Skip to main content
SpringerLink
Log in

Characterization of a Sorghum bicolor gene family encoding putative protein kinases with a high similarity to the yeast SNF1 protein kinase

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

C4 photosynthesis is functionally dependent on metabolic interactions between mesophyll and bundle-sheath cells. Although the C4 cycle is biochemically well understood many aspects of the regulation of enzyme activities, gene expression and cell differentiation are elusive.

Protein kinases are likely involved in these regulatory processes providing links to hormonal, metabolic and developmental signal transduction pathways. We have identified several protein kinases that are differentially expressed in mesophyll and bundle-sheath cells of the C4 plant Sorghum bicolor. Here we describe the characterization of two putative protein kinases that show high similarity to the SNF1/AMPK family of protein serine/threonine kinases. The mRNA of both kinases accumulates to much higher levels in mesophyll cells than in the bundle-sheath and can also be detected in root tissue. Complementation experiments with a snf1 mutant of Saccharomyces cerevisiae indicate that the S. bicolor protein kinase SNFL1 does not represent a functional homologue of the yeast SNF1 protein kinase.

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. Aguan K, Scott J, See CG, Sarkar NH: Characterization and chromosomal localization of the human homologue of a rat AMP-activated protein kinase-encoding gene: a major regulator of lipid metabolism in mammals. Gene 149: 345–350 (1994).

    PubMed  Google Scholar 

  2. Alderson A, Sabelli PA, Dickinson JR, Cole D, Richardson M, Kreis M, Shewry PR, Halford NG: Complementation of snfl, a mutation affecting global regulation of carbon metabolism in yeast, by a plant protein kinase cDNA. Proc Natl Acad Sci USA 88: 8602–8605 (1991).

    PubMed  Google Scholar 

  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 215: 403–410 (1990).

    Article  PubMed  Google Scholar 

  4. Baur B, Fischer K, Winter K, Dietz K-J: cDNA sequence of a protein kinase from the inducible crassulacean acidmetabolism plant Mesembryanthemum crystallinum L., encoding a SNF-1 homolog. Plant Physiol 106: 1225–1226 (1994).

    PubMed  Google Scholar 

  5. Carling D, Aguan K, Woods A, Verhoeven AJM, Beri RK, Brennan CH, Sidebottom C, Davison MD, Scott J: Mammalian AMP-activated protein kinase is homologous to yeast and plant protein kinases involved in the regulation of carbon metabolism. J Biol Chem 269: 11442–11448 (1994).

    PubMed  Google Scholar 

  6. Carlson M: Regulation of sugar utilization in Saccharomyces species. J Bact 169: 4873–4877 (1987).

    PubMed  Google Scholar 

  7. Celenza JL, Carlson M:Ayeast gene that is essential for release from glucose repression encodes a protein kinase. Science 233: 1175–1180 (1986).

    Google Scholar 

  8. Celenza JL, Carlson M: Mutational analysis of the Saccharomyces cerevisiae SNF1 protein kinase and evidence for functional interaction with the SNF4 protein. Mol Cell Biol 9: 5034–5044 (1989).

    PubMed  Google Scholar 

  9. Chollet R, Vidal J, O'Leary MH: Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 273–298 (1996).

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  11. Gietz RD, Schiestl RH, Willems AR, Woods RA: Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355–360 (1995).

    PubMed  Google Scholar 

  12. Guillemaut P, Maréchal-Drouard L: Isolation of plant DNA: A fast, inexpensive, and reliable method. Plant Mol Biol Rep 10: 60–65 (1992).

    Google Scholar 

  13. Halford NG, Vicente-Carbajosa J, Sabelli PA, Shewry PR, Hannappel U, Kreis M: Molecular analyses of a barley multigene family homologous to the yeast protein kinase gene SNF1. Plant J 2: 791–797 (1992).

    PubMed  Google Scholar 

  14. Hanks SK, Hunter T. The eukaryotic protein kinase superfamily. In: Hardie G, Hanks S (eds) The Protein Kinase Facts Book: Protein-Serine Kinases, pp. 7–47. Academic Press, London (1995).

    Google Scholar 

  15. Hanks SK, Quinn AM, Hunter T: The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241: 42–52 (1988).

    PubMed  Google Scholar 

  16. Hardie GH. Cellular functions of protein kinases. In: Hardie G, Hanks S (eds) The Protein Kinase Facts Book: Protein-Serine Kinases, pp. 48–56. Academic Press, London (1995).

    Google Scholar 

  17. Hatch MD: C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895: 81–106 (1987).

    Google Scholar 

  18. Huber SC, Huber JL, McMichael RW Jr.: Control of plant enzyme activity by reversible protein phosphorylation. Int Rev Cytol 149: 47–98 (1994).

    Google Scholar 

  19. Hunter T, Karin M: The regulation of transcription by phosphorylation. Cell 70: 375–387 (1992).

    PubMed  Google Scholar 

  20. Höfer MU, Santore UJ, Westhoff P: Differential accumulation of the 10-, 16-and 23-kDa peripheral components of the watersplitting 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 

  21. Joshi CP: An inspection of the domain between putative TATAbox and translation start site in 79 plant genes. Nucl Acids Res 15: 6643–6653 (1987).

    PubMed  Google Scholar 

  22. Le Guen L, Thomas M, Bianchi M, Halford NG, Kreis M: Structure and expression of a gene from Arabidopsis thaliana encoding a protein related to SNF1 protein kinase. Gene 120: 249–254 (1992).

    PubMed  Google Scholar 

  23. Logemann J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).

    PubMed  Google Scholar 

  24. McMaster GK, Carmichael GG: Analysis of single and doublestranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci USA 74: 4835–4838 (1977).

    PubMed  Google Scholar 

  25. Muranaka T, Banno H, Machida Y: Characterization of tobacco protein kinase NPK5, a homolog of Saccharomyces cerevisiae SNF1 that constitutively activates expression of the glucoserepressible SUC2 gene for a secreted invertase of S. cerevisiae. Mol Cell Biol 14: 2958–2965 (1994).

    PubMed  Google Scholar 

  26. Müller F, Brühl K-H, Freidel K, Kowallik KV, Ciriacy M: Processing of TY1 proteins and formation of Ty1 virus-like particles in Saccharomyces cerevisiae. Mol Gen Genet 207: 421–429 (1987).

    PubMed  Google Scholar 

  27. Nelson T, Langdale JA: Developmental genetics of C4 photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 43: 25–47 (1992).

    Article  Google Scholar 

  28. Ranjeva R, Boudet M: Phosphorylation of proteins in plants: regulatory effects and potential involvement in stimulus/ response coupling. Annu Rev Plant Physiol 38: 73–93 (1987).

    Google Scholar 

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

    Google Scholar 

  30. Sano H, Youssefian S: Light and nutritional regulation of transcripts encoding a wheat protein kinase homolog is mediated by cytokinins. Proc Natl Acad Sci USA 91: 2582–2586 (1994).

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  32. Sheen JY, Bogorad L: Regulation of levels of nuclear transcripts for C4 photosynthesis in bundle sheath and mesophyll cells of maize leaves. Plant Mol Biol 8: 227–238 (1987).

    Google Scholar 

  33. Stockhaus J, Schlue U, Koczor M, Chitty JA, Taylor WC, Westhoff P: The promoter of the gene encoding the C4 form of phosphoenolpyruvate carboxylase directs mesophyll-specific expression in transgenic C4 Flaveria spp. Plant Cell, 479–489 (1997).

  34. Stone JM, Walker JC: Plant protein kinase families and signal transduction. Plant Physiol 108: 451–457 (1995).

    Article  PubMed  Google Scholar 

  35. Thompson JD, Higgins DG, Gibson TJ:CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673–4680 (1994).

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse 1, 40225, Düsseldorf, Germany

    Friederike Annen & Jörg Stockhaus

Authors
  1. Friederike Annen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jörg Stockhaus
    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

Annen, F., Stockhaus, J. Characterization of a Sorghum bicolor gene family encoding putative protein kinases with a high similarity to the yeast SNF1 protein kinase. Plant Mol Biol 36, 529–539 (1998). https://doi.org/10.1023/A:1005999921669

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005999921669

Search

Navigation