Skip to main content
SpringerLink
Log in

Regulation of cytosolic pyruvate, orthophosphate dikinase expression in developing maize endosperm

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

Abstract

Pyruvate orthophosphate dikinase (PPDK, E.C. 2.7.9.1) is an abundant enzyme in the leaves of C4 plants associated with the dicarboxylic acid pathways of CO2 fixation in the dark. PPDK activity has also been detected in the seeds of maize and other, non-C4 cereals, where its role has yet to be established. Using an anti-PPDK serum, two cross-reacting species of M r close to 90 000 were detected in developing maize endosperm of wild-type plants. In two independent opaque-2 mutant lines, one of the polypeptides was absent and the other was reduced in level. Similarly, endosperm PPDK mRNA levels were greatly reduced in the opaque-2 maize lines compared to wild type, suggesting that endosperm PPDK gene expression is under Opaque-2 control. However, a low level of PPDK mRNA could still be detected in these mutants, indicating that PPDK gene expression is not absolutely dependent on Opaque-2 but rather can be modulated by it. This interpretation was reinforced by the demonstration that the distribution of PPDK transcripts is not affected in o2 mutants, although the level is reduced, and that PPDK mRNA is detectable prior to 02 mRNA during the maturation of wild-type maize endosperm. Using oligonucleotides specific for the different maize PPDK genes, the o2 mutations were shown to affect only cyPPDKZml gene expression in maize line A69Y.

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

  1. Aoyagi K, Bassham JA: Pyruvate orthophosphate dikinase of C3 seeds and leaves as compared to the enzyme from maize. Plant Physiol 75: 387–392 (1984).

    Google Scholar 

  2. Aoyagi K, Bassham JA: Pyruvate orthophosphate dikinase mRNA organ specificity in wheat and maize. Plant Physiol 76: 278–280 (1984).

    Google Scholar 

  3. Aoyagi K, Bassham JA, Greene FC: Pyruvate orthophosphate dikinase gene expression in developing wheat seeds. Plant Physiol 75: 393–396 (1984).

    Google Scholar 

  4. Balconi C, Rizzi E, Motto M, Salamini F, Thompson R: The accumulation of zein polypeptides and zein mRNA in cultured endosperms of maize is modulated by nitrogen supply. Plant J 3: 325–334 (1993).

    Google Scholar 

  5. Brochetto-Braga MR, Leite A, Arruda P: Partial purification and characterization of lysine-ketoglutarate reductase in normal and opaque-2 maize endosperms. Plant Physiol 98: 1139–1148 (1992).

    Google Scholar 

  6. Budde RIA, Chollet R: Regulation of enzyme activity in plants by reversible phosphorylation. Physiol Planta 72: 435–439 (1988).

    Google Scholar 

  7. Cerff R, Kloppstech K: Structural diversity and differential light control of mRNAs coding for angiosperm glyceraldehyde-3-phosphate dehydrogenase. Proc Natl Acad Sci USA 79: 7624–7628 (1982).

    Google Scholar 

  8. Davies DD: The central role of phosphoenolpyruvate in plant metabolism. Annu Rev Plant Physiol 30: 131–138 (1979).

    Article  Google Scholar 

  9. Gallusci P, Salamini F, Thompson RD: Differences in cell type-specific expression of the gene Opaque-2 in maize and transgenic tobacco. Mol Gen Genet 244: 391–400 (1994).

    PubMed  Google Scholar 

  10. Giroux MJ, Boyer C, Feix G, Hannah LC: Coordinated transcriptional regulation of storage product genes in the maize endosperm. Plant Physiol 106: 713–722 (1994).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  12. Habben JE, Kirleis AW, Larkins BA: The origin of lysine-containing proteins in opaque-2 maize endosperm. Plant Mol Biol 23: 825–838 (1993).

    Article  PubMed  Google Scholar 

  13. Hartings H, Maddaloni M, Lazzaroni N, DiFonzo N, Motto M, Salamini F, Thompson RD: The 02 gene which regulates zein deposition in maize endosperm encodes a protein with structural homologies to transcriptional activators. EMBO J 8: 2795–2801 (1989).

    PubMed  Google Scholar 

  14. Hatch MD, Slack CR: A new enzyme for the interconversion of pyruvate and phosphopyruvate and its role in the C4 dicarboxylic acid pathway of photosynthesis. Biochem J 106: 141 (1968).

    PubMed  Google Scholar 

  15. Hudspeth RL, Glackin CA, Bonner J, Grula JW: Genomic and cDNA clones for maize phosphoenolpyruvate carboxylase and pyruvate orthophosphate dikinase: expression of different gene family members in leaves and roots. Proc Natl Acad Sci USA 83: 2884–2888 (1986).

    Google Scholar 

  16. Hueros G, Varotto S, Salamini F, Thompson RD Molecular characterization of BET1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7: 747–757 (1975).

    Article  Google Scholar 

  17. Kawalleck P, Sommsich IE, Feldbrügge M, Hahlbrock K, Weisshaar B: Polyubiquitin gene expression and structural properties of the ubi4–2 gene in Petroselinum crispum. Plant Mol Biol 21: 673–684 (1993).

    PubMed  Google Scholar 

  18. Lee L, Tsai CY: Effect of sucrose accumulation on zein synthesis in maize starch-deficient mutants. Phytochemistry 24: 225–229 (1985).

    Article  Google Scholar 

  19. Lohmer S, Maddaloni M, Motto M, DiFonzo N, Hartings H, Salamini F, Thompson RD: The maize regulatory locus Opaque-2 encodes a DNA-binding protein which activates the transcription of the b-32 gene. EMBO J 10: 617–624 (1991).

    PubMed  Google Scholar 

  20. Marocco A, Santucci A, Cerioli S, Motto M, DiFonzo N, Thompson R, Salamini F: Three high-lysine mutations control the level of ATP-binding HSP70-like proteins in the maize endosperm. Plant Cell 3: 507–515 (1991).

    Article  PubMed  Google Scholar 

  21. 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 

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

    Article  PubMed  Google Scholar 

  23. Matsuoka M, Tada Y, Fujimura T, Kano-Murakami Y: 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 (1993).

    PubMed  Google Scholar 

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

    Google Scholar 

  25. Motto M, DiFonzo N, Hartings H, Maddaloni M, Salamini F, Soave C, Thompson RD: Regulatory genes affecting maize storage protein synthesis. Oxford Surv Plant Mol Cell Biol 6: 87–114 (1989).

    Google Scholar 

  26. Rechinger KB, Bougri OV, Cameron-Mills V: Evolutionary relationship of the members of the sulphur-rich hordein family revealed by common antigenic determinants. Theor Appl Genet 85: 829–840 (1993).

    Article  Google Scholar 

  27. Schmidt RJ, Ketudat M, Aukerman MJ, Hoschek G: Opaque-2 is a transcriptional activator that recognizes a specific target site in 22-kD zein genes. Plant Cell 4: 689–700 (1992).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  29. Sheen J-Y, Bogorad L: Differential expression of the C4 pathway genes in mesophyll and bundle sheath cells of greening maize leaves. J Biol Chem 262: 11726–11730 (1987).

    PubMed  Google Scholar 

  30. Ueda T, Waverczak W, Ward K, Sher N, Ketudat M, Schmidt RJ, Messing J: Mutations of the 22- and 27-kD zein promoters affect transactivation by the opaque-2 protein. Plant Cell 4: 701–709 (1992).

    Article  PubMed  Google Scholar 

  31. Viotti A, Balducci C, Weil JH: Adaptation of the tRNA population of maize endosperm for zein synthesis. Biochim Biophys Acta 517: 125–132 (1978).

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Philippe Gallusci

    Present address: Laboratoire de Physiologie Cellulaire Végétale, Université de Bordeaux 1, France

Authors and Affiliations

  1. Max-Planck-Institut für Züchtungsforschung, D-50829, Köln, Germany

    Philippe Gallusci, Serena Varotto & Richard D. Thompson

  2. National Institute for Agrobiological Resources, Tsukuba, 305, Ibaraki, Japan

    Makoto Matsuoko

  3. Istituto Sperimentale per la Cerealicoltura, 1-24126, Bergamo, Italy

    Massimo Maddaloni

  4. Bioscience Center, Nagoya University, 464-01, Aichi, Japan

    Makoto Matsuoko

Authors
  1. Philippe Gallusci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Serena Varotto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Makoto Matsuoko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Massimo Maddaloni
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Richard D. Thompson
    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

Gallusci, P., Varotto, S., Matsuoko, M. et al. Regulation of cytosolic pyruvate, orthophosphate dikinase expression in developing maize endosperm. Plant Mol Biol 31, 45–55 (1996). https://doi.org/10.1007/BF00020605

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00020605

Key words

Search

Navigation