Skip to main content
SpringerLink
Log in

Primary structure of the photosynthetic pyruvate orthophosphate dikinase of the C3 plant Flaveria pringlei and expression analysis of pyruvate orthophosphate dikinase sequences in C3, C3–C4 and C4 Flaveria species

  • Short Communication
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

We have isolated full-size cDNA sequences encoding the photosynthetic isoform of pyruvate orthophosphate dikinase (PPDK) of the C3 plant Flaveria pringlei. The encoded protein shares 96% identical amino acid residues with the C4 isoform of PPDK in the C4 species F. trinervia. The differing amino acid residues are evenly distributed along the polypeptide chain. Genomic Southern analysis of photosynthetic PPDK sequences in F. pringlei (C3), F. chloraefolia (C3–C4), F. linearis (C3–C4), F. floridana (C3–C4), F. brownii (C4-like) and F. trinervia (C4) reveals a simple hybridization pattern which is suggestive of a single gene. Northern hybridization experiments show that the abundance of PPDK transcripts in leaves correlates with the degree of C4 characteristics expressed in the various photosynthetic types analysed. This finding demonstrates that the increase in expression levels must have played a crucial role in evolving the C4-PPDK gene in the genus Flaveria.

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

References

  1. Aoyagi K, Bassham JA: Pyruvate orthophosphate dikinase in wheat leaves. Plant Physiol 73: 853–854 (1983).

    Google Scholar 

  2. Aoyagi K, Nakamoto H: Pyruvate, Pi dikinase in bundle sheath strands as well as in mesophyll cells in maize leaves. Plant Physiol 78: 661–664 (1985).

    Google Scholar 

  3. Budde RJA, Chollet R: Regulation of enzyme activity in plants by reversible phosphorylation. Physiol Plant 72: 435–439 (1988).

    Google Scholar 

  4. Burnell JM, Hatch MD: Light-dark modulation of leaf pyruvate,Pi dikinase. Trends Biochem Sci 10: 288–291 (1985).

    Article  Google Scholar 

  5. Carroll LJ, Xu Y, Thrall SH, Martin BM, Dunaway-Mariano D: Substrate binding domains in pyruvate phosphate dikinase. Biochemistry 33: 1134–1142 (1994).

    PubMed  Google Scholar 

  6. Church GM, Gilbert W: Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995 (1984).

    PubMed  Google Scholar 

  7. Edwards GE, Ku MSB. Biochemistry of C3–C4 intermediates. In: Hatch MD, Boardman NK (eds) The Biochemistry of Plants, vol. 10, pp. 275–325. Academic Press, New York (1987).

    Google Scholar 

  8. Glackin CA, Grula JW: Organ-specific transcripts of different size and abundance derive from the same pyruvate, orthophosphate dikinase gene in maize. Proc Natl Acad Sci USA 87: 3004–3008 (1990).

    PubMed  Google Scholar 

  9. Hatch MD, Osmond CB: Compartmentation and transport in C4 photosynthesis. In: Stocking CR, Heber U (eds) Transport in Plants. III. Intracellular Interactions and Transport Processes. Encyclopedia of Plant Physiology, vol. 3, pp. 144–184. Springer-Verlag, Berlin (1976).

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  11. Hermans J, Westhoff P: Analysis of expression and evolutionary relationships of phosphoenolpyruvate carboxylase genes in Flaveria trinervia (C4) and F. pringlei (C3). Mol Gen Genet 224: 459–468 (1990).

    Article  PubMed  Google Scholar 

  12. Hermans J, Westhoff P: Homologous genes for the C4 isoform of phosphoenolpyruvate carboxylase in a C3-and a C4 Flaveria species. Mol Gen Genet 234: 275–284 (1992).

    Article  PubMed  Google Scholar 

  13. Higgins DG, Bleasby AJ, Fuchs R: Clustal V: improved software for multiple sequence alignment. Comput Appl Biosci 8: 189–191 (1992).

    PubMed  Google Scholar 

  14. Höfer MU, Santore UJ, Westhoff P: Differential accumulation of the 10-, 16- and 23-kDa peripheral components of the water-splitting complex of photosystem II in mesophyll and bundle-sheath chloroplasts of the dicotyledonous C4 plant Flaveria trinervia (Spreng.) C. Mohr. Planta 186: 304–312 (1992).

    Google Scholar 

  15. Ku MSB, Wu J, Dai Z, Scott RA, Chu C, Edwards GE: Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiol 96: 518–528 (1991).

    Google Scholar 

  16. Lipka B, Steinmüller K, Börsch D, Rosche E, Westhoff P: The photosynthetic isoform of the NADP-malic enzyme of the C3 plant Flaveria pringlei is a chloroplastic enzyme and orthologous to the C4 isoform of the C4 plant F. trinervia. Plant Mol Biol, submitted.

  17. Matsuoka M: Structure, genetic mapping, and expression of the gene for pyruvate, orthophosphate dikinase from maize. J Biol Chem 265: 16772–16777 (1990).

    PubMed  Google Scholar 

  18. Matsuoka M, Ozeki Y, Yamamoto N, Hirano H, Kano-Murakami Y, Tanaka Y: Primary structure of maize pyruvate,orthophosphate dikinase as deduced from cDNA sequence. J Biol Chem 263: 11080–11083 (1988).

    PubMed  Google Scholar 

  19. Meyer AO, Kelly GJ, Latzko E: Pyruvate orthophosphate dikinase from the immature grains of cereal grasses. Plant Physiol 69: 7–10 (1982).

    Google Scholar 

  20. Monson RK, Moore Bd: On the significance of C3–C4 intermediate photosynthesis to the evolution of C4 photosynthesis. Plant Cell Environ 12: 689–699 (1989).

    Google Scholar 

  21. Oswald A, Streubel M, Ljungberg U, Hermans J, Eskins K, Westhoff P: Differential biogenesis of photosystem II in mesophyll and bundle sheath cells of NADP malic enzyme-type C4 plants. A comparative protein and RNA analysis. Eur J Biochem 190: 185–194 (1990).

    PubMed  Google Scholar 

  22. Pocalyko DJ, Carroll LJ, Martin BM, Babbitt PC, Dunaway-Mariano D: Analysis of sequence homologies in plant and bacterial pyruvate phosphate dikinase, enzyme I of the bacterial phosphoenolpyruvate: sugar phosphotransferase system and other PEP-utilizing enzymes. Identification of potential catalytic and regulatory motifs. Biochemistry 29: 10757–10765 (1990).

    PubMed  Google Scholar 

  23. Poetsch W, Hermans J, Westhoff P: Multiple cDNAs of phosphoenolpyruvate carboxylase in the C4 dicot Flaveria trinervia. FEBS Lett 292: 133–136 (1991).

    Article  PubMed  Google Scholar 

  24. Powell AM: Systematics of Flaveria (Flaveriinae-Asteraceae). Ann Missouri Bot Gard 65: 590–636 (1978).

    Google Scholar 

  25. Rajeevan MS, Bassett CL, Hughes DW: 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 Biol 17: 371–383 (1991).

    PubMed  Google Scholar 

  26. Rosche E, Westhoff P: Primary structure of pyruvate, orthophosphate dikinase in the dicotyledonous C4 plant Flaveria trinervia. FEBS Lett 273: 116–121 (1990).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  29. Westhoff P, Offermann-Steinhard K, Höfer M, Eskins K, Oswald A, Streubel M: Differential accumulation of plastid transcripts encoding photosystem II components in the mesophyll and bundle-sheath cells of monocotyledonous NADP-malic enzyme-type C4 plants. Planta 184: 377–388 (1991).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institut für Entwicklungs- und Molekularbiologie der Pflanzen, Heinrich-Heine-Universität Düsseldorf, D-40225, Düsseldorf, Germany

    Elke Rosche, Monika Streubel & Peter Westhoff

Authors
  1. Elke Rosche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika Streubel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter Westhoff
    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

Rosche, E., Streubel, M. & Westhoff, P. Primary structure of the photosynthetic pyruvate orthophosphate dikinase of the C3 plant Flaveria pringlei and expression analysis of pyruvate orthophosphate dikinase sequences in C3, C3–C4 and C4 Flaveria species. Plant Mol Biol 26, 763–769 (1994). https://doi.org/10.1007/BF00013761

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00013761

Key words

Search

Navigation