Skip to main content
Log in

Quantitative regulation of the Flaveria Me1 gene is controlled by the 3′-untranslated region and sequences near the amino terminus

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The Me1 gene of Flaveria bidentis codes for the C4 isoform of NADP malic enzyme, which accumulates to a high-level only in bundle sheath cells. Previous experiments demonstrated that sequences at the 5′ end of the gene control cell specificity whereas sequences at the 3′ end are necessary for high-level expression. To localize quantitative regulator sequences, we have analysed a series of Me1 3′ deletion constructs fused to the gusA reporter gene. We show that sequences within the 3′-untranslated region (3′-UTR) control quantitative levels of expression. Analysis of 5′ promoter fusions demonstrated that high-level expression also requires sequences within the N-terminal coding region of the gene, suggesting possible interactions between the 3′-UTR and 5′ coding regions. Cell-specific regulatory sequences are located in a different part of the 5′ end of the gene, between 1023 bp upstream of the transcription start and the start of translation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agostino, A., Furbank, R.T. and Hatch, M.D. 1989. Maximizing photosynthetic activity and cell integrity in isolated bundle sheath cell strands from C4 species. Aust. J. Plant Physiol. 16: 279–290.

    Google Scholar 

  • Ali, S. and Taylor, W.C. 2001. The 3′ non-coding region of a C4 photosynthesis gene increases transgene expression when combined with heterologous promoters. Plant Mol. Biol. 6: 325–333.

    Google Scholar 

  • An, G. 1987. Binary Ti vectors for plant transformation and promoter analysis. Meth. Enzymol. 153: 292–305.

    Google Scholar 

  • Berry, J.O., McCormac, D.J., Long, J.J., Boinski, J. and Corey, A.C. 1997. Photosynthetic gene expression in amaranth, an NAD-ME type C4 dicot. Aust. J. Plant Physiol. 24: 423–428.

    Google Scholar 

  • Binder, R., Horowitz, J.A., Basilion, J.P., Koeller, D.M., Klausner, R.D. and Harford, J.B. 1994. Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J. 13: 1969–1980.

    PubMed  Google Scholar 

  • Bodine, D.M., and Ley, T.J. 1987. An enhancer element lies 3′ to the human γ-globin gene. EMBO J. 6: 2997–3004.

    PubMed  Google Scholar 

  • Borsch, D., and Westhoff, P. 1990. Primary structure of NADP-dependent malic enzyme in the dycotyledonous C4 plant Flaveria trinervia. FEBS Lett. 273: 111–115.

    PubMed  Google Scholar 

  • Burgess, D.G. and Taylor, W.C. 1987. Chloroplast photooxidation affects the accumulation of cytosolic mRNAs encoding chloroplast proteins in maize. Planta 170: 520–527.

    Article  Google Scholar 

  • Chen, R., Silver, D.L. and de Bruijn, E.J. 1998. Nodule parenchyma-specific expression of the Sesbania rostrata early nodulation gene SrEnod2 is mediated by 3′-untranslated region. Plant Cell 10: 1585–1602.

    PubMed  Google Scholar 

  • Chitty, J.A., Furbank, R.T., Marshall, J.S., Chen, Z. and Taylor, W.C. 1994. Genetic transformation of the C4 plant, Flaveria bidentis. Plant J. 6: 949–956.

    Google Scholar 

  • Choi, O.R. and Engel, J.D. 1986. A 3′ enhancer is required for temporal and tissue specific transcriptional activation of the chicken adult β-globin gene. Nature 323: 731–734.

    Google Scholar 

  • Daniel, S.G. and Becker, W.M. 1995. Transgenic analysis of the 5′ and 3′ flanking regions of the NADH-dependent hydroxypyruvate reductase gene from Cucumis sativus L. Plant Mol. Biol. 28: 821–836.

    Google Scholar 

  • Dean, C., Favreau, M., Bond-Nutter, D., Bedbrook, J. and Dunsmuir, P. 1989. Sequences downstream of translation start regulate quantitative expression of two petunia RbcS genes. Plant Cell 1: 201–208.

    Article  PubMed  Google Scholar 

  • Dengler, N.G. and Taylor, W.C. 2000. Developmental aspects of C4 photosynthesis. In: R.C. Leegood, T.D. Sharkey and S. von Caemmerer (Eds.) Photosynthesis: Physiology and Metabolism, Kluwer Acdemic Publishers, Dordrecht, Netherlands, pp. 471–495.

    Google Scholar 

  • Dietrich, R.A., Radke, S.E. and Harada, J.J. 1992. Downstream DNA sequences are required to activate a gene expressed in the root cortex of embryos and seedlings. Plant Cell 4: 1371–1382.

    Article  PubMed  Google Scholar 

  • Fagard, M. and Vaucheret, H. 2000. (Trans) gene silencing in plants: how many mechanisms? Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 167–194.

    PubMed  Google Scholar 

  • Fu, H., Kim, S.Y. and Park, W.D. 1995a. High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene requires 5′ and 3′ flanking sequences and the leader intron. Plant Cell 7: 1387–1394.

    PubMed  Google Scholar 

  • Fu, H., Kim, S.Y. and Park, W.D. 1995b. A potato Sus3 sucrose synthase gene contains a context-dependent 3′ element and a leader intron with both positive and negative tissue specific effects. Plant Cell 7: 1395–1403.

    Article  PubMed  Google Scholar 

  • Hatch, M.D. 1987. C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta 895: 81–106.

    Google Scholar 

  • Janssen, B. and Gardner, R.C. 1989. Localised transient expression of GUS in leaf discs following cocultivation with Agrobacterium. Plant Mol. Biol. 14: 61–72.

    Google Scholar 

  • Jefferson, R. 1987. Assaying chimeric genes in plants. The GUS gene fusion system. Plant Mol. Biol. Rep. 5: 387–405.

    Google Scholar 

  • Larkin, J.C., Oppenheimer, D.G., Pollock, S. and Marks, M.D. 1993. Arabidopsis GLABROUS1 gene requires downstream sequences for function. Plant Cell 5: 1739–1748.

    PubMed  Google Scholar 

  • Lauridsen, P., Franssen, H., Stougaard, J., Bisseling, T. and Marker, K.H. 1993. Conserved regulation of soybean early nodulation ENOD2 gene promoter in determinate and indeterminate transgenic root nodules. Plant J. 3: 483–492.

    PubMed  Google Scholar 

  • Long, J.J. and Berry, J.O. 1996. Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria. Plant Physiol. 112: 473–482.

    PubMed  Google Scholar 

  • Marshall, J.S., Stubbs, J.D. and Taylor, W.C. 1996. Two genes encode highly similar chloroplastic NADP-malic enzymes in Flaveria. Plant Physiol. 111: 1251–1261.

    PubMed  Google Scholar 

  • Marshall, J.S., Stubbs, J.D., Chitty, J.A., Surin, B. and Taylor, W.C. 1997. Expression of the C4 Me1 gene from Flaveria bidentis requires an interaction between 5′ and 3′ sequences. Plant Cell 9: 1515–1525.

    PubMed  Google Scholar 

  • Matsuoka, M., Kyozuka, J., Shimamoto, K. and Kano-Murakami, Y. 1994. Promoters of two carboxylases in a C4 plant (maize) direct cell specific, light-regulated expression in a C3 plant (rice). Plant J. 6: 311–319.

    PubMed  Google Scholar 

  • Matsuoka, M. and Numazawa, T. 1991. Cis acting elements in the pyruvate, orthophosphate dikinase gene from maize. Mol. Gen. Genet. 228: 143–152.

    Google Scholar 

  • Matsuoka, M. and Sanada, Y. 1991. Expression of photosynthetic genes from the C4 plant, maize, in tobacco. Mol. Gen. Genet. 225: 411–419.

    Google Scholar 

  • Matsuoka, M., Tada, Y., Fujimura, T. and Kano-Murakami, Y. 1993. Tissue-specific light regulated expression directed by the promoter of a C4 gene, maize pyruvate,orthophosphate dikinase, in a C3 plant, rice. Proc. Natl. Acad. Sci. USA 90: 9586–9590.

    PubMed  Google Scholar 

  • Owen, D. and Kuhn, L.C. 1987. Non-coding 3′ sequences of the transferrin receptor gene are required for mRNA regulation by iron. EMBO J. 6: 1287–1293.

    PubMed  Google Scholar 

  • Ramsperger, V.C., Summers, R.G. and Berry, J.O. 1996. Photosynthetic gene expression in meristems and during initial leaf development in a C4 dicotyledonous plant. Plant Physiol. 111: 999–1010.

    PubMed  Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.

    Google Scholar 

  • Sheen, J. 1999. C4 gene expression. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50: 187–217.

    Google Scholar 

  • Smicun, Y., Kopf, E. and Miskin, R. 1998. The 3′-untranslated region of the urokinase gene enhances the expression of chimeric genes in cultured cells and correlates with specific brain expression in transgenic mice. Eur. J. Biochem. 251: 704–715.

    PubMed  Google Scholar 

  • Stockhaus, J., Poetsch, W., Steinmuller, K. and Westhoff, P. 1994. Evolution of the C4 phosphoenolpyruvate carboxylase promoter of the C4 dicot Flaveria trinervia: an expression analysis in the C3 plant tobacco. Mol. Gen. Genet. 245: 286–293.

    Google Scholar 

  • Stockhaus, J., Schlue, U., Koczor, M., Chitty, J.A., Taylor, W.C. and Westhoff, P. 1997. The promoter of the gene encoding the C4 form of phosphoenolpyruvate carboxylase directs mesophyll-specific expression in trangenic C4 Flaveria spp. Plant Cell 9: 479–489.

    PubMed  Google Scholar 

  • Tarun, S.Z. and Sachs, A.B. 1996. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15: 7168–7177.

    PubMed  Google Scholar 

  • Taylor, W.C., Rosche, E., Marshall, J.S., Ali, S., Chastain, C.J. and Chitty, J.A. 1997. Diverse mechanisms regulate the expression of genes coding C4 enzymes. Aust. J. Plant Physiol. 24: 437–442.

    Google Scholar 

  • Thornburg, R.W., An, G., Cleaveland, T.E., Johnson, R. and Ryan, C.A. 1987. Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyltransferase gene fusion in transgenic potato plants. Proc. Natl. Acad. Sci. USA 84: 744–748.

    Google Scholar 

  • Trainor, C.D., Stamler, S.J. and Engel, J.D. 1987. Erythroid-specific transcription of the chicken histone H5 gene is directed by a 3′ enhancer. Nature 328: 827–830.

    Article  PubMed  Google Scholar 

  • Viret, J.F., Mabrouk, Y. and Bogorad, L. 1994. Transcriptional photoregulation of cell-type-preferred expression of maize rbcS-m3: 3′ and 5′ sequences are involved. Proc. Natl. Acad. Sci. USA 91: 8577–8581.

    PubMed  Google Scholar 

  • Wang, J.L., Klessig, D.F. and Berry, J.O. 1992. Regulation of C4 gene expression in developing amaranth leaves. Plant Cell 4: 173–184.

    Article  PubMed  Google Scholar 

  • Weiss, I.M. and Liebhaber, S.A. 1995. Erythroid cell-specific mRNA stability elements in the α2-globin 3′ nontranslated region. Mol. Cell Biol. 15: 2457–2465.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ali, S., Taylor, W.C. Quantitative regulation of the Flaveria Me1 gene is controlled by the 3′-untranslated region and sequences near the amino terminus. Plant Mol Biol 46, 251–261 (2001). https://doi.org/10.1023/A:1010684509008

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010684509008

Navigation