Skip to main content
SpringerLink
Log in

Maize C4 and non-C4 NADP-dependent malic enzymes are encoded by distinct genes derived from a plastid-localized ancestor

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

NADP-dependent malic enzymes (NADP-ME; EC1.1.1.40) have been implicated in a wide range of metabolic pathways in the plastids and cytosol of plant cells. In maize, an NADP-ME type C4 plant, the most abundant NADP-ME form is the chloroplastic leaf isoform that delivers CO2 intracellularly to ribulose bisphosphate carboxylase (RuBPCase). A second NADP-ME isoform predominates in maize roots and exhibits distinct C3-like enzymatic characteristics. We show that the C3-like isoform is encoded by a pair of nearly identical genes that encode precursor proteins with functional chloroplast transit peptides. Using RT-PCR, we also show that the messages encoding the C4 and C3-like NADP-ME isoforms are differentially regulated with respect to the developmental stage of the leaf, light conditions, and tissue type. Based on these characteristics and on sequence comparison of ME families in other species, we propose a scheme for the origin of the C4-specific NADP-ME gene.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson, E. 1945. What is Zea mays? A report on progress. Chron. Bot. 9: 88–92.

    Google Scholar 

  • Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering Arabidopsis thaliana. Nature 408: 796–815.

    Google Scholar 

  • Bansel, K.C., Viret, J.-F., Haley, J., Khan, B.M., Schantz, R. and Bogorad, L. 1992. Transient expression from cab-ml and rbcSm3 promoter sequences is different in mesophyll and bundle sheath cells in maize leaves. Proc. Natl. Acad. Sci. USA 89: 3654–3658.

    Google Scholar 

  • Börsch, D. and Westhoff, P. 1990. Primary Structure of NADPdependent malic enzyme in the dicotyledonous C4 plant Flaveria trinervia. FEBS Lett. 273: 111–115.

    Google Scholar 

  • Bruce, B., Perry, S., Froehlich, J. and Keegstra, K. 1994. In vitro import of proteins into chloroplasts. In Plant Molecular Biology Manual, 2nd ed. Vol J1, Kluwer Acadamic Publishers, Boston MA: p1–15.

    Google Scholar 

  • Casati, P., Drincovich, M.F., Andreo, C.S., Donahue, R. and Edwards, G.E. 1998. UV-B, red and far-red light regulate induction of the C4 isoform of NADP-malic enzyme from wheat. Aust. J. Plant Physiol. 25: 701–708.

    Google Scholar 

  • Casati, P., Drincovich, M., Edwards, G. and Andreo, C.S. 1999a. Malate metabolism by NADP-malic enzyme in plant defense. Photosynth. Res. 61: 99–105.

    Google Scholar 

  • Casati, P., Fresco, A.G., Andreo, C.S. and Drincovich, M.F. 1999b. An intermediate form of NADP-malic enzyme from the C3 C4 intermediate species Flaveria floridana. Plant Sci. 147: 101–109.

    Google Scholar 

  • Chang, K. and Roberts, J. 1989. Observation of cytoplasmic and vacoular malate in maize root tips by 13C-NMR spectroscopy. Plant Physiol. 89: 197–203.

    Google Scholar 

  • Chang, K. and Roberts, J. 1991. Cytoplasmic malate levels in maize root tips during K+ ion uptake determined by 13C-NMR spectroscopy. Biochem. Biophys. Acta 1092: 29–34.

    Google Scholar 

  • Cockburn, W. 1983. Stomatal mechanism as the basis of the evolution of CAM and C4 photosynthesis. Plant Cell & Environ. 6: 275–279.

    Google Scholar 

  • Collins, P.D. and Hague, D.R. 1983. Light-stimulated syntheis of NADP-malic enzymes in leaves of maize. J Biol Chem 258: 4012–4018.

    Google Scholar 

  • Das, O.P., Cruz-Alvarez, M., Chaudhuri, S. and Messing, J. 1990. Molecular methods for genetic analysis of maize. Meth. Mol. Cell Biol. 1: 213–222.

    Google Scholar 

  • Drincovich, M.F., Iglesisa, A.A. and Andreo, C.S. 1991. Interaction of divalent metal ions with the NADP-malic enzyme from maize leaves. Physiol. Plant 81: 462–466.

    Google Scholar 

  • Drincovich, M.F., Spampinato, C.P. and Andreo, C.S. 1992. Evidence for the existence of two essential and proximal cysteinyl residues in NADP-malic enzyme from maize leaves. Plant Physiol. 100: 2035–2040.

    Google Scholar 

  • Drincovich, M.F., Casati, P., Andreo, C.S., Chessin, S.J., Franceschi, V.R., Edwards, G.E. and Ku, M.S.B. 1998a. Evolution of C4 photosynthesis in Flaveria species: isoforms of NADP-malic enzyme. Plant Physiol. 117: 733–744.

    Google Scholar 

  • Drincovich, M.F., Casati, P., Andreo, C.S., Donahue, R. and Edwards, G.E. 1998b. UV-B induction of NADP-malic enzyme in etiolated and green maize seedlings. Plant Cell Environ. 21: 63–70.

    Google Scholar 

  • Drincovich, M.F., Casati, P. and Andreo, C.S. 2001. NADP-malic enzyme from plants: a ubiquitous enzyme involved in different metabolic pathways. FEBS Lett. 490: 1–6.

    Google Scholar 

  • Edwards, G.E. and Andreo, C.S. 1992. NADP-malic enzyme from plants. Phytochemistry 31: 1845–1857.

    Google Scholar 

  • El-Shora, H.M. and Ap Rees, T. 1991. Intracellular location of NADP+-linked malic enzymes in C3-plants. Planta 185: 362–367.

    Google Scholar 

  • Emanuelsson, O., Nielsen, H. and von Heijne, G. 1999. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Science 8: 978–84.

    Google Scholar 

  • Feinberg, A.P. and Vogelstein, B. 1984. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity: addendum. Anal. Biochem. 137: 266–267.

    Google Scholar 

  • Fushimi, T., Umeda, M., Shimazaki, T., Kato, A., Toriyama, K. and Uchimiya, H. 1994. Plant Mol. Biol. 24: 965–967.

    Google Scholar 

  • Gaut, B.S. and Doebly, J.F. 1997. DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl. Acad. Sci. USA 94: 6809–6814.

    Google Scholar 

  • Gavel, Y. and von Heijne, G. 1990. A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett. 261: 455–458.

    Google Scholar 

  • Goodman, M.M., Stuber, C.W., Newton, K. and Weissinger, H.H. 1980. Linkage relationships of 19 enzyme loci in maize. Genetics 96: 697–710.

    Google Scholar 

  • Gottlieb, L.D. 1982. Conversion and duplication of isozymes in plants. Science 216: 373–380.

    Google Scholar 

  • Helentajris, T., Weber, T. and Wright, D. 1988. Identification of the genomic locations of duplicate nucleotide sequences in maize by analysis of restriction fragment length polymorphisms. Genetics 118: 353–363.

    Google Scholar 

  • Hunt, A.G. 1994. Messenger RNA 3' end formation in plants. Ann Rev Plant Physiol Plant Mol. Biol. 45: 47–60.

    Google Scholar 

  • Jacobson, A. 1987. Purification and fractionation of Poly (A)+ RNA. Guide to Molecular Cloning Techniques. Berger, S.L. and Kimmel, A.R. San Diego, Academic Press: 254–261.

    Google Scholar 

  • Jones, S. and Schofield, J. 1990. A rapid method for isolating high quality plasmid DNA suitable for DNA sequencing. Nucl. Acids Res. 18: 7463–7464.

    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: 6643–6652.

    Google Scholar 

  • Kang, F. and Rawsthorne, S. 1994. Starch and fatty acid synthesis in plastids from developing embryos of oil seed rape (Brassica napis L.). Plant J. 6: 795–805.

    Google Scholar 

  • Kausch, A.P., Owen, T.P., Zachwieja, S.J., Flynn, A.R. and Sheen, J. 2001. Mesophyll-specific, light, and metabolic regulation of the C(4)PPCZm1 promoter in transgenic maize. Plant Mol. Biol. 45: 1–15.

    Google Scholar 

  • Kirby, E.A. and Knight, A.H. 1977. Influence of the level of nitrate nutrition on ion uptake and assimilation, organic acid accumulation, and cation-anion balance in whole tomato plants. Physiol. Plant 60: 349–353.

    Google Scholar 

  • Kozak, M. 1984. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nuc. Acids Res. 12: 856–871.

    Google Scholar 

  • Ku, M.S.B., Kamo-Mueakami, Y. and Matsuoka, M. 1996. Evolution and expression of C4 photosynthesis genes. Plant Physiol. 111: 949–957.

    Google Scholar 

  • Lai, L.B., Tausta, S.L. and Nelson, T. 2002a. Differential regulation of transcripts encoding cytosolic NADP-malic enzyme in C3 and C4 Flaveria species. Plant Physiol. 128: 140–149.

    Google Scholar 

  • Lai, L.B., Wang, L. and Nelson, T. 2002b. Distinct but conserved functions for two chloroplastic NADP-malic enzyme isoforms in C3 and C4 Flaveria species. Plant Physiol. 128: 125–139.

    Google Scholar 

  • Langdale, J.A., Rothermal, B.A. and Nelson, T. 1988a. Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes and Dev. 2: 106–115.

    Google Scholar 

  • Langdale, J.A., Zeltich, I., Miller, E. and Nelson, T. 1988b. Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J 7: 3643–3651.

    Google Scholar 

  • Lipka, B., Steinmuller, K., Rosche, E., Borsch, D. and Westhoff, P. 1994. The C3 plant Flaveria pringlei contains a plastidic NADP651 malic enzyme which is orthologous to the C4 isoform of the C4 plant F. trinervia. Plant Mol. Biol. 26: 1775–1783.

    Google Scholar 

  • Llaca, V. and Messing, J. 1998. Amplifications of maize zein genes are conserved within genic but expanded and constricted in intergenic regions. Plant J. 15: 211–220.

    Google Scholar 

  • Lopez-Becerra, E., Puigdomenech, P. and Stiefel, V. 1998. A gene coding for a malic enzyme expressed in the embryo root epidermis from Zea mays. Plant Physiol. 117: 332.

    Google Scholar 

  • Margulis, L. 1981. Symbiosis in cell evolution. W.H. Freeman and Comp. 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.

    Google Scholar 

  • Martinoia, E. and Rentsch, D. 1994. Malate compartmentation: responses to a complex metabolism. Ann. Rev. Plant Physiol. Plant Mol. Biol. 45: 447–467.

    Google Scholar 

  • Matsuoka, M. 1995. The gene for pyruvate, orthophosphate dikinase in C4 plants: structure, regulation and evolution. Plant and Cell Phys. 36: 937–943.

    Google Scholar 

  • Maurino, V.G., Drincovich, M.F. and Andreo, C.S. 1996. Related NADP-malic enzyme isoforms in maize leaves. Biochem. Mol. Biol. Int. 38: 239–250.

    Google Scholar 

  • Maurino, V.G., Drincovich, M.S., Casati, P., Andreo, C.S., Ku, M.S.B., Gupta, S.K., Edwards, G.E. and Franceschi, V.R. 1997. NADP-malic enzyme: immunolocalization in different tissues of the C4 plant maize and the C3 plant wheat. J. Exp. Bot. 48: 799–811.

    Google Scholar 

  • Maurino, V.G., Saigo, M., Andreo, C.S. and Drincovich, M. 2001. Non-photosynthetic 'malic enzyme' from maize: a constituvely expressed enzyme that responds to plant defence inducers. Plant Mol. Bio. 45: 409–420.

    Google Scholar 

  • Metzler, M.C., Rothermal, B. and Nelson, T. 1989. Maize NADPmalate dehydrogenase complementary cDNA cloning sequence and messenger RNA characterization. Plant Mol. Biol. 12: 713–722.

    Google Scholar 

  • Monson, R.K. 1999. The origins of C4 genes and evolutionary pattern in the C4 metabolic phenotype, in C4 Plant Biology. Sage, R. and Monson, R.K. San Diego, Academic Press: 377–404.

    Google Scholar 

  • Moore, B.D., Cheng, S.-H. and Edwards, G. 1986. The influence of leaf development on the expression of C4 metabolism in Flaveria trinervia, a C4 dicot. Plant and Cell Phys. 27: 1159–1167.

    Google Scholar 

  • Moore, B.D. and Edwards, G.E. 1988. The influence of leaf age on photosynthesis and the accumulation of inorganic carbon in Flaveria trinervia, a C4 dicot. Plant Phys. 88: 125–130.

    Google Scholar 

  • Moore, P.D. 1982. Evolution of photosynthetic pathways in flowering plants. Nature 295: 647–648.

    Google Scholar 

  • Nakai, K. and Kanehisa, M. 1992. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14: 897–911.

    Google Scholar 

  • Nishikido, T. and Wada, T. 1974. Comparative studies of NADPmalic enzyme from C4 and C3 plants. Biochim. Biophys. Acta 167: 239–249.

    Google Scholar 

  • Pickett, F.B. and Meeks-Wagner, D.R. 1995. Seeing double: appreciating genetic redundancy. Plant Cell 7: 1347–1356.

    Google Scholar 

  • Preiss, M., Koopman, E., Meye, R.G., Koyro, H.-W. and Schultz, G. 1994. Malate as additional substrate for fatty acid synthesis in a C4-plant type developed by salt stress from a C3 plant type maize: a screening for malate as substrate for fatty acid synthesis in chloroplasts. J. Plant Physiol. 143: 544–549.

    Google Scholar 

  • Pry, T.A. and Hsu, R.Y. 1980. Equilibrium substrate binding studies of the malic enzyme of pigeon liver. Equivalence of nucleotide sites and anticooperativity associated with the binding of L-malate to the enzyme-manganese (II) reduced nicotinamide adenine dinucleotide phosphate ternary complex. Biochemistry 19: 951–962.

    Google Scholar 

  • Pupillo, P. and Bossi, P. 1979. Two forms of NADP-dependent malic enzyme in expanding maize leaves. Planta 144: 283–289.

    Google Scholar 

  • Rajeevan, M.S., Bassett, C.L. and Hughes, D.W. 1991. Isolation and characterization of cDNA clones for NADP-malic enzyme from leaves of Flaveria: transcript abundance distinguishes C3, C3-C4 and C4 photosynthetic types. Plant Mol. Bio. 13: 371–384.

    Google Scholar 

  • Rosche, E., Streubel, M. and Westhoff, P. 1994. Primary structure of the photosynthetic pyruvate orthophoshate dikinase of the C3 plant Flaveria pringlei and expression analysis of pyruvate orthophoshate dikinase sequences in C3, C3-C4 and C4 Flaveria species. Plant Mol. Bio. 26: 763–769.

    Google Scholar 

  • Rosche, E. and Westhoff, P. 1995. Genomic structure and expression of the pyruvate orthophosphate dikinase gene of the dicotyledonous C4 plant Flaveria trinervia (Asteraceae). Plant Mol. Bio. 29: 663–678.

    Google Scholar 

  • Rothermel, B.A. 1990. A biochemical and molecular characterization of the structures and regulation of chloroplastic NADPdependent malic enzyme from maize. New Haven, Yale University.

    Google Scholar 

  • Rothermel, B.A. and Nelson, T. 1989. Primary Structure of the maize NADP-dependent malic enzyme. J. Biol. Chem. 264: 19587–19592.

    Google Scholar 

  • Russo, P., Li, W.-Z., Hampsey, D., Zaret, K. and Sherman, F. 1991. Distinct cis-acting signals enhance 3' endpoint formation of CYCI messenger RNA in the yeast Saccharomyces cerevisiae. EMBO 10: 563–572.

    Google Scholar 

  • Scagliarini, S., Pupillo, P. and Valenti, V. 1988. Isoforms of NADPdepending malic enzymes in tissues of the greening maize leaf. J. Exp. Bot. 39: 1109–1119.

    Google Scholar 

  • Schaff, J., Walter, M. and Hess, D. 1995. Primary metabolism in plant defense: regulation of a bean malic enzyme gene promoter in transgenic tobacco by developmental and environmental cues. Plant Physiol. 108: 949–960.

    Google Scholar 

  • Schaffner, A. and Sheen, J. 1992. Maize C4 photosynthesis involves diffenential regulation of phosphoenolpyruvate carboxylase genes. Plant J. 2: 221–232.

    Google Scholar 

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

    Google Scholar 

  • Sheen, J.-Y. 1991. Molecular mechanisms underlying the differential expression of maize pyruvate orthophosphate dikinase genes. Plant Cell 3: 225–245.

    Google Scholar 

  • Sheen, J.-Y. and Bogorad, L. 1985. Differential expression of the ribulose bisphosphate carboxylase large subunit gene in bundle sheath and mesophyll cells of developing maize leaves is influenced by light. Plant Physiol. 79: 1072–1076.

    Google Scholar 

  • Sheen, J.-Y. and Bogorad, L. 1987. Regulation of levels of nuclear transcripts for C4 photosynthesis in bundle sheath and mesophyll cell of maize leaves. Plant Mol. Biol. 8: 227–238.

    Google Scholar 

  • Smeekens, S., Bauerle, C., Hageman, J., Keegstra, K. and Weisbeek, P. 1986. The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell 46: 365–375.

    Google Scholar 

  • Smith, R.G., Gauthier, D.A., Dennis, D.T. and Turpin, D.H. 1992. Malate-dependent and pyruvate-dependent fatty acid synthesis in leukoplastids from developing castor endosperm. Plant Physiol. 98: 1233–1238.

    Google Scholar 

  • Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nuc. Acids Res. 22: 4673–4680.

    Google Scholar 

  • Turgeon, R. 1989. The sink-source transition in leaves. Ann. Rev. Plant Physiol. Plant Mol. Biol. 40: 119–138.

    Google Scholar 

  • von Heijne, G., Steppuhn, J. and Herrmann, R.G. 1989. Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biochem. 180: 535–545.

    Google Scholar 

  • Wedding, R. 1989. Malic enzymes of higher plants: characteristics, regulation and physiological function. Plant Physiol. 90: 367–371.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Yale University New Haven, P.O. Box 208104, CT, 06520-8104, USA

    S. Lorraine Tausta & Timothy Nelson

  2. Connecticut State Forensic Lab Meriden, CT, 06451, USA

    Heather Miller Coyle

  3. Department of Biochemistry University of Texas Southwestern Medical Center Dallas, TX, 75235-9038, USA

    Beverly Rothermel

  4. Department of Molecular Genetics CID-CSIC, Barcelona, Spain 08034

    Virginia Stiefel

Authors
  1. S. Lorraine Tausta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heather Miller Coyle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beverly Rothermel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Virginia Stiefel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Timothy Nelson
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tausta, S.L., Miller Coyle, H., Rothermel, B. et al. Maize C4 and non-C4 NADP-dependent malic enzymes are encoded by distinct genes derived from a plastid-localized ancestor. Plant Mol Biol 50, 635–652 (2002). https://doi.org/10.1023/A:1019998905615

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1019998905615

Search

Navigation