Skip to main content
SpringerLink
Log in

Evidence for functional convergence of redox regulation in G6PDH isoforms of cyanobacteria and higher plants

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In a recent paper (Wenderoth et al., J Biol Chem 272: 26985–26990, 1997) we reported that the positions of the two redox regulatory cysteines identified in a plastidic G6PD isoform from potato (Solanum tuberosum L.) differ substantially from those conserved in cyanobacterial G6PDH sequences. To investigate the origin of redox regulation in G6PDH enzymes from photoautotrophic organisms, we isolated and characterized several G6PD cDNA sequences from higher plants and from a green and a red alga. Alignments of the deduced amino acid sequences showed that the cysteine residues cluster in the coenzyme-binding domain of the plastidic isoforms and are conserved at three out of six positions. Comparison of the mature proteins and the signal peptides revealed that two different plastidic G6PDH classes (P1 and P2) evolved from a common ancestral gene. The two algal sequences branch off prior to this class separation in higher plants, sharing about similar amino acid identity with either of the two plastidic G6PDH classes. The genes for cytosolic plant isoforms clearly share a common ancestor with animal and fungal G6PDH homologues, whereas the cyanobacterial isoforms branch within the eubacterial G6PDH sequences. The data suggest that cysteine-mediated redox regulation arose independently in G6PDH isoenzymes of eubacterial and eukaryotic lineages.

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

  • Buchanan, B.B. 1991. Regulation of CO2 assimilation in oxigenic photosynthesis: the ferredoxin/thioredoxin system. Arch. Biochem. Biophys. 288: 1–9.

    Google Scholar 

  • Bult, C.J., White, O., Olsen, G.J., Zhou, L., Fleischmann, R.D., Sutton, G.G., Blake, J.A., FitzGerald, L.M., Clayton, R.A., Gocayne, J.D., Kerlavage, A.R., Dougherty, B.A., Tomb, J.-F., Adams, M.D., Reich, C.I., Overbeek, R., Kirkness, E.F., Weinstock, K.G., Merrick, J.M., Glodek, A., Scott, J.L., Geoghagen, N.S.M., Weidman, J.F., Fuhrmann, J.L., Nguyen, D., Utterback, T.R., Kelley, J.M., Peterson, J.D., Sadow, P.W., Hanna, M.C., Cotton, M.D., Roberts, K.M., Hurst, M.A., Kaine, B.P., Borodovsky, M., Klenk, H.-P., Fraser, C.M., Smith, H.O., Woese, C.R. and Venter, J.C. 1986. Complete genome sequence of the methanogenic Archeon, Methanococcus jannaschii. Science 273: 1058–1073.

    Google Scholar 

  • Church, G.M. and Gilbert, W. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81: 1991–1995.

    Google Scholar 

  • Copeland, L. and Turner, J.F. 1987. The regulation of glycolysis and the pentose-phosphate pathway. In: A. Marcus (Ed.), The Biochemistry of plants, vol. 11, Academic press, New York, pp. 107–125.

    Google Scholar 

  • Cossar, J.D., Rowell, P. and Stewart, W.D.P. 1984. Thioredoxin as a modulator of glucose-6-phosphate dehydrogenase in a N2-fixing cyanobacterium. J. Gen. Microbiol. 130: 991–998.

    Google Scholar 

  • de Boer, A.D. and Weisbeek, P.J. 1991. Chloroplast protein topogenesis: import, sorting and assembly. Biochim. Biophys. Acta 1071: 221–253.

    Google Scholar 

  • Dubois, F., Brugière, N., Sangwan, R.S. and Hirel, B. 1996. Localisation of tobacco cytosolic glutamine synthetase enzymes and the corresponding transcripts shows organ-and cell-specific patterns of protein synthesis and gene expression. Plant Mol. Biol. 31: 803–817.

    Google Scholar 

  • Elledge, S.J., Mulligan, J.T., Ramer, S.W., Spottswood, M. and Davis, R.W. 1991. λYES: a multifunctional cDNA expression vector for the isolation of genes by complementation of yeast and Escherichia coli mutations. Proc. Natl. Acad. Sci. USA 88: 1731–1735.

    Google Scholar 

  • Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    Google Scholar 

  • Fukasawa-Akada, T., Kung, S.D. and Watson, J.C. 1996. Phenylalanine ammonia-lyase gene structure, expression, and evolution in Nicotiana. Plant Mol. Biol. 30: 711–722.

    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 

  • Graeve, K., von Schaewen, A. and Scheibe, R. 1994. Purification, characterization and cDNA sequence of glucose-6-phosphate dehydrogenase from potato (Solanum tuberosum L.). Plant J. 5: 353–361.

    Google Scholar 

  • Kawarabayasi, Y., Sawada, M., Horikawa, H., Haikawa, Y., Hino, Y., Yamamoto, S., Sekine, M., Baba, S.-I., Kosugi, H., Hosoyama, A., Nagai, Y., Sakai, M., Ogura, K., Otsuka, R., Nakazawa, H., Takamiya, M., Ohfuku, Y., Funahashi, T., Tanaka, T., Kudoh, Y., Yamazaki, J., Kushida, N., Oguchi, A., Aoki, K.-I., Yoshizawa, T., Nakamura, Y., Robb, F.T., Horikoshi, K., Masuchi, Y., Shizuya, H. and Kikuchi, H. 1998. Complete sequence and gene organization of the genome of a hyper-thermophilic Archaebacterium, Pyrococcus horikoshii OT3 (supplement). DNA Res. 5 (Suppl.): 147–155.

    Google Scholar 

  • Klenk, H.P., Clayton, R.A., Tomb, J.F., White, O., Nelson, K.E., Ketchum, K.A., Dodson, R.J., Gwinn, M., Hickey, E.K., Peterson, J.D., Richardson, D.L., Kerlavage, A.R., Graham, D.E., Kyrpides, N.C., Fleischmann, R.D., Quackenbush, J., Lee, N.H., Sutton, G.G., Gill, S., Kirkness, E.F., Dougherty, B.A., Mckenney, K., Adams, M.D., Loftus, B., Peterson, S., Reich, C.I., McNeil, L.K., Badger, J.H., Glodek, A., Zhou, L., Overbeek, R., Gocayne, J.D., Weidman, J.F., McDonald, L., Utterback, T., Cotton, M.D., Spriggs, T., Artiach, P., Kaine, B.P., Sykes, S.M., Sadow, P.W., D'Andrea, K.P., Bowman, C., Fujii, C., Garland, S.A., Mason, T.M., Olsen, G.J., Fraser, C.M., Smith, H.O., Woese, C.R. and Venter, J.C. 1997. The complete genome sequence of the thermophilic, sulphate-reducing Archaeon Archaeoglobus fulgidus. Nature 390: 364–370.

    Google Scholar 

  • Knight, M.E., Halpin, C. and Schuch, W. 1992. Identification and characterisation of cDNA clones encoding cinnamyl alcohol dehydrogenase from tobacco. Plant Mol. Biol. 19: 793–801.

    Google Scholar 

  • Kronenberger, J., Lepingle, A., Caboche, M. and Vaucheret, H. 1993. Cloning and expression of distinct nitrite reductases in tobacco leaves and roots. Mol. Gen. Genet. 236: 203–208.

    Google Scholar 

  • Lechtreck, K.-F., Frins, S., Bilski, J., Teltenkötter, A., Weber, K. and Melkonian, M. 1996. The cruciated microtubule-associated fibers of the green alga Dunaliella bioculata consist of a 31 kDa SF-assemblin. J. Cell Sci. 109: 827–835.

    Google Scholar 

  • Lee, D. and Douglas, C.J. 1996. Two different members of a tobacco 4-coumarate:coenzyme A ligase (4CL) gene family. Plant Physiol. 112: 193–205.

    Google Scholar 

  • Lee, K.Y., Townsend, J., Tepperman, J., Black, M., Chui, C.F., Mazur, B., Dunsmuir, P. and Bedbrook, J. 1988. The molecular basis of sulfonylurea herbicide resistance in tobacco. EMBO J. 1241–1248.

  • Martin,W. and Herrmann, R.G. 1998. Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 118: 9–17.

    Google Scholar 

  • Martin, W. and Schnarrenberger, C. 1997. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr. Genet. 32: 1–18.

    Google Scholar 

  • Narayan, R.K.J. 1987. Nuclear DNA changes, genome differentiation and evolution in Nicotiana (Solanaceae). Plant Syst. Evol. 157: 161–180.

    Google Scholar 

  • Newman, J., Karakaya, H., Scanlan, D.J. and Mann, N.H. 1995. A comparison of gene organization in the zwf region of the genomes of the cyanobacteria Synechococcus sp. PCC 7942 and Anabaena sp. PCC 7120. FEMS Microbiol. Lett. 133: 187–193.

    Google Scholar 

  • Nicholas, K.B. and Nicholas, H.B. 1997. GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the authors.

  • Page, R.D.M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comp. Appl. Biosci. 12: 357–358.

    Google Scholar 

  • Purwantini, E., Gillis, T.P. and Daniels, L. 1997. Presence of F420-dependent glucose-6-phosphate dehydrogenase in Mycobacterium and Nocardia species, but absence from Streptomyces and Corynebacterium species and methanogenic Archaea. FEMS Microbiol. Lett. 146: 129–134.

    Google Scholar 

  • Rossmann, M.G., Liljas, A., Brändén, C.I. and Banaszak, L.J. 1975. Evolutionary and structural relationship among dehydrogenases. In: P.D. Boyer (Ed.), The Enzymes, 11, Academic Press, New York, pp. 61–102.

    Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.

    Google Scholar 

  • Sambrook, J., Fritsch, E.F. and Maniatis, P.J. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Scanlan, D.J., Newman, J., Sebaihia, M., Mann, N.H. and Carr, N.G. 1992. Cloning and sequence analysis of the glucose-6-phosphate dehydrogenase gene from the cyanobacterium Synechococcus PCC 7942. Plant Mol. Biol. 19: 877–880.

    Google Scholar 

  • Scheibe, R. 1990. Light/dark modulation: regulation of chloroplast metabolism in a new light. Bot. Acta 103: 327–334.

    Google Scholar 

  • Smith, D.R., Doucette-Stamm, L.A., Deloughery, C., Lee, H.M., Dubois, J., Aldredge, T., Bashirzadeh, R., Blakely, D., Cook, R., Gilbert, K., Harrison, D., Hoang, L., Keagle, P., Lumm, W., Pothier, B., Qiu, D.Y., Spadafora, R., Vicaire, R., Wang, Y., Wierzbowski, J., Gibson, R., Jiwani, N., Caruso, A., Bush, D., Safer, H., Patwell, D., Prabhakar, S., McDougall, S., Shimer, G., Goyal, A., Pietrokovski, S., Church, G.M., Daniels, C.J., Mao, J.-I., Rice, P., Nölling, J. and Reeve, J.N. 1997. Complete genome sequence of Methanobacterium thermoautotrophicum 1H: Functional analysis and comparative genomics. J. Bact. 179: 7135–7155.

    Google Scholar 

  • Summers, M.L., Meeks, J.C., Chu, S. and Wolf, R.E. Jr. 1995. Plant Gene register. Nucleotide sequence of an operon in Nostoc sp. strain ATCC 29133 encoding four genes of the oxidative pentose phosphate cycle. Plant Physiol. 107: 267–268.

    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, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.

    Google Scholar 

  • van Buuren, M., Neuhaus, J.-M., Shinshi, H., Ryals, J. and Meins, F. 1992. The structure and regulation of homologous tobacco endochitinase genes of Nicotiana sylvestris and N. tomentosiformis origin. Biochem. Plants 2: 279–316.

    Google Scholar 

  • Vaucheret, H., Vincenentz, M., Kronenberger, J., Caboche, M. and Rouzé, P. 1989. Molecular cloning and characterisation of the two homologous genes coding for nitrate reductase in tobacco. Mol. Gen. Genet. 232: 460–469.

    Google Scholar 

  • von Schaewen, A., Langenkämper, G., Graeve, K., Wenderoth, I. and Scheibe, R. 1995. Molecular characterization of the plastidic glucose-6-phosphate dehydrogenase from potato in comparison to its cytosolic counterpart. Plant Physiol. 109: 1327–1335.

    Google Scholar 

  • Wenderoth, I., Scheibe, R. and von Schaewen, A. 1997. Identifi-cation of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J. Biol. Chem. 272: 26985–26990.

    Google Scholar 

Download references

Author information

Author notes

  1. Urte K. Wendt & Irina Wenderoth

    Present address: MPB College GmbH, Eupener Str. 161, Eingang 60, 50933 , Köln, Germany

Authors and Affiliations

  1. Pflanzenphysiologie, FB 5, Biologie/Chemie, Universität Osnabrück, 49069, Osnabrück, Germany

    Rüdiger Hauschild, Mario Pietersma & Antje von Schaewen

  2. GenProfile AG, Robert-Roessle-Str. 10, 13125 , Berlin, Germany

    Christian Lange

Authors
  1. Urte K. Wendt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rüdiger Hauschild
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Lange
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mario Pietersma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Irina Wenderoth
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Antje von Schaewen
    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

Wendt, U.K., Hauschild, R., Lange, C. et al. Evidence for functional convergence of redox regulation in G6PDH isoforms of cyanobacteria and higher plants. Plant Mol Biol 40, 487–494 (1999). https://doi.org/10.1023/A:1006257230779

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006257230779

Search

Navigation