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Redox-Modification of Chloroplast Enzymes in Galdieria Sulphuraria: Trial-and-Error in Evolution or Perfect Adaptation to Extreme Conditions?

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Red Algae in the Genomic Age

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 13))

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Abstract

Regulation of enzyme activities is required for metabolism, in particular for assimilatory pathways in plastids of all photosynthetic eukaryotic organisms as well as in prokaryotes performing oxygenic photosynthesis. In order to be able to adjust the metabolic fluxes to the actual energy input and the demand, various enzymes have developed structures that are suitable for post-translational regulation by covalent redox-modification (Dietz et al., 2002). Reversible reduction/oxidation of cysteine residues is extremely suited for this purpose. It is mediated by thioredoxins that are present in all organisms (for review see: Buchanan, 1980)

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References

  • Baalmann, E., Backhausen, J.E., Kitzmann, C. and Scheibe, R. (1994) Regulation of NADP-dependent glyceraldehyde 3-phosphate dehydrogenase activity in spinach chloroplasts. Bot. Acta 107: 313–320.

    CAS  Google Scholar 

  • Baalmann, E., Backhausen, J.E., Vetter, S. and Scheibe, R. (1995) Reductive modification and non-reductive activation of purified spinach chloroplast NADP-glyceraldehyde 3-phosphate dehydrogenase. Arch. Biochem. Biophys. 324: 201–208.

    Article  PubMed  CAS  Google Scholar 

  • Baranowski, M. and Stec, B. (2007) Crystallization and characterization of Galdieria sulphuraria RUBISCO in two crystal forms: structural phase transition observed in P21 crystal form. Int. J. Mol. Sci. 8: 1039–1051.

    Article  CAS  Google Scholar 

  • Barbier, G., Oesterhelt, C., Larson, M.D., Halgren, R.G., Wilkerson, C., Garavito, R.M., Benning, C. and Weber, A.P.M. (2005) Comparative genomics of two closely related unicellular thermo-acidophilic red algae, Galdieria sulphuraria and Cyanidioschyzon merolae, reveals the molecular basis of the metabolic flexibility of Galdieria sulphuraria and significant differences in carbohydrate metabolism of both algae. Plant Physiol. 137: 460–474.

    Article  PubMed  CAS  Google Scholar 

  • Buchanan, B.B. (1980) Role of light in the regulation of chloroplast enzymes. Annu. Rev. Plant Physiol. 31: 341–374.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Buchanan, B.B. and Balmer, Y. (2005) Redox regulation: a broadening horizon. Annu. Rev. Plant Biol. 56: 187–220.

    Article  PubMed  CAS  Google Scholar 

  • Ciniglia, C., Yoon, H.S., Pollio, A., Pinto, G. and Bhattacharya, D. (2004) Hidden biodiversity of the extrremophilic Cyanidiales red algae. Mol. Ecol. 13: 1827–1838.

    Article  PubMed  CAS  Google Scholar 

  • Dietz, K.-J., Link, G., Pistorius, E.K. and Scheibe, R. (2002) Redox regulation in oxigenic photosynthesis. Prog. Bot. 63: 207–245.

    Article  CAS  Google Scholar 

  • Dunford, R.P., Durrant, M.C., Catley, M.A. and Dyer, T.A. (1998) Location of the redox-active cysteines in chloroplast sedoheptulose-1,7-bisphosphatase indicates that its allosteric regulation is similar but not identical to that of fructose-1,6-bisphosphatase. Photosynth. Res. 58: 221–230.

    Article  CAS  Google Scholar 

  • Faske, M., Holtgrefe, S., Ocheretina, O., Meister, M., Backhausen, J.E. and Scheibe, R. (1995) Redox equilibria between the regulatory thiols of light/dark-modulated enzymes and dithiothreitol: fine-tuning by metabolites. Biochim. Biophys. Acta 1247: 135–142.

    Article  PubMed  Google Scholar 

  • Geigenberger, P., Kolbe, A. and Tiessen, A. (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J. Exp. Bot. 56: 1469–1479.

    Article  PubMed  CAS  Google Scholar 

  • Gou, P., Hanke, G.T., Kimata-Ariga, Y., Standley, D.M., Kubo, A., Taniguchi, I., Nakamura, H. and Hase, T. (2006) Higher order structure contributes to specific differences in redox potential and electron transfer efficiency of root and leaf ferredoxins. Biochemistry 45: 14389–14396.

    Article  PubMed  CAS  Google Scholar 

  • Graciet, E., Lebreton, S., Camadro, J.-M. and Gontero, B. (2003) Characterization of native and recombinant A4 glyceraldehyde 3-phosphate dehydrogenase. Kinetic evidence for conformation changes upon association with the small protein CP12. Eur. J. Biochem. 270: 129–136.

    Article  PubMed  CAS  Google Scholar 

  • Gross, W. and Schnarrenberger, C. (1995) Heterotrophic growth to two strains of the acido-thermophilic red algae Galdieria sulphuraria. Plant Cell Physiol. 36: 633–638.

    CAS  Google Scholar 

  • Gross, W., Küver, J., Tischendorf, G., Bouchaala, N. and Büsch, W. (1998) Cryptoendolithic growth of the red alga Galdieria sulphuraria in volcanic areas. Eur. J. Phycol. 33: 25–31.

    Article  Google Scholar 

  • Hanke, G.T., Kimata-Ariga, Y., Taniguchi, I. and Hase, T. (2004) A post-genomic characterization of Arabidopsis ferredoxins. Plant Physiol. 134: 255–264.

    Article  PubMed  CAS  Google Scholar 

  • Jacquot, J.-P., Eklund, H., Rouhier, N. and Schürmann, P. (2009) Structural and evolutionary aspects of ­thioredoxin reductases in photosynthetic organisms. Trends Plant Sci. 14: 336–343.

    Article  PubMed  CAS  Google Scholar 

  • Martin, W., Scheibe, R. and Schnarrenberger, C. (1999) The calvin cycle and its regulation, In: R.C. Leegood, T.D. Sharkey and S. von Caemmerer (eds.) Advances of Photosynthesis, Vol. 9, Photosynthesis: Physiology and Metabolism. Kluwer, Dordrecht, The Netherlands, pp. 9–51.

    Chapter  Google Scholar 

  • Meyer, Y., Reichheld, J.P. and Vignols, F. (2005) Thioredoxins in Arabidopsis and other plants. Photosynth. Res. 86: 419–433.

    Article  PubMed  CAS  Google Scholar 

  • Mills, J.D. and Mitchell, P. (1982) Modulation of coupling factor ATPase activity in intact chloroplasts reversal of thiol modulation in the dark. Biochim. Biophys. Acta 679: 75–83.

    Article  CAS  Google Scholar 

  • Oesterhelt, C., Klocke, S., Holtgrefe, S., Linke, V., Weber, V.P.M. and Scheibe, R. (2007a) Redox regulation of chloroplast enzymes in Galdieria sulphuraria in view of eukaryotic evolution. Plant Cell Physiol. 48: 1359–1373.

    Article  PubMed  CAS  Google Scholar 

  • Oesterhelt, C., Schmälzlin, E., Schmitt, J.M. and Lokstein, H. (2007b) Regulation of photosynthesis in the unicellular acidophilic red alga Galdieria sulphuraria. Plant J. 51: 500–511.

    Article  PubMed  CAS  Google Scholar 

  • Onda, Y., Matsumura, T., Kimata-Ariga, Y., Sakakibara, H., Sugiyama, T. and Hase, T. (2000) Differential interaction of maize root ferredoxin: NADP+ oxidoreductase with photosynthetic and non-photosynthetic ferredoxin isoproteins. Plant Physiol. 123: 1037–1045.

    Article  PubMed  CAS  Google Scholar 

  • Pancic, P.G. and Strotmann, H. (1993) Structure of the nuclear encoded γ subunit of CF0CF1 of the diatom Odontella sinensis including its presequence. FEBS Lett. 320: 61–66.

    Article  PubMed  CAS  Google Scholar 

  • Pohlmeyer, K., Paap, B.K., Soll, J. and Wedel, N. (1996) CP12: a small nuclear-encoded chloroplast protein provides novel insights into higher-plant GAPDH evolution. Plant Mol. Biol. 32: 969–978.

    Article  PubMed  CAS  Google Scholar 

  • Porter, M.A., Stringer, C.D. and Hartman, F.C. (1988) Characterization of the regulatory thioredoxin site of phosphoribulokinase. J. Biol. Chem. 263: 123–129.

    PubMed  CAS  Google Scholar 

  • Reichert, A., Dennes, A., Vetter, S. and Scheibe, R. (2003) Chloroplast fructose 1,6-bisphosphatase with changed redox modulation: comparison of the Galdieria enzyme with cysteine mutants from spinach. Biochim. Biophys. Acta 1645: 212–217.

    Article  PubMed  CAS  Google Scholar 

  • Reyes-Prieto, A., Weber, A.P.M. and Bhattacharya, D. (2007) The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet. 41: 147–168.

    Article  PubMed  CAS  Google Scholar 

  • Reynolds, A.E., Chesnick, J.M., Woolford, J. and Cattolico, R.A. (1994) Chloroplast encoded thioredoxin genes in the red algae Porphyra yezoensis and Griffithsia pacifica: evolutionary implications. Plant Mol. Biol. 25: 13–21.

    Article  PubMed  CAS  Google Scholar 

  • Scheibe, R. (1991) Redox-modulation of chloroplast enzymes. A common principle for individual control. Plant Physiol. 96: 1–3.

    Article  PubMed  CAS  Google Scholar 

  • Scheibe, R., Wedel, N., Vetter, S., Emmerlich, V. and Sauermann, S.-M. (2002) Coexistence of two regulatory NADP-glyceraldehyde 3-P dehydrogenase complexes in higher plant chloroplasts. Eur. J. Biochem. 269: 5617–5624.

    Article  PubMed  CAS  Google Scholar 

  • Schürmann, P. and Buchanan, B.B. (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid. Redox Signal. 10: 1–39.

    Article  Google Scholar 

  • Schürmann, P. and Wolosiuk, R.A. (1978) Studies on the regulatory properties of chloroplast fructose-1,6-bisphosphatase. Biochim. Biophys. Acta 522: 130–138.

    Article  PubMed  Google Scholar 

  • Serrato, A.J., Pérez-Ruiz, J.M., Spínola, M.C. and Cejudo, F.J. (2004) A novel NADPH thoredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J. Biol. Chem. 279: 43821–43827.

    Article  PubMed  CAS  Google Scholar 

  • Sesma, J.I. and Iglesias, A.A. (1998) Synthesis of Floridean starch in the red alga Gracilaria Gracilis occurs via ADP-glucose, In: G. Garab (ed.) Photosynthesis: Mechanisms and Effects. Kluwer, Dordrecht, The Netherlands, pp. 3537–3540.

    Google Scholar 

  • Suzuki, A., Oaks, A., Jacquot, J.-P., Vidal, J. and Gadal, P. (1985) An electron transport system in maize roots for reactions of glutamate synthase and nitrite reductase: physiological and immunochemical properties of the electron carrier and pyridine nucleotide reductase. Plant Physiol. 78: 374–378.

    Article  PubMed  CAS  Google Scholar 

  • Takeda, T., Yokota, A. and Shigeoka, S. (1995) Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol. 36: 1089–1095.

    CAS  Google Scholar 

  • Tamoi, M., Murakami, A., Takeda, T. and Shigeoka, S. (1998) Lack of light/dark regulation of enzymes in the photosynthetic carbon reduction cycle in cyanobacteria Synechococcus PCC 7942 and Synechocystis PCC 6803. Biosci. Biotechnol. Biochem. 62: 374–376.

    Article  Google Scholar 

  • Udvardy, J., Borbély, G., Juhász, A. and Farkas, G.L. (1984) Thioredoxins and the redox modulation of glucose-6-phosphate dehydrogenase in Anabaena sp. strain PCC 7120 vegetative cells and heterocysts. J. Bacteriol. 157: 681–683.

    PubMed  CAS  Google Scholar 

  • Uemura, K., Anwaruzzaman, M., Miyachi, S. and Yokota, A. (1997) Ribulose-1,5-bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation. Biochem. Biophys. Res. Commun. 233: 568–571.

    Article  PubMed  CAS  Google Scholar 

  • Viola, R., Nyvall, P. and Pedersén, M. (2001) The unique features of starch metabolism in red algae. Proc. R. Soc. Lond. B 268: 1417–1422.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Wakao, S. and Benning, C. (2005) Genome-wide analysis of glucose-6-phosphate dehydrogenases in Arabidopsis. Plant J. 41: 243–256.

    Article  PubMed  CAS  Google Scholar 

  • Weber, A.P.M., Oesterhelt, C., Gross, W., Bräutigam, A., Imboden, L.A., Krassovskaya, I., Linka, N., Truchina, J., Schneidereit, J., Voll, H., Voll, L.M., Zimmermann, M., Jamai, A., Riekhof, W.R., Yu, B., Garavito, R.M. and Benning, C. (2004) EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol. Biol. 55: 17–32.

    Article  PubMed  CAS  Google Scholar 

  • Wedel, N. and Soll, J. (1998) Evolutionary conserved light regulation of Calvin cycle activity by NADPH-mediated reversible phosphoribulokinase/CP12/glyceraldehyde-3-phosphate dehydrogenase complex dissociation. Proc. Natl. Acad. Sci. USA 95: 9699–9704.

    Article  PubMed  CAS  Google Scholar 

  • Wedel, N., Soll, J. and Paap, B.K. (1997) CP12 provides a new mode of light regulation of Calvin cycle activity in higher plants. Proc. Natl. Acad. Sci. USA 94: 10479–10484.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Werner-Grüne, S., Gunkel, D., Schumann, J. and Strotmann, H. (1994) Insertion of a “chloroplast-like” regulatory segment responsible for thiol modulation into γ-subunit of F0F1-ATPase of the cyanobacterium Synechocystis 6803 by mutagenesis of atpC. Mol. Gen. Genet. 244: 144–150.

    Article  PubMed  Google Scholar 

  • Zhang, N. and Portis, A.R., Jr. (1999) Mechanism of light regulation of Rubisco: a specific role for the larger Rubisco activase isoform involving reductive activation by thioredoxin-f. Proc. Natl. Acad. Sci. USA 96: 9438–9443.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, N., Schürmann, P. and Portis, A.R., Jr. (2001) Characterization of the regulatory function of the 46-kD isoform of Rubisco activase from Arabidopsis. Photosynth. Res. 68: 29–37.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors wish to thank Heike Schwiderski for the preparation of the manuscript. Some of the work described in this paper has been financially supported by the Deutsche Forschungsgemeinschaft.

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Correspondence to Nicolas König .

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König, N., Scheibe, R. (2010). Redox-Modification of Chloroplast Enzymes in Galdieria Sulphuraria: Trial-and-Error in Evolution or Perfect Adaptation to Extreme Conditions?. In: Seckbach, J., Chapman, D. (eds) Red Algae in the Genomic Age. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 13. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3795-4_21

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