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Arabidopsis E2F1 binds a sequence present in the promoter of S-phase-regulated gene AtCDC6 and is a member of a multigene family with differential activities

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Abstract

Mammalian E2F transcription factors are composed of E2F and DP subunits, and with their negative regulators, Rb-related proteins, govern expression of cell-division-related genes. Six E2Fs and two DPs are present in mammals, but only single E2F genes are known from wheat, tobacco and carrot. Here we show that E2Fs are a multigene family in Arabidopsis, and report isolation of three E2F-like clones AtE2F1-3, with 45–62% identity to wheat, tobacco and carrot E2Fs. Sequence analysis reveals that AtE2F1 and AtE2F3 are closely related to previously identified plant E2Fs, whereas AtE2F2 is related to human E2F6 and Drosophila dE2F2 which are unusual in lacking transcriptional activation potential. Consistent with this, we show that AtE2F1 and AtE2F3 activate transcription in yeast cells and bind a plant Rb protein, but AtE2F2 cannot activate transcription or bind Rb. Consensus E2F-binding sites were identified in promoters of several cell cycle related genes, including the D-type cyclin CycD3 and the Arabidopsis homologue of the replication origin protein CDC6. Accumulation of AtE2F1-3 was observed in partially synchronised Arabidopsis cells re-entering the cell cycle, before induction of CycD3 and CDC6 expression in late G1. AtE2F1 complexes bound to consensus E2F sequences and to the AtCDC6 promoter in vitro. We conclude that Arabidopsis contains a family of functionally distinct E2F genes, most probably involved in the G1-to-S phase progression.

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References

  • Ach, R.A., Durfee, T., Miller, A.B., Taranto, P., Hanley-Bowdoin, L., Zambryski, P.C. and Gruissem, W. 1997. RRB1 and RRB2 encode maize retinoblastoma-related proteins that interact with a plant D-type cyclin and geminivirus replication protein. Mol. Cell Biol. 17: 5077–5086.

    Google Scholar 

  • Adams, P.D., Sellers, W.R., Sharma, S.K., Wu, A.D., Nalin, C.M. and Kaelin, W.G., Jr. 1996. Identification of a cyclin-cdk2 recognition motif present in substrates and p21-like cyclin-dependent kinase inhibitors. Mol. Cell Biol. 16: 6623–6633.

    Google Scholar 

  • Albani, D., Mariconti, L., Ricagno, S., Pitto, L., Moroni, C., He-lin, K. and Cella, R. 2000. DcE2F, a functional plant E2F-like transcriptional activator from Daucus carota. J. Biol. Chem. 275: 19258–19267.

    Google Scholar 

  • Allen, K.E., de la Luna, S., Kerkhoven, R.M., Bernards, R. and La Thangue, N.B. 1997. Distinct mechanisms of nuclear accumulation regulate the functional consequence of E2F transcription factors. J. Cell Sci. 110: 2819–2831.

    Google Scholar 

  • Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389–3402.

    Google Scholar 

  • Bai, C. and Elledge, S.J. 1997. Searching for interacting proteins with the two-hybrid system I. In: P.L. Bartel and S. Fields(Eds) The Yeast Two-Hybrid System, Oxford University Press, New York, pp. 11–28.

    Google Scholar 

  • Bandara, L.R., Buck, V.M., Zamanian, M., Johnston, L.H. and La Thangue, N.B. 1993. Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. EMBO J. 12: 4317–4324.

    Google Scholar 

  • Bartel, P.L., Chien, C.-T., Sternglanz, R. and Fields, S. 1993. Using the two-hybrid system to detect protein-protein interactions. In: D.A. Hartley (Ed.) Cellular Interactions in Development: A Practical Approach, IRL Press, New York, pp. 153–179.

    Google Scholar 

  • Beijersbergen, R.L., Kerkhoven, R.M., Zhu, L., Carlée, L., Voorhoeve, P.M. and Bernards, R. 1994. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev. 8: 2680–2690.

    Google Scholar 

  • Beijersbergen, R.L. and Bernards, R. 1996. Cell cycle regulation by the retinoblastoma family of growth inhibitory proteins. Biochim. Biophys. Acta 1287: 103–120.

    Google Scholar 

  • Black, A.R. and Azizkhan-Clifford, J. 1999. Regulation of E2F: a family of transcription factors involved in proliferation control. Gene 237: 281–302.

    Google Scholar 

  • Breeden, L. and Nasmyth, K. 1985. Regulation of the yeast HO gene. Cold Spring Harbor Symp. Quant. Biol. 50: 643–650.

    Google Scholar 

  • Cartwright, P., Müller, H., Wagener, C., Holm, K. and Helin, K. 1998. E2F-6: a novel member of the E2F family is an inhibitor of E2F-dependent transcription. Oncogene 17: 611–623.

    Google Scholar 

  • Chabouté, M.-E., Clément, B., Sekine, M., Philipps, G. and Chaubet-Gigot, N. 2000. Cell cycle regulation of the tobacco ribonucleotide reductase small subunit gene is mediated by E2F-like elements. Plant Cell 12: 1987–1999.

    Google Scholar 

  • Chaubet, N., Flénet, M., Clément, B., Brignon, P. and Gigot, C. 1996. Identification of cis-elements regulating the expression of an Arabidopsis histone H4 gene. Plant J. 10: 425–435.

    Google Scholar 

  • de Jager, S.M. and Murray, J.A.H. 1999. Retinoblastoma proteins in plants. Plant Mol. Biol. 41: 295–299.

    Google Scholar 

  • De Veylder, L., de Almeida Engler, J., Burssens, S., Manevski, A., Lescure, B., Van Montagu, M., Engler, G. and Inzé, D. 1999. A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation. Planta 208: 453–462.

    Google Scholar 

  • Durfee, T., Becherer, K., Chen, P.-L., Yeh, S.-H., Yang, Y., Kilburn, A.E., Lee, W.-H. and Elledge, S.J. 1993. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7: 555–569.

    Google Scholar 

  • Dyson, N. 1998. The regulation of E2F by pRB-family proteins. Genes Dev. 12: 2245–2262.

    Google Scholar 

  • Fountain, M.D., Murray, J.A.H. and Beck, E. 1999a. Isolation of a full-length cDNA encoding a retinoblastoma protein from suspension cultured photoautotrophic Chenopodium rubrum L. cells. Plant Physiol. 119: 363.

    Google Scholar 

  • Fountain, M.D., Murray, J.A.H. and Beck, E. 1999b. Nucleotide se-quence of a cDNA encoding a cyclin D3 protein from suspension cultured photoautotrophic Chenopodium rubrum L. cells. Plant Physiol. 119: 363.

    Google Scholar 

  • Fuerst, R.A.U.A., Soni, R., Murray, J.A.H. and Lindsey, K. 1996. Modulation of cyclin transcript levels in cultured cells of Arabidopsis thaliana. Plant Physiol. 112: 1023–1033.

    Google Scholar 

  • Gaubatz, S., Wood, J.G. and Livingston, D.M. 1998. Unusual proliferation arrest and transcriptional control properties of a newly discovered E2F family member, E2F-6. Proc. Natl. Acad. Sci. USA 95: 9190–9195.

    Google Scholar 

  • Ginsberg, D., Vairo, G., Chittenden, T., Xiao, Z.-X., Xu, G., Wydner, K.L., DeCaprio, J.A., Lawrence, J.B. and Livingston, D.M. 1994. E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev. 8: 2665–2679.

    Google Scholar 

  • Girling, R., Partridge, J.F., Bandara, L.R., Burden, N., Totty, N.F., Hsuan, J.J. and La Thangue, N.B. 1993. A new component of the transcription factor DRTF1/E2F. Nature 362: 83–87.

    Google Scholar 

  • Grafi, G., Burnett, R.J., Helentjaris, T., Larkins, B.A., DeCaprio, J., Sellers, W.R. and Kaelin, W.G. Jr. 1996. A maize cDNA encoding a member of the retinoblastoma protein family: Involvement in endoreduplication. Proc. Natl. Acad. Sci. USA 93: 8962–8967.

    Google Scholar 

  • Gutiérrez, C. 1998. The retinoblastoma pathway in plant cell cycle and development. Curr. Opin. Plant Biol. 1: 492–497.

    Google Scholar 

  • Harper, J.W., Adami, G.R., Wei, N., Keyomarsi, K. and Elledge, S.J. 1993. The p21 cdk-interacting protein cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805–816.

    Google Scholar 

  • Hateboer, G., Wobst, A., Petersen, B.O., Le Cam, L., Vigo, E., Sardet, C. and Helin, K. 1998. Cell cycle-regulated expression of mammalian CDC6 is dependent on E2F. Mol. Cell Biol. 18: 6679–6697.

    Google Scholar 

  • Helin, K., Lees, J.A., Vidal, M., Dyson, N., Harlow, E. and Fat-taey, A. 1992. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell 70: 337–350.

    Google Scholar 

  • Helin, K., Wu, C.-L., Fattaey, A.R., Lees, J.A., Dynlacht, B.D., Ngwu, C. and Harlow, E. 1993. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7: 1850–1861.

    Google Scholar 

  • Helin, K. 1998. Regulation of cell proliferation by the E2F tran-scription factors. Curr. Opin. Genet. Dev. 8: 28–35.

    Google Scholar 

  • Herwig, S. and Strauss, M. 1997. The retinoblastoma protein: a master regulator of cell cycle, differentiation and apoptosis. Eur. J. Biochem. 246: 581–601.

    Google Scholar 

  • Huntley, R. P. and Murray, J.A.H. 1999. The plant cell cycle. Curr. Opin. Plant Biol. 2: 440–446.

    Google Scholar 

  • Huntley, R., Healy, S., Freeman, D., Lavender, P., de Jager, S., Greenwood, J., Makker, J., Walker, E., Jackman, M., Xie, Q., Bannister, A. J., Kouzarides, T., Guitiérrez, C., Doonan, J. and Murray, J.A.H. 1998. The maize retinoblastoma protein homo-logue ZmRb-1 is regulated during leaf development and displays conserved interactions with G1/S regulators and plant cyclin D (CycD) proteins. Plant Mol. Biol. 37: 155–169.

    Google Scholar 

  • Inzé, D., Gutiérrez, C. and Chua, N.-H. 1999. Trends in plant cell cycle research. Plant Cell 11: 991–994.

    Google Scholar 

  • Kaelin, W.G., Jr., Krek, W., Sellers, W.R., DeCaprio, J.A., Ajchen-baum, F., Fuchs, C.S., Chittenden, T., Li, Y., Farnham, P.J., Blana, M.A., Livingston, D.M. and Flemington, E.K. 1992. Ex-pression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell 70: 351–364.

    Google Scholar 

  • Kong, L.J., Orozco, B.M., Roe, J.L., Nagar, S., Ou, S., Feiler, H.S., Durfee, T., Miller, A.B., Gruissem, W., Robertson, D. and Hanley-Bowdoin, L. 2000. A geminivirus replication protein in-teracts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants. EMBO J. 19: 3485–3495.

    Google Scholar 

  • Krek, W., Livingston, D.M. and Shirodkar, S. 1993. Binding to DNA and the retinoblastoma gene product promoted by com-plex formation of different E2F family members. Science 262: 1557–1560.

    Google Scholar 

  • Leone, G., DeGregori, J., Yan, Z., Jakoi, L., Ishida, S., Williams, R.S. and Nevins, J.R. 1998. E2F3 activity is regulated during the cell cycle and is required for the induction of S phase. Genes Dev. 12: 2120–2130.

    Google Scholar 

  • Lindeman, G.J., Gaubatz, S., Livingston, D.M. and Ginsberg, D. 1997. The subcellular localization of E2F-4 is cell-cycle dependent. Proc. Natl. Acad. Sci. USA 94: 5095–5100.

    Google Scholar 

  • Magae, J., Wu, C.-L., Illenye, S., Harlow, E. and Heintz, N.H. 1996 Nuclear localisation of DP and E2F transcription factors by het-erodimeric partners and retinoblastoma protein family members. J. Cell Sci. 109: 1717–1726.

    Google Scholar 

  • Magyar, Z., Atanassova, A., De Veylder, L., Rombauts, S. and Inzé, D. 2000. Characterization of two distinct DP-related genes from Arabidopsis thaliana. FEBS Lett. 486: 79–87.

    Google Scholar 

  • Martínez-Balbás, M., Bauer, U.-M., Nielsen, S.J., Brehm, A. and Kouzarides, T. 2000. Regulation of E2F1 activity by acetylation. EMBO J. 19: 101–110.

    Google Scholar 

  • May, M.J. and Leaver, C.J. 1993. Oxidative stimulation of glutathione synthesis in Arabidopsis thaliana suspension cultures. Plant Physiol. 103: 621–627.

    Google Scholar 

  • Miller, J.H. 1972. Assay of β¶galactosidase. In: Experiments in Molecular Genetics, Cold Spring Harbor Laboraty Press, Plainview, NY, pp. 352–355.

    Google Scholar 

  • Minet, M., Dufour, M.-E. and Lacroute, F. 1992. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2: 417–422.

    Google Scholar 

  • Müller, H., Moroni, M.C., Vigo, E., Petersen, B.O., Bartek, J. and Helin K. 1997. Induction of S-phase entry by E2F transcription factors depends on their nuclear localization. Mol. Cell Biol. 17: 5508–5520.

    Google Scholar 

  • Murray, J.A.H. 1997. The retinoblastoma protein is in plants! Trends Plant Sci. 2: 82–84.

    Google Scholar 

  • Murray, J.A.H., Scarpa, M., Rossi, N. and Cesareni, G. 1987. Antagonistic controls regulate copy number of the yeast 2 µ plasmid. EMBO J. 6: 4205–4212.

    Google Scholar 

  • Nakagami, H., Sekine, M., Murakami, H. and Shinmyo, A. 1999. Tobacco retinoblastoma-related protein phosphorylation by a distinct cyclin-dependent kinase complex with Cdc2/cyclin D in vitro. Plant J. 18: 243–252.

    Google Scholar 

  • Nakai, K. and Kanehisa, M. 1992. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14: 897–911.

    Google Scholar 

  • Ohtani, K. and Nevins, J. R. 1994. Functional properties of a Drosophila homolog of the E2F1 gene. Mol. Cell Biol. 14: 1603–1612.

    Google Scholar 

  • Ohtani, K., DeGregori, J., Leone, G., Herendeen, D.R., Kelly, T.J. and Nevins, J.R. 1996. Expression of the HsOrc1 gene, a human ORC1 homolog, is regulated by cell proliferation via the E2F transcription factor. Mol. Cell Biol. 16: 6977–6984.

    Google Scholar 

  • Ramírez-Parra, E. and Gutiérrez, C. 2000. Characterisation of wheat DP, a heterodimerisation partner of the plant E2F transcription factor which stimulates E2F-DNA binding. FEBS Lett. 486: 73–78.

    Google Scholar 

  • Ramírez-Parra, E., Xie, Q., Boniotti, M.B. and Gutiérrez, C. 1999. The cloning of plant E2F, a retinoblastoma-binding protein, re-veals unique and conserved features with animal G1/S regulators. Nucl. Acids Res. 27: 3527–3533.

    Google Scholar 

  • Reichheld, J.-P., Sonobe, S., Clément, B., Chaubet, N. and Gigot, C. 1995. Cell cycle-regulated histone gene expression in synchronised plant cells. Plant J. 7: 245–252.

    Google Scholar 

  • Reichmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C.-Z., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R., Creelman, R., Pilgrim, M., Broun, P., Zhang, J.Z., Ghandehari, D., Sherman, B.K. and Yu, G.-L. 2000. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105–2110.

    Google Scholar 

  • Renaudin, J.-P., Doonan, J.H., Freeman, D., Hashimoto, J., Hirt, H., Inzé, D., Jacobs, T., Kouchi, H., Rouzé, P., Sauter, M., Savouré, A., Sorrell, D.A., Sundaresan, V. and Murray, J.A.H. 1996. Plant cyclins: a unified nomenclature for plant A-, B-and D-type cyclins based on sequence organization. Plant Mol. Biol. 32: 1003–1018.

    Google Scholar 

  • Renz, A., Fountain, M.D. and Beck, E. 1997. Nucleotide sequence of a cDNA encoding a D-type cyclin from a photoautotrophic cell suspension culture of Chenopodium rubrum L. Plant Physiol. 113: 1004.

    Google Scholar 

  • Riou-Khamlichi, C., Huntley, R., Jacqmard, A. and Murray, J.A.H. 1999. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544.

    Google Scholar 

  • Riou-Khamlichi, C., Menges, M., Healy, J.M.S. and Murray, J.A.H. 2000. Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol. Cell Biol. 20: 4513–4521.

    Google Scholar 

  • Sardet, C., Vidal, M., Cobrinik, D., Geng, Y., Onufryk, C., Chen, A. and Weinberg, R.A. 1995. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc. Natl. Acad. Sci. USA 92: 2403–2407.

    Google Scholar 

  • Sawado, T., Yamaguchi, M., Nishimoto, Y., Ohno, K., Sakaguchi, K. and Matsukage, A. 1998. dE2F2, a novel E2F-family transcription factor in Drosophila melanogaster.Biochem. Biophys. Res. Commun. 251: 409–415.

    Google Scholar 

  • Schiestl, R.H., Manivasakam, P., Woods, R.A. and Gietz, R.D. 1993. Introducing DNA into yeast by transformation. Methods (A Companion to Meth. Enzymol.) 5: 79–85.

    Google Scholar 

  • Sears, R., Ohtani, K. and Nevins, J.R. 1997. Identification of positively and negatively acting elements regulating expression of the E2F gene in response to cell growth signals. Mol Cell Biol. 17: 5227–5235.

    Google Scholar 

  • Segers, G., Gadisseur, I., Bergounioux, C., de Almeida Engler, J., Jacqmard, A., Van Montagu, M. and Inzé, D. 1996. The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases of the cell cycle. Plant J. 10: 601–612.

    Google Scholar 

  • Sekine, M., Ito, M., Uemukai, K., Maeda, Y., Nakagami, H. and Shinmyo, A. 1999. Isolation and characterization of the E2F-like gene in plants. FEBS Lett. 460: 117–122.

    Google Scholar 

  • Shan, B., Zhu, Z., Chen, P.-L., Durfee, T., Yang, Y., Sharp, D. and Lee, W.-H. 1992. Molecular cloning of cellular genes encoding retinoblastoma-associated proteins: identification of a gene with properties of the transcriptional factor E2F Mol. Cell Biol. 12: 5620–5631.

    Google Scholar 

  • Shan, B., Durfee, T. and Lee, W.-H. 1996. Disruption of Rb/E2F-1 interaction by single point mutations in E2F-1 enhances S-phase entry and apoptosis. Proc. Natl. Acad. Sci. USA 93: 679–684.

    Google Scholar 

  • Shirodkar, S., Ewen, M., DeCaprio, J.A., Morgan, J., Livingston, D.M. and Chittenden, T. 1992. The transcription factor E2F interacts with the retinoblastoma product and a p107-cyclin A complex in a cell cycle-regulated manner. Cell 68: 157–166.

    Google Scholar 

  • Slansky, J.E., Li, Y., Kaelin, W.G. and Farnham, P.J. 1993. A protein synthesis-dependent increase in E2F1 mRNA correlates with growth regulation of the dihydrofolate reductase promoter. Mol. Cell Biol. 13: 1610–1618.

    Google Scholar 

  • Slansky, J.E. and Farnham, P.J. 1996. Introduction to the E2F family: Protein structure and gene regulation. In: P.J. Farnham (Ed.) Transcriptional Control of Cell Growth: The E2F Gene Family, Springer-Verlag, Berlin, pp. 1–30.

    Google Scholar 

  • Soni, R., and Murray, J.A.H. 1994. Isolation of intact DNA and RNA from plant tissues. Anal. Biochem. 218: 474–476.

    Google Scholar 

  • Soni, R., Carmichael, J.P., Shah, Z.H. and Murray, J.A.H. 1995. A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblas-toma protein interaction motif. Plant Cell 7: 85–103.

    Google Scholar 

  • Sorrell, D.A., Combettes, B., Chaubet-Gigot, N., Gigot, C. and Murray, J.A.H. 1999. Distinct cyclin D genes show mitotic accumulation or constant levels of transcripts in tobacco bright yellow-2 cells. Plant Physiol. 119: 343–351.

    Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 24: 4876–4882.

    Google Scholar 

  • Trimarchi, J.M., Fairchild, B., Verona, R., Moberg, K., Andon, N. and Lees, J.A. 1998. E2F-6, a member of the E2F family that can behave as a transcriptional repressor. Proc. Natl. Acad. Sci. USA 95: 2850–2855.

    Google Scholar 

  • Vaishnav, Y.N., Vaishnav, M.Y. and Pant, V. 1998. The molecu-lar and functional characterization of E2F-5 transcription factor. Biochem. Biophys. Res. Commun. 242: 0586–592.

    Google Scholar 

  • Verona, R., Moberg, K., Estes, S., Starz, M., Vernon, J.P. and Lees, J.A. 1997. E2F activity is regulated by cell cycledependent changes in subcellular localization. Mol. Cell Biol. 17: 7268–7282.

    Google Scholar 

  • Verwoerd, T.C., Dekker, B.M.M. and Hoekema, A. 1989. A small-scale procedure for the rapid isolation of plant RNAs. Nucl. Acids Res. 17: 2362.

    Google Scholar 

  • Vigo, E., Müller, H., Prosperini, E., Hateboer, G., Cartwright, P., Moroni, M.C. and Helin, K. 1999. CDC25A phosphatase is a target of E2F and is required for efficient E2F-induced S phase. Mol. Cell Biol. 19: 6379–6395.

    Google Scholar 

  • Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell 81: 323–330.

    Google Scholar 

  • Xie, Q., Sanz-Burgos, A., Hannon, G. and Gutiérrez, C. 1996. Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. EMBO J. 15: 4900–4908.

    Google Scholar 

  • Zheng, N., Fraenkel, E., Pabo, C.O. and Pavletich, N.P. 1999. Struc-tural basis of DNA recognition by the heterodimer cell cycle transcription factor E2F-DP. Genes Dev. 13: 666–674.

    Google Scholar 

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de Jager, S., Menges, M., Bauer, UM. et al. Arabidopsis E2F1 binds a sequence present in the promoter of S-phase-regulated gene AtCDC6 and is a member of a multigene family with differential activities. Plant Mol Biol 47, 555–568 (2001). https://doi.org/10.1023/A:1011848528377

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