Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T15:49:09.378Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of insulin on the cell cycle of germinating maize seeds (Zea mays L.)

Published online by Cambridge University Press:  11 January 2013

Alma X. Avila-Alejandre ,
Fulgencio Espejel ,
Esmeralda Paz-Lemus ,
Edith Cortés-Barberena ,
Fernando Díaz de León-Sánchez ,
Tzvetanka D. Dinkova ,
Estela Sánchez de Jiménez  and
Laura J. Pérez-Flores
Alma X. Avila-Alejandre
Affiliation:
Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana, Av. San Rafael Atlixco 186, Col., VicentinaCP 09340, D.F. México
Fulgencio Espejel
Affiliation:
Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana, Av. San Rafael Atlixco 186, Col., VicentinaCP 09340, D.F. México
Esmeralda Paz-Lemus
Affiliation:
Departamento de Bioquímica y Biología Molecular de Plantas, Facultad de Química, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP 04510, D.F. México
Edith Cortés-Barberena
Affiliation:
Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana, Av. San Rafael Atlixco 186, Col., VicentinaCP 09340, D.F. México
Fernando Díaz de León-Sánchez
Affiliation:
Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana, Av. San Rafael Atlixco 186, Col., VicentinaCP 09340, D.F. México
Tzvetanka D. Dinkova
Affiliation:
Departamento de Bioquímica y Biología Molecular de Plantas, Facultad de Química, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP 04510, D.F. México
Estela Sánchez de Jiménez
Affiliation:
Departamento de Bioquímica y Biología Molecular de Plantas, Facultad de Química, Universidad Nacional Autónoma de México, Ciudad Universitaria, CP 04510, D.F. México
Laura J. Pérez-Flores*
Affiliation:
Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana, Av. San Rafael Atlixco 186, Col., VicentinaCP 09340, D.F. México
*
*Correspondence E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

During seed germination, metabolism is reactivated, DNA is repaired and cell division is restarted in the meristems. The mechanisms that co-ordinate cell growth and division in maize embryonic axes during germination are not well understood. However, the presence of a factor similar to IGF (insulin-like growth factor) that accelerates germination has been reported. In the present work, the regulation of the cell-cycle restart by bovine insulin [which has been demonstrated to produce similar effects as insulin-like growth factor of maize (ZmIGF) in maize seeds] was studied in germinating embryonic axes. Our results showed that bovine insulin differentially stimulates growth, S6K phosphorylation, S6rp transcript accumulation on the polysomal fraction, as well as de novo DNA synthesis in the radicles and the coleoptiles of the embryonic axis. A stronger and earlier effect was observed in radicles compared to coleoptiles; therefore, the effect of insulin on the cell cycle of the root meristem was studied by flow cytometry. The G1–S transition was stimulated and cell proliferation was induced. Furthermore, it was determined by quantitative reverse transcription-polymerase chain reaction (qRT-PCR) that bovine insulin increased E2F and PCNA (proliferating cell nuclear antigen) transcription after 15 h of germination and PCNA de novo synthesis at 15 h of germination. These results show that bovine insulin preferentially stimulates growth in the radicles of germinating embryonic axes and suggest that its effect on the G1–S transition and the activation of cell proliferation is mediated by the induction of E2F and PCNA transcription.

Keywords

E2F transcription factorinsulin-like growth factor in Zea mays (ZmIGF)proliferating cell nuclear antigen (PCNA)Zea mays
Type
Research Papers
Information
Seed Science Research , Volume 23 , Issue 1 , March 2013 , pp. 3 - 14
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexandrov, N.N., Brover, V.V., Freidin, S., Troukhan, M.E., Tatarinova, T.V., Zhang, H., Swaller, T.J., Lu, Y.P., Bouck, J., Flavell, R.B. and Feldmann, K.A. (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Molecular Biology 69, 179–194.CrossRefGoogle ScholarPubMed
Baíza, M.A. and Sánchez de Jiménez, E. (1989) Effect of auxin, 2-(2 methyl-4-chloro-phenoxy) propionic acid on cell cycle regulation in maize embryonic tissues. Physiologia Plantarum 75, 261–266.CrossRefGoogle Scholar
Barroco, R.M., Van Poucke, K., Bergervoet, J.H., De Veylder, L., Groot, S.P., Inzé, D. and Engler, G. (2005) The role of the cell cycle machinery in resumption of post-embryonic development. Plant Physiology 137, 127–140.CrossRefGoogle Scholar
Baserga, R. (2007) Is cell size important? Cell Cycle 7, 814–816.CrossRefGoogle Scholar
Blagosklonny, M.V. and Pardee, A.B. (2002) The restriction point of the cell cycle. Cell Cycle 2, 103–110.Google 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, 248–254.CrossRefGoogle ScholarPubMed
Buentello-Volante, B., Díaz de León-Sánchez, F., Rivera-Cabrera, F., Aguilar Caballero, R., Ponce-Valadez, M., Sánchez de Jiménez, E. and Pérez-Flores, L.J. (2010) Apparent cross-talk of two signaling pathways that regulate Zea mays coleoptile growth. Phyton 79, 101–108.CrossRefGoogle Scholar
Bustin, S.A., Benes, V., Garson, J.A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M.W., Shipley, G.L., Vandesompele, J. and Wittwer, C.T. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.CrossRefGoogle ScholarPubMed
Chakravarty, K. and Hanson, R.W. (2007) Insulin regulation of phosphoenolpyruvate carboxykinase-C gene transcription: the role of sterol regulatory element-binding protein 1c. Nutrition Reviews 65, S47–S56.CrossRefGoogle ScholarPubMed
Collier, E., Watkinson, A., Cleland, C.F. and Roth, J. (1987) Partial purification and characterization of an insulin-like material from spinach and Lemna gibba G3. Journal of Biological Chemistry 262, 6238–6247.CrossRefGoogle ScholarPubMed
Dinkova, T.D., Reyes de la Cruz, H., García-Flores, C., Aguilar, R., Jiménez-Garcıa, L.F. and Sánchez de Jiménez, E. (2007) Dissecting the TOR–S6K signal transduction pathway in maize seedlings: relevance on cell growth regulation. Physiologia Plantarum 130, 1–10.CrossRefGoogle Scholar
Dissmeyer, N., Weimer, A.K., Veylder, L.D., Novak, B. and Schnittger, A. (2010) The regulatory network of cell cycle progresssion is fundamentally different in plants versus yeast or metazoans. Plant Signaling & Behavior 5, 1613–1618.CrossRefGoogle ScholarPubMed
Frederick, T.J., Min, J., Altieri, S.C., Mitchell, N.E. and Wood, T.L. (2007) Synergistic induction of cyclin D1 in oligodendrocyte progenitor cells by IGF-I and FGF-2 requires differential stimulation of multiple signaling pathways. Glia 55, 1011–1022.CrossRefGoogle ScholarPubMed
García-Flores, C., Aguilar, R., Reyes de la Cruz, H., Albores, M. and Sánchez de Jiménez, E. (2001) A maize insulin-like growth factor signals to a transduction pathway that regulates protein synthesis in maize. Biochemical Journal 358, 95–100.CrossRefGoogle ScholarPubMed
Garrocho-Villegas, V. and Sánchez de Jiménez, E. (2012) TOR pathway activation in Zea mays L. tissues: Conserved function between animal and plant kingdoms. Plant Signaling & Behavior 7, 1–3.CrossRefGoogle ScholarPubMed
Gendreau, E., Romaniello, S., Barad, S., Leymarie, J., Benech-Arnold, R. and Corbineau, F. (2008) Regulation of cell cycle activity in the embryo of barley seeds during germination as related to grain hydration. Journal of Experimental Botany 52, 203–212.CrossRefGoogle Scholar
Goodman, D.B.P. and Davis, W.L. (1993) Insulin accelerates the post germinative development of several fat-storing seeds. Biochemical and Biophysical Research Communications 190, 440–446.CrossRefGoogle ScholarPubMed
Harashima, H. and Schnittger, A. (2010) The integration of cell division, growth and differentiation. Current Opinion in Plant Biology 13, 66–74.CrossRefGoogle ScholarPubMed
Herrera, I., Sánchez-de la Paz, M., Molinab, J., Plasencia, J. and Vázquez-Ramos, J. (2000) Proliferating cell nuclear antigen expression in maize seed development and germination: Regulation by phytohormones and its association with putative cell cycle proteins. Physiologia Plantarum 110, 127–134.CrossRefGoogle Scholar
Jiménez-López, S., Mancera-Martínez, E., Donayre-Torres, A., Rangel, C., Uribe, L., March, S., Jiménez-Sánchez, G. and Sánchez de Jiménez, E. (2011) Expression profile of maize (Zea mays L.) embryonic axes during germination: translational regulation of ribosomal protein mRNAs. Plant & Cell Physiology 52, 1719–1733.CrossRefGoogle ScholarPubMed
Lammens, T., Li, J., Leone, G. and De Veylder, L. (2009) A typical E2Fs: new players in the E2F transcription factor family. Trends in Cell Biology 19, 111–118.CrossRefGoogle Scholar
Luthe, D.S. and Quatrano, R.S. (1980) Transcription in isolated wheat nuclei: I. Isolation of nuclei and elimination of endogenous ribonuclease activity. Plant Physiology 65, 305–308.CrossRefGoogle ScholarPubMed
Lydeard, J.R., Lipkin-Moore, Z., Sheu, Y.J., Stillman, B., Burgers, P.M. and Haber, J.E. (2010) Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes & Development 24, 1133–1144.CrossRefGoogle ScholarPubMed
Magyar, Z., De Veylder, L., Atanassova, A., Bakó, L., Inzé, D. and Bogre, L. (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin cell division. Plant Cell 17, 2527–2541.CrossRefGoogle ScholarPubMed
Mairet-Coello, G., Tury, A. and DiCicco-Bloom, E. (2009) Insulin-like growth factor-1 promotes G(1)/S cell cycle progression through bidirectional regulation of cyclins and cyclin-dependent kinase inhibitors via the phosphatidylinositol 3-kinase/Akt pathway in developing rat cerebral cortex. Journal of Neuroscience 29, 775–788.CrossRefGoogle ScholarPubMed
Meyuhas, O. and Dreazen, A. (2009) Ribosomal protein S6 kinase: from TOP mRNAs to cell size. Progress in Molecular Biology and Translational Science 90, 109–153.CrossRefGoogle ScholarPubMed
Mounier, C. and Posner, B.I. (2006) Transcripcional regulation by insulin: from the receptor to the gene. Canadian Journal of Physiology and Pharmacology 84, 713–724.CrossRefGoogle Scholar
Nelsen, C.J., Rickheims, D.G., Tucker, M.M., Hansen, L.K. and Albrech, J.H. (2003) Evidence that cyclin D1 mediates both growth and proliferation downstream of TOR in hepatocytes. Journal of Biological Chemistry 278, 3656–3663.CrossRefGoogle ScholarPubMed
Oliveira, A., Ribeiro, E.S., da Cunha, M., Gomes, V.M., Fernández, K. and Xavier-Filho, J. (2004) Insulin accelerates seedling growth of Canavalia ensiformis (Jack bean). Plant Growth Regulation 43, 57–62.CrossRefGoogle Scholar
Patursky-Polischuk, I., Stolovich-Rain, M., Hausner-Hanochi, M., Kasir, J., Cybulski, N., Avruch, J., Rüegg, M.A., Hall, M.N. and Meyuhas, O. (2009) The TSC-mTOR pathway mediates translational activation of TOP mRNAs by insulin largely in a raptor- or rictor-independent manner. Molecular and Cellular Biology 29, 640–649.CrossRefGoogle ScholarPubMed
Reyes de la Cruz, H., Aguilar, R. and Sánchez de Jiménez, E. (2004) Functional characterization of a maize ribosomal S6 protein kinase (ZmS6K), a plant ortholog of metazoan p70 (S6K). Biochemistry 43, 533–539.CrossRefGoogle ScholarPubMed
Rodríguez-López, C.D., Rodríguez-Romero, A., Aguilar, R. and Sánchez de Jiménez, E. (2011) Biochemical characterization of a new maize (Zea mays L.) peptide growth factor. Protein and Peptide Letters 18, 84–91.CrossRefGoogle ScholarPubMed
Sabelli, P.A., Dante, R.A., Leiva-Neto, J.T., Jung, R., Gordon-Kamm, W.J. and Larkins, B.A. (2005) RBR3, a member of the retinoblastoma-related family from maize, is regulated by the RBR1/E2F pathway. Proceedings of the National Academy of Sciences, USA 102, 13005–13012.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning: A laboratory manual (2nd edition). New York, Cold Spring Harbor Laboratory Press.Google Scholar
Sánchez, M.P., 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, 515–523.CrossRefGoogle ScholarPubMed
Sánchez de Jiménez, E., Beltrán-Peña, E. and Ortíz-López, A. (1999) Insulin-stimulated ribosomal protein synthesis in maize embryonic axes during germination. Physiologia Plantarum 105, 148–154.CrossRefGoogle Scholar
Santisree, P., Nongmaithem, S., Vasuki, H., Sreelakshmi, Y., Ivanchenko, M. and Sharma, R. (2011) Tomato root penetration in soil requires a co-action between ethylene and auxin signaling. Plant Physiology 156, 1424–1438.CrossRefGoogle Scholar
Sliwinska, E., Zielinska, E.andJedrzejczyk, I. (2005) Are seeds suitable for flow cytometric estimation of plant genome size? Cytometry 64, 72–79.CrossRefGoogle ScholarPubMed
Sotelo, R., Garrocho-Villegas, V., Aguilar, R., Calderón, M.E. and Sánchez de Jiménez, E. (2010) Coodination of cell growth and cell division in maize (Zea mays): Relevance of the conserved TOR signal transduction pathway. In Vitro Cellular & Developmental Biology Plant 46, 578–586.CrossRefGoogle Scholar
Sozzani, R., Maggio, C., Giordo, R., Umana, E., Ascencio-Ibañez, J.T., Hanley-Bowdoin, L., Bergouioux, C., Cella, R. and Albani, D. (2010) The E2F/DEL2 factor is a component of a regulatory and development in Arabidopsis. Plant Molecular Biology 72, 381–395.CrossRefGoogle ScholarPubMed
Strzalka, W. and Ziemienowicz, A. (2011) Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Annals of Botany 107, 1127–1140.CrossRefGoogle ScholarPubMed
Sun, H., Tu, X. and Baserga, R. (2007) A mechanism for cell size regulation by insulin and insulin like growth factor-I receptors. Cancer Research 66, 11106–11109.CrossRefGoogle Scholar
Suryadinata, R., Sadowski, M. and Sarcevic, B. (2010) Control of cell cycle progression by phosphorylation of cyclin-dependent kinase (CDK) substrates. Bioscience Reports 4, 243–255.CrossRefGoogle Scholar
Thomas, G. (2002) The S6 kinase signaling pathway in the control of development and growth. Biological Research 35, 305–313.CrossRefGoogle ScholarPubMed
Urban, J., Soulard, A., Huber, A., Lippman, S., Mukhopadhyay, D., Deloche, O., Wanke, V., Anrather, D., Ammerer, G., Riezman, H., Broach, J.R., De Virgilio, C., Hall, M.N. and Loewith, R. (2007) Sch9 is a major target of TORC1 in Saccharomyces cerevisiae. Molecular Cell 5, 663–674.CrossRefGoogle Scholar
Vázquez-Ramos, J.M. and Sánchez, M.P. (2003) The cell cycle and seed germination. Seed Science Research 13, 113–130.CrossRefGoogle Scholar
Willems, E., Leyns, L. and Vandesompele, J. (2008) Standarization or real-time PCR gene expression data from independent biological replicates. Analytical Biochemistry 379, 127–129.CrossRefGoogle ScholarPubMed
Wu, A., Tu, X., Prisco, M. and Baserga, R. (2005) Regulation of upstream binding factor 1 activity by insulin-like growth factor I receptor signaling. Journal of Biological Chemistry 280, 2863–2872.CrossRefGoogle ScholarPubMed