Biopolym. Cell. 2010; 26(3):163-174.
http://dx.doi.org/10.7124/bc.000153
Reviews
Cell cycle and epigenetic changes of plant DNA
1Shevchenko G. V.
  1. M. G. Kholodny Institute of Botany, NAS of Ukraine
    2, Tereschenkivska Str., Kyiv, Ukraine, 01601

Abstract

Plants can apply various strategies to minimize environmental impact. One of the strategies is heritable modifications of gene expression which occur without changing original DNA sequence and are known as epigenetic. Signaling pathway Rb-E2F (retinoblastoma (Rb)-transcription factor E2F/DP) connects the cell cycle with factors, modifying structure of chromatin and DNA. It also co- ordinates cell proliferation and differentiation influenced by external stimuli. The article highlights the activity of Rb-E2F/DP signaling pathway and its connection with the epigenetic changes of DNA in plants.
Keywords: DNA, transcription factor E2F, chromatin-modifying complexes, epigenetic
Full text: (PDF, in English) (PDF, in Russian)

References

[1] Inze D., de Veylder L. Cell cycle regulation in plant development Annu. Rev. Genet 2006 40, N 1:77–105.
[2] Gutierrez C. The retinoblastoma pathway in plant cell cycle and development Curr. Opin. Plant Biol 1998 1, N 6 P. 492–497.
[3] Dewitte W., Murray J. The plant cell cycle Annu. Rev. Plant Biol 2003 54, N 1:235–264.
[4] Harbour J., Dean, D. The Rb/E2F pathway: expanding roles and emerging paradigms Genes Develop 2000a 14, N 19:2393.
[5] De Veylder L., Beeckman T., Beemster G., de Almeida Engler J., Ormenese S., Maes S., Naudts M., van der Schueren E., Jacqmard A. Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-Dpa transcription factor EMBO J 2002 21, N 6:1360–1368.
[6] Blais A., Dynlacht B. E2F-associated chromatin modifiers and cell cycle control Curr. Opin. Cell Biol 2007 19, N 6:658–662.
[7] Sekine M., Ito M., Uemukai K., Maeda Y., Nakagami H., Shinmyo A. Isolation and characterization of the E2F-like gene in plants FEBS Lett 1999; 460(1):117–122.
[8] Albani D., Mariconti L., Ricagno S., Pitto L., Moroni C., Helin K., Cella R. DcE2F, a functional plant E2F-like transcriptional activator from D. carota J. Biol. Chem 2000 275, N 25:19258–19267.
[9] Kosugi S., Ohashi Yu. Constitutive E2F expression in tobacco plant exhibits altered cell cycle control and morphological changes in a cell type specific manner Plant Physiol 2003 132, N 4:2012–2022.
[10] Sabelli P. A., Dante R. A., Leiva-Neto J. T., Jung R., GordonKamm W. J., Larkins B. A. RBR3, a member of the retinoblastoma-related family from maize is regulated by the RBR1/E2F pathway Proc. Nat. Acad. Sci. USA 2005 102, N 37:13005–13012.
[11] Vandepoele K., Raes J., De Veylder L., Rouze P., Rombauts S., Inze D. Genome-wide analysis of core cell cycle genes in Arabidopsis Plant Cell 2002 14, N 4:903–916.
[12] Oakenfull E., Riou-Khamlichi C., Murray J. Plant D-type cyclins and the control of G1 progression Phil. Trans. Roy. Soc. Lond 2002 357, N 1422:749–760.
[13] Mariconti L., Pellegrini B., Cantoni R., Stevens R., Bergounioux C., Cella R., Albani D. The E2F family of transcription factors from A. thaliana: novel and conserved components of plant retinoblastoma/E2F pathway in plants J. Biol. Chem 2002 277, N 12:9911–9919.
[14] Shen W. The plant E2F-Rb pathway and epigenetic control Trends Plant Sci 2002 7, N 11:505–511.
[15] Kovesdi I., Reichel R., Nevins J. R. Identification of a cellular transcription factor involved in E1A transactivation Cell 1986 45, N 2:219–228.
[16] Lavia P., Jansen-Durr P. E2F target genes and cell-cycle checkpoint control BioEssays 1999 21, N 3:221– 230.
[17] De Jager S., Menges M., Bauer U., Murray J. Arabidopsis E2F-1 binds a sequence present in the promoter of S-phaseregulated gene AtCDC6 and is a member of a multigene family with differential activities Plant Mol. Biol 2001 47, N 4:555–568.
[18] Kosugi S., Ohashi Yu. E2F sites that interact with E2F protein cloned from rice are required for meristematic tissue-specific expression of rice and tobacco proliferating cell nuclear antigen promoters Plant J 2002 29, N 1:45–59.
[19] Del Pozo J., Boniotti M., Gutierrez C. Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF (AtSKP2) pathway in response to light Plant Cell 2002 14, N 12:3057–3071.
[20] Ramirez-Parra E., Lopez-Matas M.A., Frundt C., Gutierrez C. Role of an atypical E2F transcription factor in the control of Arabidopsis cell growth and differentiation Plant Cell 2004 16, N 9:2350–2363.
[21] Sozzani R., Maggio C., Varotto S., Canova S., Bergounioux C., Albani D., Cella R. Interplay between Arabidopsis activating factors E2Fb and E2Fa in cell cycle progression and development Plant Physiol 2006 140, N 4:1355– 1366.
[22] Shan B., Lee W. Deregulated expression of E2F-1 induces Sphase entry and leads to apoptosis. Mol. Cell Biol. 1994; 14, N 1:8166–8173.
[23] Chaboute M., Clement B., Sekine M., Philipps G., ChaubetGigot N. Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell. 2000; 12, N 10:1987–2000.
[24] Stevens R., Mariconti L., Rossignol P., Perennes C., Cella R., Bergounioux C. Two E2F sites in the Arabidopsis MCM3 promoter have different roles in cell cycle activation and meristematic expression J. Biol. Chem 2002 277, N 30 P. 32978–32984.
[25] Reyes J., Hennig L., Gruissem W. Chromatin-remodeling and memory factors. New regulators of plant development Plant Physiol 2002 130, N 3:1090–1101.
[26] Martin C., Zhang Yi. Mechanisms of epigenetic inheritance Curr. Opin. Cell Biol 2007 19, N 3:266–272.
[27] Vignali M., Hassan A., Neely K., Workman J. ATP-dependent chromatin-remodelling complexes Mol. Cell. Biol 2000 20, N 6:1899–1910.
[28] Saha A., Wittmeyer J., Cairns B. Chromatin remodeling: the industrial revolution of DNA around histones Nat. Rev. Mol. Cell Biol 2006 7, N 6:437–447.
[29] Bezhani S., Winter C., Hershman S., Wagner J., Kennedy J., Kwon Ch., Pfluger J., Su Ya., Wagner D. Unique, shared, and redundant roles for the Arabidopsis SWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED Plant Cell 2007 19, N 2:403–416.
[30] Mohrmann L., Verrijzer C. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes Biochim. Biophys. Acta 2005 1681, N 2–3:59–73.
[31] Flaus A., Martin D., Barton G., Owen-Hughes T. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs Nucl. Acids Res 2006 34, N 10 P. 2887–2905.
[32] Sarnowski T., Swiezewski Sz., Pawlikowska K., Kaczanowski Sz., Jerzmanowski A. AtSWI3B, an Arabidopsis homolog of SWI3, a core subunit of yeast Swi/Snf chromatin remodeling complex, interacts with FCA, a regulator of flowering time Nucl. Acids Res 2002 30, N 15:3412–3421.
[33] Verbsky M., Richards E. Chromatin remodeling in plants Curr. Opin. Plant Biol 2001 4, N 6:494–500.
[34] Harbour J., Dean D. Chromatin remodeling and Rb activity Curr. Opin. Cell Biol 2000 12, N 6:685–689.
[35] Sarnowski T., Rios G., Swiezewski Sz., Kaczanowski Sz., Li Y., Kwiatkowska A., Pawlikowska K., Kozbial M., Kozbial P., Concz C., Jerzmanowski A. SWI3B subunits of putative SWI/ SNF chromatin remodeling complex play distinct roles during Arabidopsis development Plant Cell 2005 17, N 9 P. 2454–2472.
[36] Peterson C., Zhao J., Chait B. Subunits of the yeast SWI/SNF complex are members of the actin-related protein (ARP) family J. Biol. Chem 1998 273, N 37:23641–23644.
[37] Chen M., Shen X. Nuclear actin and actin-related proteins in chromatin dynamics Curr. Opin. Cell Biol 2007 19, N 3:326–330.
[38] Kwon C., Hibara K., Pfluger J., Bezhani S., Metha H., Aida M., Tasaka M., Wagner D. A role for chromatin remodeling in regulation of CUC gene expression in the Arabidopsis cotyledon boundary Development 2006 133, N 16 P. 3223– 3230.
[39] Su Y., Kwon G., Bezhani S., Huvermann B., Chen C., Peragine A., Kennedy J., Wagner D. The N-terminal ATPase AThook containing region of the Arabidopsis-remodelling protein SPLAYED is sufficient for biological activity Plant J 2006 46, N 4:685–699.
[40] Farrona S., Hurtado L., Bowman J., Reyes J.The Arabidopsis thaliana SNF2 homolog AtBRM controls shoot development and flowering Development 2004 131, N 20:4965– 4975.
[41] Lusser A., Kolle D., Loidl P. Histone acetylation: lessons from the plant kingdom Trends Plant Sci 2001 6, N 2 P. 59–65.
[42] Fuchs J., Demidov D., Houben A., Schubert I. Chromosomal histone modification patterns – from conservation to diversity Trends Plant Sci 2006 11, N 4:199–208.
[43] Andrin Ch., Hendzel M. F-actin dependent insolubility of chromatin-modifying components J. Biol. Chem 2004 279, N 24:25017–25023.
[44] Tian L., Fong M., Wang J., Wei N., Jiang H., Doerge R., Chen Z. Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development Genetics 2005 169, N 1:337–345.
[45] Wu K., Malik K., Tian L., Brown D., Miki B. Functional analysis of a RPD3 histone deacetylase homologue in A. thaliana Plant Mol. Biol 2000 44, N 2:167–176.
[46] Tian L., Chen Z. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development Proc. Nat. Acad. Sci. USA 2001 98, N 1 P. 200–205.
[47] Rossi V., Locatelli S., Varotto S., Donn G., Pirona R., Henderson D., Hartings H., Motto M. Maize histone deacetylase hda101 is involved in plant development gene transcription and sequense-specific modulation of histone modification of genes and repeats Plant Cell 2007 19, N 4:1145– 1162.
[48] Khochbin S., Verdel A., Lemercier C., Seigneurin-Berny D. Functional significance of histone deacetylase diversity Curr. Opin. Genet. Devel 2001 11, N 2 P. 162–166.
[49] Lusser A., Brosch G., Loidl A., Haas H., Loidl P. Identification of maize histone deacetylase HD2 as an acidic nucleolar phosphoprotein Science 1997 277, N 5322:88–91.
[50] Wu K., Tian L., Malik K., Brown D., Miki B. Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana Plant J 2000 22, N 1 P. 19–27.
[51] Harbour J., Dean D. Chromatin remodeling and Rb activity Curr. Opin. Cell Biol 2000 12, N 6:685–689.
[52] Fisher U., Kuhlmann M., Pecinka A., Schmidt R., Mette M. Local DNA features affects RNA-directed transcriptional gene silencing and DNA methylation Plant J 2008 53, N 1 P. 1–10.
[53] Nakayama J., Rice J., Strahl B., Allis C., Grewal S. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly Science 2001 292, N 5514 P. 110–113.
[54] Li X., Wang X., He K., Ma Y., Su N., He H., Stolc V., Tongprasit W., Jin W., Jiang J., Terzaghi W., Li S., Deng X. Highresolution mapping of epigenetic modifications of the rice genome uncovers interplay between DNA methylation, histone methylation and gene expression Plant Cell 2008 20, N 2:259–276.
[55] Jackson J., Johnson L., Jasencakova Z., Zhang X., PerezBurgos L., Singh P., Cheng X., Schubert I., Jenuwein T., Jacobsen S. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in A. thaliana Chromosoma 2004 112, N 6:308–315.
[56] Springer N., Napoli C., Selinger D. Comparative analysis of SET-domain proteins inmaize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots Plant Physiol 2003 132, N 2:907–925.
[57] Jackson J., Lindroth A., Cao X., Jacobsen S. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase Nature 2002 416, N 6880:556– 560.
[58] Naumann K., Fischer A., Hofmann I., Krauss V., Phalke S., Irmler K., Hause G., Aurich A., Dorn R., Jenuwein T., Reuter G. Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis EMBO J 2005 24, N 7:1418–1429.
[59] Chan S., Henderson I., Jacobsen S.Gardening the genome: DNA methylation in Arabidopsis thaliana Nat. Rev. Genet 2005 6, N 12:351–360.
[60] Bannister A., Zegerman P., Partridge J., Miska E., Thomas J., Allshire R., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromodomain. Nature. 2000; 410, N 6824:120–124.
[61] Gaudin V., Libault M., Pouteau S., Juul T., Zhao G., Lefebvre G., Grand-Jean O. Mutations in like heterochromatin protein 1 affects flowering time and plant architecture in Arabidopsis. Development. 2001; 128, N 23:4847–4858.
[62] Zemah A., Li Yan., Ben-Meir H., Oliva M., Mosquna A., Kiss V., Avivi Y., Ohad N., Grafi G. Diferent domains control the localization and mobility of LIKE HETEROCHROMATIN PROTEIN 1 in Arabidopsis nuclei Plant Cell 2006 18, N 1 P. 133–145.
[63] Nielsen S., Schneider R., Bauer U., Bannister A. J., Morrison A., O'Carroll D., Firestein R., Cleary M., Jenuwein T., Herrera R., Kouzarides T. Rb targets histone H3 methylation and HP1 to promoters Nature 2000 412, N 6846:561– 565.
[64] Williams L., Grafi G. The retinoblastoma protein–a bridge to heterochromatin Trends Plant Sci 2000 5, N 7:239– 240.
[65] Penterman J., Uzawa R., Fischer R. Genetic interactions between DNA demethylation and methylation in Arabidopsis Plant Physiol 2007 145, N 4:1549–1557.
[66] Kovalchuk I., Abramov V., Pogribny I., Kovalchuk O. Molecular aspects of plant adaptation to life in the Chernobyl zone Plant Physiol 2004 135, N 1:357–363.
[67] Singh A., Zubko E., Meyer P. Cooperative activity of DNA methyltransferases for maintenance of symmetrical and nonsymmetrical cytosine methylation in Arabidopsis thaliana Plant J 2008 56, N 4:814–823.
[68] Boyko A., Kovalchuk I. Epigenetic control of plant stress response Environ. Mol. Mutagen 2008 49, N 1:61–72.
[69] Soppe W., Jasencakova Z., Houben A., Kakutani T., Meister A., Huang M., Jacobsen S., Schubert J., Fransz P. F. DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis EMBO J 2002 21, N 23:6549–6559.