Thanks to visit codestin.com
Credit goes to link.springer.com

Skip to main content
Springer Nature Link
Log in

Chloroplast and cytosolic triosephosphate isomerases from spinach: purification, microsequencing and cDNA cloning of the chloroplast enzyme

  • Research Article
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Chloroplast and cytosolic triosephosphate isomerases from spinach were separated and purified to homogeneity. Both enzymes were partially sequenced by Edman degradation. Using degenerate primers designed against the amino acid sequences, a homologous probe for the chloroplast enzyme was amplified and used to isolate several full-size cDNA clones. Chloroplast triosephosphate isomerase is encoded by a single gene in spinach. Analysis of the chloroplast cDNA sequence in the context of its homologues from eukaryotes and eubacteria reveals that the gene arose through duplication of its pre-existing nuclear counterpart for the cytosolic enzyme during plant evolution.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from £29.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Abbreviations

TPI:

triosephosphate isomerase

PEG:

polyethylene glycol

cp:

plastid

c:

cytosolic

SDS:

sodium dodecyl sulphate

PAGE:

polyacrylamide gel electrophoresis

PVP:

polyvinylpyrrolidone

PCR:

polymerase chain reaction

PGK:

3-phosphoglycerate kinase

References

  1. Alber T, Kawasaki G: Nucleotide sequence of the triose phosphate isomerase gene of Saccharomyces cerevisiae. J Mol Appl Genet 1: 419–434 (1982).

    Google Scholar 

  2. Ansorge W, Sproat BS, Stegemann J, Schwager C: A non-radioactive automated method for DNA sequence determination. J Biochem Biophys Meth 13: 315–323 (1986).

    Google Scholar 

  3. Beisenherz G: Triosephosphate isomerase from calf muscle. Meth Enzymol 1: 387–391 (1955).

    Google Scholar 

  4. Bergmeyer HU: Methods of Enzymatic Analysis, vol. 2. Verlag Chemie, Weinheim (1983).

    Google Scholar 

  5. Bertsch U, Schlicher TB, Schröder I, Soll J: Sequence of mature phosphoglycerate kinase from spinach chloroplasts. Plant Physiol 103: 1449–1450 (1993).

    Google Scholar 

  6. Brinkmann H, Cerff R, Salomon M, Soll J: Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach. Plant Mol Biol 13: 81–94 (1989).

    Google Scholar 

  7. Chen EY, Seeburg PH: Supercoil sequencing: A fast and simple method for sequencing plasmid DNA. DNA 4: 165–170 (1985).

    Google Scholar 

  8. Corran PH, Waley SG: The amino acid sequence of rabbit muscle triose phosphate isomerase. Biochem J 145: 335–344 (1975).

    Google Scholar 

  9. Devereux J, Haeberli P, Smithies O: A comprehensive set of sequence analysis programms for the VAX. Nucl Acids Res 12: 387–395 (1984).

    Google Scholar 

  10. Eckerskorn C, Lottspeich F: Internal amino acid sequence analysis of proteins separated by gel electrophoresis after tryptic digestion in polyacrylamid matrix. Chromatographia 28: 92–94 (1989).

    Google Scholar 

  11. Edman P, Begg G: A protein sequenator. Eur J Biochem 1: 80–91 (1967).

    Google Scholar 

  12. Eikmanns BJ: Identification, sequence analysis and expression of a Corynebacterium glutamicum gene cluster encoding the three glycolytic enzymes glyceraldehydephosphate dehydrogenase, 3-phosphoglycerate kinase and triosephosphate isomerase. J Bact 174: 6076–6086 (1992).

    Google Scholar 

  13. Feinberg AP, Vogelstein B: A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 137: 266–267 (1984).

    Google Scholar 

  14. Fothergill-Gilmore LA, Michels PAM: Evolution of glycolysis. Progr Biophys Mol Biol 59: 105–238 (1993).

    Google Scholar 

  15. Gottlieb LD: Conservation and duplication of isozymes in plants. Science 216: 373–380 (1982).

    Google Scholar 

  16. Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T: Early branchings in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36: 380–388 (1993).

    Google Scholar 

  17. Henikoff S: Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351–359 (1984).

    Google Scholar 

  18. Higgins DH, Sharp PM: Clustal: a package for performing multiple sequence alignment on a microcomputer. Gene 73: 237–244 (1988).

    Google Scholar 

  19. Jansson S, Meyer-Gauen G, Cerff R, Martin W: Nucleotide distribution in gymnosperm nuclear sequences suggests a model for GC-content change in land plant nuclear genomes. J Mol Evol 39: 34–46 (1994).

    Google Scholar 

  20. Kersanach R, Brinkmann H, Liaud M-F, Zhang D-X, Martin W, Cerff R: Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature 367: 387–389 (1994).

    Google Scholar 

  21. Kohl L, Callens M, Wierenga R, Opperdoes F, Michels P: Triosephosphate isomerase from Leishmania mexicana mexicana: cloning and characterization of the gene, overexpression in Escherichia coli and analysis of the protein. Eur J Biochem 220: 331–338 (1994).

    Google Scholar 

  22. Kolb E, Harris JI, Bridgen J: Triose phosphate isomerase from the coelecanth. Biochem J 137: 185–197 (1974).

    Google Scholar 

  23. Köpke-Secundo E, Molnar I, Schnarrenberger C: Isolation and characterization of the cytosolic and chloroplastic 3-phosphoglycerate kinase from spinach leaves. Plant Physiol 93: 40–47 (1990).

    Google Scholar 

  24. Krebbers E, Seurinck J, Herdies L, Cashmore AR, Timko MP: Four genes in two diverged subfamilies encode the ribulose-1,5-bisphosphate carboxylase small subunit polypeptides of Arabidopsis thaliana. Plant Mol Biol 11: 745–759 (1988).

    Google Scholar 

  25. Kurzok HG, Feierabend J: Comparison of a cytosolic and a chloroplast triosephosphate isomerase isoenzyme from rye leaves. I. Purification and catalytic properties. Biochim Biophys Acta 788: 214–221 (1984).

    Google Scholar 

  26. Kurzok HG, Feierabend J: Comparison of a cytosolic and a chloroplast triosephosphate isomerase isoenzyme from rye leaves. II. Molecular properties and phylogenetic relationships. Biochim Biophys Acta 788: 222–233 (1984).

    Google Scholar 

  27. Kurzok HG, Feierabend J: Comparison of the development and site of synthesis of a cytosolic and a chloroplast isoenzyme of triosephosphate isomerase in rye leaves. J Plant Physiol 126: 207–212 (1986).

    Google Scholar 

  28. Maniatis T, Fritsch E, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1989).

    Google Scholar 

  29. Maquat LE, Chilcote R, Ryan PM: Human triosephosphate isomerase cDNA and protein structure: studies of triosephosphate isomerase deficiency in man. J Biol Chem 260: 3748–3753 (1985).

    Google Scholar 

  30. Marchionni M, Gilbert W: The triosephosphate isomerase gene from maize: Introns antedate the plantanimal divergence. Cell 46: 133–141 (1986).

    Google Scholar 

  31. Martin W, Brinkmann H, Savona C, Cerff R: Evidence for a chimaeric nature of nuclear genomes: Eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. Proc Natl Acad Sci USA 90: 8692–8696 (1993).

    Google Scholar 

  32. Martin W, Lagrange T, Li Y-F, Bisanz-Seyer C, Mache R: Hypothesis for the evolutionary origin of the chloroplast ribosomal protein L21 of spinach. Curr Genet 18: 553–556 (1990).

    Google Scholar 

  33. McFadden GI, Gilson PR, Hofmann CJB, Adcock GJ, Maier U-G: Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc Natl Acad Sci USA, in press (1994).

  34. McKnight GL, O'Hara PJ, Parker ML: Nucleotide sequence of the triosephosphate isomerase gene from Aspergillus nidulans: implications for a differential loss of introns. Cell 46: 143–147 (1986).

    Google Scholar 

  35. Morden CW, Golden SS: Sequence analysis and phylogenetic reconstruction of the genes encoding the large and small subunits of ribulose-1,5-bisphosphate carboxylase/oxygenase from the chlorophyll b-containing prokaryote Prochlorothrix hollandica. J Mol Evol 32: 379–395 (1991).

    Google Scholar 

  36. Mowatt MR, Weinbach EC, Howard TC, Nash TE: Complementation of an Escherichia coli glycolysis mutant by Giardia lamblia triosephosphate isomerase. Exp Parasitol 78: 85–92 (1994).

    Google Scholar 

  37. Mo Y, Harris BG, Gracy RW: Triosephosphate isomerases and aldolases from light- and dark-grown Euglena gracilis. Arch Biochem Biophys 57: 580–587 (1973).

    Google Scholar 

  38. Murray NE: Phage lambda and molecular cloning. In: Hendrix RW (ed) Lambda II, pp. 395–432. Cold Spring Harbour Laboratory Press, Cold Spring Harbor, NY (1983).

    Google Scholar 

  39. Okada N, Koizumi N, Tanaka T, Ohkubo H, Nakanishi S, Yamada Y: Isolation, sequence, and bacterial expression of a cDNA for (S)-tetrahydroberberine oxidase from cultured berberine-producing Coptis japonica cells. Proc Natl Acad Sci USA 86: 534–538 (1989).

    Google Scholar 

  40. Ota T, Nei M: Estimation of the number of amino acid substitutions per site when the substitution rate varies among sites. J Mol Evol 38: 642–643 (1994).

    Google Scholar 

  41. Pelzer-Reith B, Penger A, Schnarrenberger C: Plant aldolase: cDNA and deduced amino-acid sequence of the chloroplast and cytosol enzyme from spinach. Plant Mol Biol 21: 331–340 (1993).

    Google Scholar 

  42. Pichersky E, Gottlieb LD, Hess JF: Nucleotide sequence of the triose phosphate isomerase gene of Escherichia coli. Mol Gen Genet 195: 314–320 (1984).

    Google Scholar 

  43. Pichersky E, Gottlieb LD: Plant triose phosphate isomerase isoenzymes: Purification, immunological and structural characterisation and partial amino acid sequences. Plant Physiol 74: 340–347 (1984).

    Google Scholar 

  44. Raines CA, Lloyd JC, Willingham NM, Potts S, Dyer TA: cDNA and gene sequences of wheat chloroplast sedulose-1,7-bisphosphatase reveal homology with fructose-1,6-bisphosphatases. Eur J Biochem 205: 1053–1059 (1992).

    Google Scholar 

  45. Reith M, Munholland J: A high resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell 5: 465–475 (1993).

    Google Scholar 

  46. Roesler KR, Ogren WL: Nucleotide sequence of spinach cDNA encoding phosphoribulokinase. Nucl Acids Res 16: 7192 (1988).

    Google Scholar 

  47. Russell PR: Transcription of the triose-phosphate-isomerase gene of Schizosaccharomyces pombe initiates from a start point different from that in Saccharomyces cerevisiae. Gene 40: 125–130 (1985).

    Google Scholar 

  48. Saitou N, Nei M: The neighbor-joining method: a new method for the reconstruction of phylogenetic trees. Mol Biol Evol 4: 406–425 (1987).

    Google Scholar 

  49. Sanger F, Nicklen S, Coulson AR: DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    Google Scholar 

  50. Schlaepfer BS, Zuber H: Cloning and sequencing of the genes encoding glyceraldehyde-3-phosphate dehydrogenase, phosphoglycerate kinase and triosephosphate isomerase (gap operon) from mesophilic Bacillus megaterium: comparison with corresponding sequences from thermophilic B. Gene 122: 53–63 (1992).

    Google Scholar 

  51. Schnarrenberger C, Jacobshagen S, Müller B, Krüger I: Evolution of isozymes of sugar phosphate metabolism in green algae. In: Isozymes: Structure, Function and Use in Biology and Medicine, pp. 743–764. Wiley-Liss, New York (1990).

    Google Scholar 

  52. Schnarrenberger C, Pelzer-Reith B, Yatsuki H, Freund S, Jacobshagen S, Hori K: Expression and sequence of the only detectable aldolase in Chlamydomonas reinhardtii. Arch Biochem Biophys 313: 173–178 (1994).

    Google Scholar 

  53. Shaw-Lee RL, Lissemore JL, Sullivan DT: Structure and expression of the triose phosphate isomerase (Tpi) gene of Drosophila melanogaster. Mol Gen Genet 230: 225–229 (1991).

    Google Scholar 

  54. Shih M: Cloning and sequencing of a cDNA clone encoding cytosolic triose phosphate isomerase from Arabidopsis thaliana. Plant Physiol 194: 1103–1104 (1994).

    Google Scholar 

  55. Sogin M, Gunderson J, Elwood H, Alonso R, Peattie D: Phylogenetic meaning of the kingdom concept: an unusual Ribosomal RNA from Giardia lamblia. Science 243: 75–77 (1989).

    Google Scholar 

  56. Swinkels BW, Gibson WC, Osinga KA, Kramer R, Veeneman GH, van Boom JH, Borst P: Characterization of the gene for the microbody (glycosomal) triosephosphate isomerase of Trypanosoma brucei. EMBO J 5: 1291–1298 (1986).

    Google Scholar 

  57. Tabor S, Richardson CC: DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci USA 84: 4767–4771 (1987).

    Google Scholar 

  58. Tingey S, Tsai F, Edwards J, Walker E, Coruzzi G: Chloroplast and cytosolic glutamine synthetase are encoded by homologous nuclear genes which are differentially expressed in vivo. J Biol Chem 263: 9651–9657 (1988).

    Google Scholar 

  59. Tittiger C, Whyard S, Walker VK: A novel intron site in the triosephosphate isomerase gene from the mosquito, Culex tarsalis. Nature 361: 470–472 (1993).

    Google Scholar 

  60. Weeden NF: Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 17 133–139 (1981).

    Google Scholar 

  61. Wierenga RK, Noble MEM, Vriend G, Nauche S, Hol WGJ: Refined 1.83 Å structure of trypanosomal triosephosphate isomerase crystallized in the presence of 2.4 M ammonium sulfate. J Mol Biol 220: 995–1015 (1991).

    Google Scholar 

  62. Wolfe KH, Morden CW, Palmer JD: Function and Evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. Proc Natl Acad Sci USA 89: 10648–10652 (1992).

    Google Scholar 

  63. Wolter F, Fritz C, Willmitzer L, Schell J, Schreier P: rbcS genes in Solanum tuberosum: conservation of transit peptide and exon shuffling during evolution. Proc Natl Acad Sci USA 85: 846–850 (1988).

    Google Scholar 

  64. Xu Y, Harris-Haller LW, McCollum JC, Hardin SH, Hall TC: Nuclear gene encoding cytosolic triosephosphate isomerase from rice (Oryza sativa L.). Plant Physiol 102: 697 (1993).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Genetik, Technische Universität Braunschweig, Spielmannstrasse 7, D-38106, Braunschweig, FRG

    Katrin Henze & William Martin

  2. Institut für Pflanzenphysiologie und Mikrobiologie, Freie Universität Berlin, Königin-Luise-Strasse 12-16a, D-14195, Berlin, Germany

    Claus Schnarrenberger

  3. Max Planck Institut für Biochemie, Am Klopferspitz, D-82152, Martinsried, Germany

    Josef Kellermann

Authors
  1. Katrin Henze
    View author publications

    Search author on:PubMed Google Scholar

  2. Claus Schnarrenberger
    View author publications

    Search author on:PubMed Google Scholar

  3. Josef Kellermann
    View author publications

    Search author on:PubMed Google Scholar

  4. William Martin
    View author publications

    Search author on:PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Henze, K., Schnarrenberger, C., Kellermann, J. et al. Chloroplast and cytosolic triosephosphate isomerases from spinach: purification, microsequencing and cDNA cloning of the chloroplast enzyme. Plant Mol Biol 26, 1961–1973 (1994). https://doi.org/10.1007/BF00019506

Download citation

  • Received:

  • Accepted:

  • Issue date:

  • DOI: https://doi.org/10.1007/BF00019506

Key words