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Tight translational control by the initiation factors eIF4E and eIF(iso)4E is required for maize seed germination

Published online by Cambridge University Press:  21 March 2011

Tzvetanka D. Dinkova ,
Norma A. Márquez-Velázquez ,
Raúl Aguilar ,
Pedro E. Lázaro-Mixteco  and
Estela Sánchez de Jiménez
Tzvetanka D. Dinkova
Affiliation:
Departamento de Bioquímica, Facultad de Química, Universidad Nacional Autónoma de México, 04510 México D.F., México
Norma A. Márquez-Velázquez
Affiliation:
Departamento de Bioquímica, Facultad de Química, Universidad Nacional Autónoma de México, 04510 México D.F., México
Raúl Aguilar
Affiliation:
Departamento de Bioquímica, Facultad de Química, Universidad Nacional Autónoma de México, 04510 México D.F., México
Pedro E. Lázaro-Mixteco
Affiliation:
Departamento de Bioquímica, Facultad de Química, Universidad Nacional Autónoma de México, 04510 México D.F., México
Estela Sánchez de Jiménez*
Affiliation:
Departamento de Bioquímica, Facultad de Química, Universidad Nacional Autónoma de México, 04510 México D.F., México
*
*Correspondence Fax: +52 55 56225329 Email: estelas@servidor.unam.mx
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Abstract

A characteristic mechanism of gene expression regulation during seed germination is the selective translation of mRNAs. Previous findings indicate that the two cap-binding complexes eIF4F (with eIF4E and eIF4G subunits) and eIF(iso)4F [with eIF(iso)4E and eIF(iso)4G subunits] are differentially expressed during maize seed germination. In addition, several studies in vitro have suggested that these factors may participate in selective mRNA translation. The translational activities of eIF4E and eIF(iso)4E were tested in vitro using transcripts from two different sets: dry (0 h) and 24-h-imbibed maize embryonic axes. In vitro translation of these mRNA pools in the presence of the recombinant eIF4E or eIF(iso)4E, and the native cap-binding complexes from dry- or 24-h-imbibed axes, produced different profiles of proteins which were visualized by two-dimensional protein gels and autoradiography. The data indicated that eIF(iso)4E was particularly required for translation of the stored mRNAs from dry seeds, and that eIF4E was unable to fully replace the eIF(iso)4E activity. In addition, the dry seed mRNA pool was translated by the cap-binding complex isolated from dry seeds better than by the complex isolated from 24-h-imbibed seeds, whereas the translational efficiency of the mRNA pool from 24-h-imbibed seeds was similar between the cap-binding complexes from these two stages. Interestingly, eIF(iso)4E was more abundant than eIF4E in dry seeds, while both cap-binding proteins were present at similar levels in 24-h-imbibed seeds. These results suggest that the ratio of eIF(iso)4E to eIF4E in the corresponding eIF4F complex is critical for the mechanisms of translational control during maize germination.

Keywords

cap-binding proteinseIF4EeIF(iso)4Egerminationmaizestored mRNAstranslation regulation
Type
Research Papers
Information
Seed Science Research , Volume 21 , Issue 2 , June 2011 , pp. 85 - 93
Copyright
Copyright © Cambridge University Press 2011

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References

Browning, K.S. (2004) Plant translation initiation factors: it is not easy to be green. Biochemical Society Transactions 32, 589–591.CrossRefGoogle Scholar
Browning, K.S., Webster, C., Roberts, J.K.M. and Ravel, J.M. (1992) Identification of an isozyme form of protein synthesis initiation factor 4F in plants. Journal of Biological Chemistry 267, 10096–10100.CrossRefGoogle ScholarPubMed
Bush, M.S., Hutchins, A.P., Jones, A.M., Naldrett, M.J., Jarmolowski, A., Lloyd, C.W. and Doonan, J.H. (2009) Selective recruitment of proteins to 5′ cap complexes during the growth cycle in Arabidopsis. The Plant Journal 59, 400–412.CrossRefGoogle ScholarPubMed
Carberry, S.E. and Goss, D.J. (1991) Wheat germ initiation factors 4F and (iso)4F interact differently with oligoribonucleotide analogues of rabbit α-globin mRNA. Biochemistry 30, 4542–4545.CrossRefGoogle ScholarPubMed
Catusse, J., Job, C. and Job, D. (2008) Transcriptome- and proteome-wide analyses of seed germination. Comptes Rendus Biologies 331, 815–822.CrossRefGoogle ScholarPubMed
Dinkova, T.D. and Sanchez de Jimenez, E. (1999) Differential expression and regulation of translation initiation factors -4E and -iso4E during maize germination. Physiologia Plantarum 107, 419–425.CrossRefGoogle Scholar
Dinkova, T.D., Reyes de la Cruz, H., Garcia-Flores, C., Aguilar, R., Jimenez-Garcia, L.F. and Sanchez de Jimenez, E. (2007) Dissecting the TOR-S6K signal transduction pathway in maize seedlings: relevance on cell growth regulation. Physiologia Plantarum 130, 1–10.CrossRefGoogle Scholar
Duprat, A., Caranta, C., Revers, F., Menand, B., Browning, K.S. and Robaglia, C. (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. The Plant Journal 32, 927–934.CrossRefGoogle ScholarPubMed
Fischer, P.M. (2009) Cap in hand: targeting eIF4E. Cell Cycle 8, 2535–2541.CrossRefGoogle ScholarPubMed
Freire, M.A. (2005) Translation initiation factor (iso) 4E interacts with BTF3, the beta subunit of the nascent polypeptide-associated complex. Gene 345, 271–277.CrossRefGoogle ScholarPubMed
Freire, M.A., Tourneur, C., Granier, F., Camonis, J., El Amrani, A., Browning, K.S. and Robaglia, C. (2000) Plant lipoxygenase 2 is a translation initiation factor-4E-binding protein. Plant Molecular Biology 44, 129–140.CrossRefGoogle ScholarPubMed
Holdsworth, M.J., Finch-Savage, W.E., Grappin, P. and Job, D. (2008) Post-genomics dissection of seed dormancy and germination. Trends in Plant Science 13, 7–13.CrossRefGoogle ScholarPubMed
Hubbard, K.E., Nishimura, N., Hitomi, K., Getzoff, E.D. and Schroeder, J.I. (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes and Development 24, 1695–1708.CrossRefGoogle ScholarPubMed
Lellis, A.D., Allen, M.L., Aertker, A.W., Tran, J.K., Hillis, D.M., Harbin, C.M., Caldwell, C., Gallie, D.R. and Browning, K.S. (2010) Deletion of the eIFiso4G subunit of the Arabidopsis eIFiso4F translation initiation complex impairs health and viability. Plant Molecular Biology 74, 249–263.CrossRefGoogle ScholarPubMed
Mayberry, L.K., Allen, M.L., Dennis, M.D. and Browning, K.S. (2009) Evidence for variation in the optimal translation initiation complex: plant eIF4B, eIF4F and eIF(iso)4F differentially promote translation of mRNAs. Plant Physiology 150, 1844–1854.CrossRefGoogle ScholarPubMed
O'Farrell, P.H. (1975) High resolution two-dimensional electrophoresis of proteins. Journal of Biological Chemistry 250, 4007–4021.CrossRefGoogle ScholarPubMed
Pause, A., Belsham, G.J., Gingras, A.C., Donze, O., Lin, T.A., Lawrence, J.C. Jr and Sonenberg, N. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature 371, 762–767.CrossRefGoogle Scholar
Pestova, T.V., Lorsch, J.R. and Hellen, C.U. (2007) The mechanism of translation initiation in eukaryotes. pp. 87–128 in Mathews, M.B.; Sonenberg, N.; Hershey, J.W.B. (Eds) Translational control in biology and medicine. Cold Spring Harbor, New York, CSHL Press.Google Scholar
Rhoads, R.E. (2009) eIF4E: new family members, new binding partners, new roles. Journal of Biological Chemistry 284, 16711–16715.CrossRefGoogle ScholarPubMed
Robaglia, C. and Caranta, C. (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends in Plant Science 11, 40–45.CrossRefGoogle ScholarPubMed
Rodriguez, C.M., Freire, M.A., Camilleri, C. and Robaglia, C. (1998) The Arabidopsis thaliana cDNAs coding for eIF4E and eIF(iso)4E are not functionally equivalent for yeast complementation and are differentially expressed during plant development. The Plant Journal 13, 465–473.CrossRefGoogle Scholar
Sanchez de Jimenez, E. and Aguilar, R. (1984) Protein synthesis patterns: relevance of old and new messenger RNA in germinating maize embryos. Plant Physiology 75, 231–234.CrossRefGoogle Scholar
Sonenberg, N. and Hinnebusch, A.G. (2007) New modes of translational control in development, behavior, and disease. Molecular Cell 28, 721–729.CrossRefGoogle ScholarPubMed
Van Der Kelen, K., Beyaert, R., Inze, D. and De Veylder, L. (2009) Translational control of eukaryotic gene expression. Critical Reviews in Biochemistry and Molecular Biology 44, 143–168.CrossRefGoogle ScholarPubMed
Volpon, L., Osborne, M.J., Capul, A.A., de la Torre, J.C. and Borden, K.L. (2010) Structural characterization of the Z RING-eIF4E complex reveals a distinct mode of control for eIF4E. Proceedings of the National Academy of Sciences, USA 107, 5441–5446.CrossRefGoogle ScholarPubMed