Abstract
We have isolated cDNA clones for the maize leaf enzymes phosphoenolpyruvate (P-ePrv) carboxylase [orthophosphate:oxaloacetate carboxy-lyase (phosphorylating) EC 4.1.1.31] and pyruvate,orthophosphate (Prv,Pi) dikinase (ATP:pyruvate,orthophosphate phosphotransferase, EC 2.7.9.1) by exploiting the light-inducibility and large size of the mRNAs (3.5 kilobases) that encode the two enzymes. The clones were identified by hybrid-selection and immunoprecipitation assays. From a maize genomic library, two different types of genomic clones were screened with both the P-ePrv carboxylase and the Prv,Pi dikinase cDNA clones. Information from these genomic clones and genome blots indicates that the P-ePrv carboxylase gene family has at least three members and the Prv,Pi dikinase family at least two. Transcripts for both enzymes were detected in green leaves, etiolated leaves, and roots. The results show that the P-ePrv carboxylase mRNAs in green leaves and roots are encoded by different genes. Whereas the P-ePrv carboxylase mRNAs in all three tissues appear to be the same size, the Prv,Pi dikinase mRNA in green leaves is about 0.5 kilobases longer than the Prv,Pi dikinase mRNAs in etiolated leaves and roots. It is possible that all these Prv,Pi dikinase transcripts are encoded by one gene, and the size differences may correspond to the presence or absence of a sequence encoding a chloroplast transit peptide.
Keywords: photosynthesis, enzymes, light-regulation, tissue specificity
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aoyagi K., Bassham J. A. Pyruvate orthophosphate dikinase mRNA organ specificity in wheat and maize. Plant Physiol. 1984 Sep;76(1):278–280. doi: 10.1104/pp.76.1.278. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aoyagi K., Bassham J. A. Pyruvate orthophosphate dikinase of c(3) seeds and leaves as compared to the enzyme from maize. Plant Physiol. 1984 Jun;75(2):387–392. doi: 10.1104/pp.75.2.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aoyagi K., Bassham J. A. Synthesis and uptake of cytoplasmically synthesized pyruvate, pi dikinase polypeptide by chloroplasts. Plant Physiol. 1985 Aug;78(4):807–811. doi: 10.1104/pp.78.4.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aoyagi K., Nakamoto H. Pyruvate, pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves. Plant Physiol. 1985 Jul;78(3):661–664. doi: 10.1104/pp.78.3.661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baer G. R., Schrader L. E. Stabilization of pyruvate, pi dikinase regulatory protein in maize leaf extracts. Plant Physiol. 1985 Mar;77(3):608–611. doi: 10.1104/pp.77.3.608. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
- Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
- Cullen S. E., Schwartz B. D. An improved method for isolation of H-2 and Ia alloantigens with immunoprecipitation induced by protein A-bearing staphylococci. J Immunol. 1976 Jul;117(1):136–142. [PubMed] [Google Scholar]
- Efstratiadis A., Kafatos F. C., Maxam A. M., Maniatis T. Enzymatic in vitro synthesis of globin genes. Cell. 1976 Feb;7(2):279–288. doi: 10.1016/0092-8674(76)90027-1. [DOI] [PubMed] [Google Scholar]
- Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
- Fujita N., Miwa T., Ishijima S., Izui K., Katsuki H. The primary structure of phosphoenolpyruvate carboxylase of Escherichia coli. Nucleotide sequence of the ppc gene and deduced amino acid sequence. J Biochem. 1984 Apr;95(4):909–916. doi: 10.1093/oxfordjournals.jbchem.a134718. [DOI] [PubMed] [Google Scholar]
- Goldberg R. B., Hoschek G., Tam S. H., Ditta G. S., Breidenbach R. W. Abundance, diversity, and regulation of mRNA sequence sets in soybean embryogenesis. Dev Biol. 1981 Apr 30;83(2):201–217. doi: 10.1016/0012-1606(81)90467-x. [DOI] [PubMed] [Google Scholar]
- Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hague D. R., Sims T. L. Evidence for Light-stimulated Synthesis of Phosphoenolpyruvate Carboxylase in Leaves of Maize. Plant Physiol. 1980 Sep;66(3):505–509. doi: 10.1104/pp.66.3.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hague D. R., Uhler M., Collins P. D. Cloning of cDNA for pyruvate, Pi dikinase from maize leaves. Nucleic Acids Res. 1983 Jul 25;11(14):4853–4865. doi: 10.1093/nar/11.14.4853. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jeffery W. R., Brawerman G. Characterization of the steady-state population of messenger RNA and its poly(adenylic acid) segment in mammalian cells. Biochemistry. 1974 Oct 22;13(22):4633–4637. doi: 10.1021/bi00719a026. [DOI] [PubMed] [Google Scholar]
- Kafatos F. C., Jones C. W., Efstratiadis A. Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res. 1979 Nov 24;7(6):1541–1552. doi: 10.1093/nar/7.6.1541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [DOI] [PubMed] [Google Scholar]
- Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson T., Harpster M. H., Mayfield S. P., Taylor W. C. Light-regulated gene expression during maize leaf development. J Cell Biol. 1984 Feb;98(2):558–564. doi: 10.1083/jcb.98.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Norgard M. V. Rapid and simple removal of contaminating RNA from plasmid DNA without the use of RNase. Anal Biochem. 1981 May 1;113(1):34–42. doi: 10.1016/0003-2697(81)90040-3. [DOI] [PubMed] [Google Scholar]
- O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
- Pitout M. J., Potgieter D. J. The isolation of highly polymerized deoxyribonucleic acid from maize. Biochim Biophys Acta. 1968 Jun 18;161(1):188–196. doi: 10.1016/0005-2787(68)90308-0. [DOI] [PubMed] [Google Scholar]
- Sims T. L., Hague D. R. Light-stimulated increase of translatable mRNA for phosphoenolpyruvate carboxylase in leaves of maize. J Biol Chem. 1981 Aug 25;256(16):8252–8255. [PubMed] [Google Scholar]
- Sugiyama T., Mizuno M., Hayashi M. Partitioning of Nitrogen among Ribulose-1,5-bisphosphate Carboxylase/Oxygenase, Phosphoenolpyruvate Carboxylase, and Pyruvate Orthophosphate Dikinase as Related to Biomass Productivity in Maize Seedlings. Plant Physiol. 1984 Jul;75(3):665–669. doi: 10.1104/pp.75.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugiyama T. Purification, molecular, and catalytic properties of pyruvate phosphate dikinase from the maize leaf. Biochemistry. 1973 Jul 17;12(15):2862–2868. doi: 10.1021/bi00739a014. [DOI] [PubMed] [Google Scholar]
- Ting I. P. CO(2) Metabolism in Corn Roots. III. Inhibition of P-enolpyruvate Carboxylase by l-malate. Plant Physiol. 1968 Dec;43(12):1919–1924. doi: 10.1104/pp.43.12.1919. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uedan K., Sugiyama T. Purification and characterization of phosphoenolpyruvate carboxylase from maize leaves. Plant Physiol. 1976 Jun;57(6):906–910. doi: 10.1104/pp.57.6.906. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Villa-Komaroff L., Efstratiadis A., Broome S., Lomedico P., Tizard R., Naber S. P., Chick W. L., Gilbert W. A bacterial clone synthesizing proinsulin. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3727–3731. doi: 10.1073/pnas.75.8.3727. [DOI] [PMC free article] [PubMed] [Google Scholar]