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Expression and activity of a Kip-related protein, Zeama;KRP1, during maize germination

Published online by Cambridge University Press:  01 June 2008

Natividad de Jesús Juárez
Affiliation:
Facultad de Química, Departamento de Bioquímica, Universidad Nacional Autónoma de México, MéxicoD.F. 04510
Alfredo Mancilla
Affiliation:
Facultad de Química, Departamento de Bioquímica, Universidad Nacional Autónoma de México, MéxicoD.F. 04510
Elpidio García
Affiliation:
Facultad de Química, Departamento de Bioquímica, Universidad Nacional Autónoma de México, MéxicoD.F. 04510
Jorge M. Vázquez-Ramos*
Affiliation:
Facultad de Química, Departamento de Bioquímica, Universidad Nacional Autónoma de México, MéxicoD.F. 04510
*
*Correspondence Fax: +52 55 56225329[email protected]

Abstract

Plant KRP proteins are cyclin/cyclin-dependent kinase subunit (Cdk) inhibitors that share a limited homology with mammalian p27Kip1 proteins. Several KRPs have been reported in maize (Zea mays L.), of which Zeama;KRP1 was studied during maize germination. Expression of the Zeama;KRP1 gene did not vary during the 24 h germination period. A homologous antibody raised against the 13 kDa carboxy end of the Zeama;KRP1 polypeptide, a sequence containing the cyclin/Cdk inhibitory domain, indicated the existence of a 22 kDa protein in maize embryonic axes, the amount of which also remained unchanged during germination. Neither abscisic acid nor cytokinins modified the amount of protein. The purified Zeama;KRP1 polypeptide inhibited the kinase activity associated with Zeama;PCNA and Zeama;CycD2;1, and also the kinase activity in p13Suc1-pulled-down complexes. However, there were differences in the inhibition pattern during germination. Whereas kinase activity in proliferating cell nuclear antigen (PCNA) or CycD2;1 immunoprecipitates was strongly inhibited mainly during early germination, that in p13Suc1-pulled-down complexes was mainly inhibited at late times, suggesting that each protein complex is composed of different cyclins and/or Cdks.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2008

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References

Baíza, A.M., Vázquez-Ramos, J.M. and Sánchez de Jiménez, E. (1989) DNA synthesis and cell division in embryonic maize tissues during germination. Journal of Plant Physiology 135, 416421.CrossRefGoogle Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248252.CrossRefGoogle ScholarPubMed
Coelho, C.M., Dante, R.A., Sabelli, P.A., Sun, Y., Dilkes, B.P., Gordon-Kamm, W.J. and Larkins, B.A. (2005) Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication. Plant Physiology 138, 23232336.CrossRefGoogle ScholarPubMed
De Veylder, L., Beeckman, T., Beemster, G.T.S., Krols, L., Terras, P., Landrieu, I., Van der Schueren, E., Maes, S., Naudts, M. and Inzé, D. (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13, 16531667.CrossRefGoogle ScholarPubMed
Gutiérrez, R., Quiroz, F. and Vázquez-Ramos, J.M. (2005) Maize cyclin D2 expression, associated kinase activity and effect of phytohormones during germination. Plant and Cell Physiology 46, 166173.CrossRefGoogle ScholarPubMed
Hayles, J., Aves, S. and Nurse, P. (1986) suc1 is an essential gene involved in both the cell cycle and growth in fission yeast. EMBO Journal 5, 33733379.CrossRefGoogle ScholarPubMed
Jasinski, S., Riou-Khamlichi, C., Roche, O., Perennes, C., Bergounioux, C. and Glab, N. (2002) The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3;1-overexpressing plants. Journal of Cell Science 115, 973982.CrossRefGoogle ScholarPubMed
Jemmerson, R. (1987) Multiple overlapping epitopes in the three antigenic regions of horse cytochrome C. Journal of Immunology 138, 213219.CrossRefGoogle Scholar
Nakai, T., Kato, K., Shinmyo, A. and Sekine, M. (2006) Arabidopsis KRPs have distinct inhibitory activity toward cyclin D2-associated kinases, including plant-specific B-type cyclin-dependent kinase. FEBS Letters 580, 336340.CrossRefGoogle ScholarPubMed
Pavletich, N.P. (1999) Mechanisms of cyclin-dependent kinase regulation: structures of Cdks, their cyclin activators, and Cip and INK4 inhibitors. Journal of Molecular Biology 287, 821828.CrossRefGoogle ScholarPubMed
Pettkó-Szandtner, A., Mészaros, M., Horvath, G.V., Bakó, L., Csordás-Toth, E., Blastyák, A., Zhiponova, M., Miskolczi, P. and Dudits, D. (2006) Activation of an alfalfa cyclin-dependent kinase inhibitor by calmodulin-like domain protein kinase. Plant Journal 46, 111123.CrossRefGoogle ScholarPubMed
Pines, J. (1995) Cyclins and cyclin-dependent kinases: theme and variations. Advances in Cancer Research 66, 181212.CrossRefGoogle ScholarPubMed
Quiroz-Figueroa, F. and Vázquez-Ramos, J.M. (2006) Expression of maize D-type cyclins: comparison, regulation by phytohormones during seed germination and description of a new D cyclin. Physiologia Plantarum 128, 556568.CrossRefGoogle Scholar
Ramirez-Parra, E., Xie, Q., Boniotti, M.B. and Gutierrez, C. (1999) The cloning of plant E2F, a retinoblastoma-binding protein, reveals unique and conserved features with animal G1/S regulators. Nucleic Acids Research 27, 35273533.Google Scholar
Rank, K.B., Evans, D.B. and Sharma, S.K. (2000) The N-terminal domains of cyclin-dependent kinase inhibitory proteins block the phosphorylation of cdk2/cyclin E by the CDK-activating kinase. Biochemical and Biophysical Research Communications 271, 469473.CrossRefGoogle 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 Molecular Biology 32, 10031018.CrossRefGoogle Scholar
Sánchez, M.D., Gurusinghe, S.H., Bradford, K.J. and Vázquez-Ramos, J.M. (2005) Differential response of PCNA and Cdk-A proteins and associated kinase activities to benzyladenine and abscisic acid during maize seed germination. Journal of Experimental Botany 56, 515523.CrossRefGoogle ScholarPubMed
Sánchez, M.D., Torres, A., Boniotti, M.B., Gutierrez, C. and Vázquez-Ramos, J.M. (2002) PCNA protein associates to Cdk-A type protein kinases in germinating maize. Plant Molecular Biology 50, 167175.CrossRefGoogle Scholar
Sherr, C.J. and Roberts, J.M. (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes and Development 13, 15011512.CrossRefGoogle ScholarPubMed
Stals, H. and Inzé, D. (2001) When plant cells decide to divide. Trends in Plant Science 6, 359364.CrossRefGoogle ScholarPubMed
Vandepoele, K., Raes, J., De Veylder, L., Rouzé, P., Rombauts, S. and Inzé, D. (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14, 903916.CrossRefGoogle ScholarPubMed
Vázquez-Ramos, J.M. and Sánchez, M.D. (2003) The cell cycle and seed germination. Seed Science Research 13, 113130.CrossRefGoogle Scholar
Verkest, A., Weinl, C., Inzé, D., De Veylder, L. and Schnittger, A. (2005) Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiology 139, 10991106.CrossRefGoogle ScholarPubMed
Wang, G.F., Kong, H.Z., Sun, Y.J., Zhang, X.H., Zhang, W., Altman, N., de Pamphilis, C.W. and Ma, H. (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of the plant cyclin-like proteins. Plant Physiology 135, 10841099.CrossRefGoogle ScholarPubMed
Wang, H., Qi, Q.G., Schorr, P., Cutler, A.J., Crosby, W.L. and Fowke, L.C. (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant Journal 15, 501510.CrossRefGoogle Scholar
Wang, H., Zhou, Y., Gilmer, S., Cleary, A., John, P., Whitwill, S. and Fowke, L. (2003) Modifyng plant growth and development using the CDK inhibitor ICK1. Cell Biology International 27, 297299.CrossRefGoogle Scholar
Weinl, C., Marquardt, S., Kuijt, S.J.H., Nowack, M.K., Jakoby, M.J., Hülskamp, M. and Schnittger, A. (2005) Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell 17, 17041722.CrossRefGoogle ScholarPubMed
Xiong, Y., Zhang, H. and Beach, D. (1992) D-type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71, 505514.CrossRefGoogle ScholarPubMed
Zhou, Y., Fowke, L.C. and Wang, H. (2002) Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Reports 20, 967975.CrossRefGoogle Scholar