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Temporal and tissue-specific expression of the tobacco ntf4 MAP kinase

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Abstract

The large number of mitogen-activated protein (MAP) kinase genes identified to date in plants suggests that their encoded proteins have a wide array of functions in development and physiological responses, as has been indicated by studies on the factors which lead to the activation of these kinases. Signalling pathways involving members of a multigene family employ a variety of mechanisms to ensure response specificity, one of which is via differential gene expression. We have performed detailed analyses of the expression of the tobacco ntf4 MAP kinase gene using a variety of approaches. The ntf4 gene promoter region was isolated and a chimeric ntf4 promoter-GUS fusion construct was introduced into plants. GUS expression was detected in pollen, in developing and mature embryos, and shortly after seed germination, but not in other floral tissues and tissues such as leaf, root, or stem. This expression pattern was confirmed by northern and western analyses. In situ hybridization and immunolocalization studies showed that the expression of the ntf4 gene and its encoded protein p45Ntf4 occurred in embryos at least from the globular embryo stage until the mature seed, as well as in the seed endosperm. Taken together, the results show that the p45Ntf4 MAP kinase has a very restricted expression pattern, being found only in pollen and seeds. These findings should be important when considering MAP kinase function in plants.

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References

  • Albani, D., Robert, L.S., Donaldson, P.A., Altosaar, I., Arnison, P.G. and Fabijanski, S.F. 1990. Characterization of a pollen-specific gene family from Brassica napus which is activated during early microspore development. Plant Mol. Biol. 15: 605–622.

    Google Scholar 

  • Baskin, T.I., Busby, C.H., Fowke, L.C., Sammut, M. and Gubler, F. 1992. Improvements in immunostaining samples embedded in methacrylate: localization of microtubules and other antigens throughout developing organs in plants of diverse taxa. Planta 187: 405–413.

    Google Scholar 

  • Decroocq-Ferrant, V., Decroocq, S., VanWent, J., Schmidt, E. and Kreis, M. 1995. A homologue of the MAP/ERK family of protein kinases is expressed in vegetative and in female reproductive organs of Petunia hybrida. Plant Mol. Biol. 27: 339–350.

    Google Scholar 

  • Dornelas, M.C., Wittich, P., von Recklinghausen, I., van Lammeren, A.A.M. and Kreis, M. 1999. Characterization of three novel members of the Arabidopsis SHAGGY-related protein kinase (ASK) multigene family. Plant Mol. Biol. 39: 137–147.

    Google Scholar 

  • Durbin, M.L., McCaig, B. and Clegg, M.T. 2000. Molecular evolution of the chalcone synthase multigene family in the morning glory genome. Plant Mol. Biol. 42: 79–92.

    Google Scholar 

  • Ellerström, M., Stalberg, K., Ezcurra, I. and Rask, L. 1996. Functional dissection of a napin gene promoter: identification of promoter elements required for embryo and endosperm-specific transcription. Plant Mol. Biol. 32: 1019–1027.

    Google Scholar 

  • Faux, M.C. and Scott, J.D. 1996. More on target with protein phosphorylation: conferring specificity by location. Trends Biochem. Sci. 21: 312–315.

    Google Scholar 

  • Fourgoux-Nicol, A., Drouaud, J., Haouazine, N., Pelletier, G. and Guerche, P. 1999. Isolation of rapeseed genes expressed early and specifically during development of the male gametophyte. Plant Mol. Biol. 40: 857–872.

    Google Scholar 

  • García, F., Zalba, G., Páez, G., Encío, I.. and de Miguel, C. 1998. Molecular cloning and characterization of the human p44 mitogen-activated protein kinase gene. Genomics 50: 69–78.

    Google Scholar 

  • Garrington, T.P. and Johnson, G.L. 1999. Organization and regulation of mitogen-activated protein kinase signalling pathways. Curr. Opin. Cell Biol. 11: 211–218.

    Google Scholar 

  • Gonzalez, F.A., Raden, D.L., Rigby, M.R. and Davis, R.J. 1992. Heterogeneous expression of four MAP kinase isoforms in human tissues. FEBS Lett. 304: 170–178.

    Google Scholar 

  • Grotewold, E., Drummond, B.J., Bowen, B. and Peterson, T. 1994. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76: 543–553.

    Google Scholar 

  • Huttly, A.K. and Phillips, A.L. 1995. Gibberellin-regulated expression in oat aleurone cells of two kinases that show homology to MAP kinase and a ribosomal protein kinase. Plant Mol. Biol. 27: 1043–1052.

    Google Scholar 

  • Jacobs, D., Glossip, D., Xing, H., Muslin, A.J. and Kornfeld, K. 1999. Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev. 13: 163–175.

    Google Scholar 

  • Jefferson, R.A., Kavanagh, T.A. and Bevan M.W. 1987. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901–3907.

    Google Scholar 

  • Jonak, C., Páy, A., Bögre, L., Hirt, H. and Heberle-Bors, E. 1993. The plant homologue of MAP kinase is expressed in a cell cycle-dependent and organ-specific manner. Plant J. 3: 611–617.

    Google Scholar 

  • Jonak, C., Kiegerl, S., Ligterink, W., Barker, P.J., Huskisson, N.S. and Hirt, H. 1996. Stress signalling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc. Natl. Acad. Sci. USA 93: 11274–11279.

    Google Scholar 

  • Joshi, C.P. 1987. An inspection of the domain between putative TATA box and translation start site in 79 plant genes. Nucl. Acids Res. 15: 6643–53.

    Google Scholar 

  • Kranz, H.D., Denekamp, M., Greco, R., Jin, H., Leyva, A., Meissner, R.C., Petroni, K., Urzainqui, A., Beven, M., Martin, C., Smeekens, S., Tonelli, C., Paz-Ares, J. and Weisshaar, B. 1998. Towards functional characterisation of the members of the R2R3–MYB gene family from Arabidopsis thaliana. Plant J. 16: 263–276.

    Google Scholar 

  • Kültz, D. 1998. Phylogenetic and functional classification of mitogen-and stress-activated protein kinases. J. Mol. Evol. 46: 571–588.

    Google Scholar 

  • Lee, S.W., Heinz, R., Robb, J. and Nazar, R.N. 1994. Differential utilization of alternate initiation sites in a plant defense gene responding to environmental stimuli. Eur. J. Biochem. 15: 109–114.

    Google Scholar 

  • Ligterink, W. 2000. MAP kinases in plant signal transduction: how many, and what for? In: H. Hirt (Ed.), MAP Kinases in Plant Signal Transduction. Results and Problems in Cell Differentiation, Vol. 27, Springer-Verlag, Heidelberg, pp. 11–27.

    Google Scholar 

  • Madhani, H.D. and Fink, G.R. 1998. The riddle of MAP kinase signalling specificity. Trends Genet. 14: 151–155.

    Google Scholar 

  • Memelink, J., Hoge, J.H.C. and Schilperoort, R.A. 1987. Cytokinin stress changes the developmental regulation of several defense-related genes in tobacco. EMBO J. 6: 3579–3583.

    Google Scholar 

  • Mizoguchi, T., Irie, K., Hirayama, T., Hayashida, N., Yamaguchi-Shinozaki, K., Matsumoto, K. and Shinozaki, K. 1996. A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold and water stress in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 93: 765–769.

    Google Scholar 

  • Navarro-Avino, J.P., Hentzen, A.E. and Bennett, A.B. 1999. Alternative transcription initiation sites generate two LCA1 Ca 2+-ATPase mRNA transcripts in tomato roots. Plant Mol. Biol. 40: 133–140.

    Google Scholar 

  • Oldenhof, M.T., de Groot, P.F.M., Visser, J.H., Schrauwen, J.A.M. and Wullems G.J. 1996. Isolation and characterization of a microspore-specific gene from tobacco. Plant Mol. Biol. 31: 213–225.

    Google Scholar 

  • Pagès, G., Stanley, E.R., Le Gall, M., Brunet, A. and Pouysséur, J. 1995. The mouse p44 mitogen-activated protein kinase (ex-tracellular signal-regulated kinase 1) gene. J. Biol. Chem. 270: 26986–26992.

    Google Scholar 

  • Pay, A., Jonak, C., Bögre, L., Meskiene, I., Mairinger, T., Szalay, A., Heberle-Bors, E. and Hirt, H. 1993. The MsK family of alfalfa protein kinase genes encodes homologues of shaggy/glycogen synthase kinase-3 and shows differential ex-pression patterns in plant organs and development. Plant J. 3: 847–856.

    Google Scholar 

  • Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D.G. 1999. Rapid Avr9–and Cf-9–dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell 11: 273–287.

    Google Scholar 

  • Seo, S., Sano, H. and Ohashi, Y. 1999. Jasmonate-based wound signal transduction requires activation of WIPK, a tobacco mitogen-activated protein kinase. Plant Cell 11: 289–298.

    Google Scholar 

  • Sieburth, L.E. and Meyerowitz, E.M. 1997. Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell 9: 355–365.

    Google Scholar 

  • Singh, K.B. 1998. Transcriptional regulation in plants: the importance of combinatorial control. Plant Physiol. 118: 1111–1120.

    Google Scholar 

  • Slocombe, S.P., Piffanelli, P., Fairbairn, D., Bowra, S., Hat-zopoulos, P., Tsiantis, M. and Murphy, D.J. 1994. Temporal and tissue-specific regulation of a Brassica napus stearoyl-acyl carrier protein desaturase gene. Plant Physiol. 104: 1167–1176.

    Google Scholar 

  • Stöger, E., Benito Moreno, R.M., Ylstra, B., Vicente, O. and Heberle-Bors E. 1992. Comparison of different techniques for gene transfer into mature and immature tobacco pollen. Transgenic Res. 1: 71–78.

    Google Scholar 

  • Sugiura, N., Suga, T., Ozeki, Y., Mamiya, G. and Takishima, K. 1997. The mouse extracellular signal-regulated kinase 2 gene. J. Biol. Chem. 272: 21575–21581.

    Google Scholar 

  • Takezawa, D. 1999. Elicitor-and A23187–induced expression of WCK-1, a gene encoding mitogen-activated protein kinase in wheat. Plant Mol. Biol. 40: 921–933.

    Google Scholar 

  • Tan, P.B.O. and Kim, S.K. 1999. Signaling specificity: the RTK/RAS/MAP kinase pathway in metazoans. Trends Genet. 15: 145–149.

    Google Scholar 

  • Thomas, S.M. and Brugge, J.S. 1997. Cellular functions regulated by SRC family kinases. Annu. Rev. Cell Dev. Biol. 13: 513–609.

    Google Scholar 

  • Touraev, A. and Heberle-Bors, E. 1999. Microspore embryogenesis and in vitro pollen maturation in tobacco. In: R.D. Hall (Ed.), Plant Cell Culture Protocols, Humana Press, Totowa, NJ, pp. 281–291.

    Google Scholar 

  • van der Geest, A.H.M., Frisch, D.A., Kemp, J.D. and Hall, T.C. 1995. Cell ablation reveals that expression from the phaseolin promoter is confined to embryogenesis and microsporogenesis. Plant Physiol. 109: 1151–1158.

    Google Scholar 

  • Weterings, K., Schrauwen, J., Wullems, G. and Twell, D. 1995. Functional dissection of the promoter of the pollen-specific gene NTP303 reveals a novel pollen-specific, and conserved cis-regulatory element. Plant J. 8: 55–63.

    Google Scholar 

  • Whitmarsh, A.J. and Davis, R.J. 1998. Structural organization of MAP-kinase signalling modules by scaffold proteins in yeast and mammals. Trends Biochem. Sci. 23: 481–485.

    Google Scholar 

  • Wilson, C., Voronin, V., Touraev, A., Vicente, O. and Heberle-Bors, E. 1997. A developmentally regulated MAP kinase activated by hydration in tobacco pollen. Plant Cell 9: 2093–2100.

    Google Scholar 

  • Wilson, C. and Heberle-Bors, E. 2000. MAP kinases in pollen. In: H. Hirt (Ed.), MAP Kinases in Plant Signal Transduction. Results and Problems in Cell Differentiation, Vol. 27, Springer-Verlag, Heidelberg, pp. 39–51.

    Google Scholar 

  • Wittich, P.E., de Heer, R.F., Cheng, X.F., Kieft, H., Colombo, L., Angenent, G.C. and van Lammeren, A.A.M. 1999. Immunolocalization of the petunia floral binding proteins 7 and 11 during seed development in wild-type and expression mutants of Petunia hybrida. Protoplasma 208: 224–229.

    Google Scholar 

  • Zhang, S., and Klessig, D.F. 1997. Salicylic acid activates a 48–kD MAP kinase in tobacco. Plant Cell 9: 809–824.

    Google Scholar 

  • Zhang, S. and Klessig, D.F. 1998a. Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc. Natl. Acad. Sci. USA 95: 7433–7438.

    Google Scholar 

  • Zhang, S. and Klessig, D.F. 1998b. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl. Acad. Sci. USA 95: 7225–7230.

    Google Scholar 

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Authors and Affiliations

  1. Institute of Microbiology and Genetics, University of Vienna, Dr. Bohrgasse 9, 1030, Vienna, Austria

    Viktor Voronin, Alisher Touraev, Erwin Heberle-Bors & Cathal Wilson

  2. Laboratory of Experimental Plant Morphology and Cell Biology, Wageningen University, Arboretumlaan 4, 6703 BD, Wageningen, Netherlands

    Henk Kieft & André A.M. van Lammeren

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  1. Viktor Voronin
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  2. Alisher Touraev
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  4. André A.M. van Lammeren
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  5. Erwin Heberle-Bors
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Voronin, V., Touraev, A., Kieft, H. et al. Temporal and tissue-specific expression of the tobacco ntf4 MAP kinase. Plant Mol Biol 45, 679–689 (2001). https://doi.org/10.1023/A:1010645431133

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