Rev Biochem 76: 75–100.

Shilatifard, A. 2006. Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75: 243–269.

Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J.R., Cole, P.A. and Casero, R.A. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941–953.

Shi, Y. and Whetstine, J.R. 2007. Dynamic regulation of histone lysine methylation by demethylases. Mol Cell 25: 1–14.

Smith, C.L. and Peterson, C.L. 2005. ATP-dependent chromatin remodeling. Curr Top Dev Biol 65: 115–148.

Strahl, B.D. and Allis, C.D. 2000. The language of covalent histone modifications. Nature 403: 41–45.

Tamaru, H. and Selker, E.U. 2001. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414: 277–283.

Tian, L. and Chen, Z.J. 2001. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc Natl Acad Sci USA 98: 200–205.

Tian, L., Fong, M.P., Wang, J.J., Wei, N.E., Jiang, H., Doerge, R.W. and Chen, Z.J. 2005. Reversible histone acetylation and deacetylation mediate genomewide, promoter-dependent and locus-specific changes in gene expression during plant development. Genetics 169: 337–345.

Tschiersch, B., Hofmann, A., Krauss, V., Dorn, R., Korge, G. and Reuter, G. 1994. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. Embo J 13: 3822–3831.

Tsukiyama, T. 2002. The in vivo functions of ATP-dependent chromatin-remodelling factors. Nat Rev Mol Cell Biol 3: 422–429.

Vaillant, I., Tutois, S., Jasencakova, Z., Douet, J., Schuber,t I. and Tourmente, S. 2008. Hypomethylation and hypermethylation of the tandem repetitive 5S rRNA genes in Arabidopsis. Plant J 54: 299–309.

van Vugt, J.J., Ranes, M., Campsteijn, C. and Logie, C. 2007. The ins and outs of ATP-dependent chromatin remodeling in budding yeast: Biophysical and proteomic perspectives. Biochim Biophys Acta 1769: 153–171.

Vanyushin, B.F. and Ashapkin, VV. 2011. DNA methylation in higher plants: past, present and future. Biochim Biophys Acta 1809: 360–368.

Vongs, A., Kakutani, T., Martienssen, R.A. and Richards, E.J. 1993. Arabidopsis thaliana DNA methylation mutants. Science 260: 1926–1928.

Waddington, C. 1942. The epigenotype. Endeavour 1: 18–20.

Wutz, A. 2011. Gene silencing in X-chromosome inactivation: advances in understanding facultative heterochromatin formation. Nat. Rev. Genet. 12: 542–553.

Yang, P.K. and Kuroda, M.I. 2007. Noncoding RNAs and intranuclear positioning in monoallelic gene expression. Cell 128: 777–786.

Yokthongwattana, C., Bucher, E., Caikovski, M., Vaillant, I., Nicolet, J., Mittelsten Scheid, M. and Paszkowski, J. 2010. MOM1 and Pol-IV/V interactions regulate the intensity and specificity of transcriptional gene silencing. EMBO J. 29: 340–351.

Zaratiegui, M., Irvine, D.V. and Martienssen, R.A. 2007. Noncoding RNAs and gene silencing. Cell 128: 763–776.

Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S.W., Chen, H., Henderson, I.R., Shinn, P., Pellegrini, M., Jacobsen, S.E. and Ecker, J.R. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126: 1189–1201.

Zhang, M., Kimatu, J.N., Xu, K. and Lui, B. 2010. DNA cytosine methylation in plant development. J. Genet. Genomics 37: 1–12.

Zhu, J., Kapoor, A., Sridhar, VV., Agius, F. and Zhu, J.K. 2007. The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr. Biol. 17: 54–59.

Downloads

Published

2012-04-12

Issue

Section

Review Articles