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Regulation of the low-CO2-inducible polypeptides in Chlamydomonas reinhardtii

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Abstract

Polypeptides of 21, 36 and 37 kDa are induced in the unicellular green alga Chlamydomonas reinhardtii Dang. when cells are transferred from high (2%) to low (0.03%) CO2 concentrations. The synthesis of these polypeptides is correlated with the induction of the CO2-concentrating mechanism. In this work we studied the effect of the growth conditions on the synthesis of these polypeptides with the aim of clarifying whether the induction of all three of these low-CO2-inducible polypeptides requires the same environmental factor. Our results showed that induction of the 21- and 36-kDa polypeptides under low-CO2 conditions occurred only in the light, while the 37-kDa periplasmic carbonic anhydrase (EC 4.2.1.1) was induced in light, darkness, and in both synchronous and asynchronous cultures. In addition, induction of these polypeptides appeared to be determined more by the O2/CO2 ratio than by the CO2 concentrations. None of these polypeptides could be induced in either of two different mutants of C. reinhardtii, one lacking ribulose-1,5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39) and the other with inactive enzyme. Our results indicate that the 21- and 36-kDa polypeptides are regulated by a mechanism different from that controlling the 37-kDa polypeptide.

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Abbreviations

pCA:

(periplasmic) carbonic anhydrase

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

TAP:

Trisacetate phosphate medium

References

  • Badger MR, Kaplan A, Berry JA (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii: Evidence for a carbon dioxide concentrating mechanism. Plant Physiol 66: 407–413

    Google Scholar 

  • Bailly J, Coleman JR (1988) Effect of CO2 concentration on protein biosynthesis and carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 87: 833–840

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254

    Google Scholar 

  • Chen Z, Green D, Westhoff C, Spreitzer RJ (1990) Nuclear mutation restores the reduced CO2/O2 specificity of ribulosebisphosphate carboxylase/oxygenase in a temperature-conditional chloroplast mutant of Chlamydomonas reinhardtii. Arch Biochem Biophys 283: 60–67

    Google Scholar 

  • Coleman JR (1990) The molecular biology of carbonic anhydrase expression in Chlamydomonas reinhardtii. In: Baltscheffsky M. (ed) Current research in photosynthesis, vol. IV. Kluwer Academic Publishers, Dordrecht, pp 455–462

    Google Scholar 

  • Coleman JR, Grossman AR (1984) Biosynthesis of carbonic anhydrase in Chlamydomonas reinhardtii during adaptation to low CO2. Proc Natl Acad Sci USA 81: 6049–6053

    Google Scholar 

  • Coleman JR, Berry JA, Togasaki RT, Grossman AR (1984) Identification of extracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 76: 472–477

    Google Scholar 

  • Dionisio-Sese ML, Fukuzawa H, Miyachi S (1990) Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 94: 1103–1120

    Google Scholar 

  • Eriksson M, Ramazanov Z, Villarejo A, Gardeström P, Samuelsson G (1995) Mitochondrial localisation of a 22 kilodalton polypeptide induced by low CO2 in Chlamydomonas reinhardtii. Planta, in press

  • Fukuzawa H, Fujiwara S, Yamamoto Y, Dionisio-Sese ML, Miyachi S (1990) cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: regulation by environment CO2 concentration. Proc Natl Acad Sci USA 87: 4383–4387

    Google Scholar 

  • Geraghty AM, Spalding MH (1995) Molecular and ultrastructure aspects of the adaptation of Chlamydomonas to limiting CO2. Plant Physiol 108: 424

    Google Scholar 

  • Geraghty AM, Anderson JC, Spalding MH (1990) A 36 kilodalton limiting-CO2 induced polypeptide of Chlamydomonas reinhardtii is distinct from the 37 kilodalton periplasmic carbonic anhydrase. Plant Physiol 93: 116–121

    Google Scholar 

  • Husic HD (1991) Extracellular carbonic anhydrase from Chlamydomonas reinhardtii: localization, structural properties, and catalytic properties. Can J Bot 69: 1079–1087

    Google Scholar 

  • Husic HD, Marcus CA (1994) Identification of intracellular carbonic anhydrase in Chlamydomonas reinhardtii with a carbonic anhydrase-directed photoaffinity label. Plant Physiol 105: 133–139

    Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680–685

    PubMed  Google Scholar 

  • Manuel LJ, Moroney JV (1988) Inorganic carbon accumulation in Chlamydomonas reinhardtii: new proteins are made during adaptation to low CO2. Plant Physiol 88: 491–496

    Google Scholar 

  • Moroney JV, Mason CB (1991) The role of the chloroplast in inorganic carbon acquisition by Chlamydomonas reinhardtii. Can J Bot 69: 1017–1024

    Google Scholar 

  • Palmqvist K, Ramazanov Z, Samuelsson G (1990) The role of extracellular carbonic anhydrase for accumulation of inorganic carbon in the green alga Chlamydomonas reinhardtii. A comparison between wild-type and cell-wall-less mutant cells. Physiol Plant 80: 267–276

    Google Scholar 

  • Plumed MP, Jiménez del Ro M, Garca Reina G, Ramazanov Z (1995) The function of ribulose-1,5-bisphosphate carboxylase/oxygenase is required for the induction of the 37-kDa periplasmic carbonic anhydrase in Chlamydomonas reinhardtii. Scientia Marina, in press

  • Ramazanov Z, Cárdenas J (1992) Involvement of photorespiration and glycolate pathway in carbonic anhydrase induction and inorganic carbon concentration in Chlamydomonas reinhardtii. Physiol Plant 84: 502–508

    Google Scholar 

  • Ramazanov ZM, Semenenko VE (1984) Oxygen-dependent induction of synthesis of the CO2-dependent soluble form of carbonic anhydrase in Chlorella cells. Sov Plant Physiol 31: 344–349

    Google Scholar 

  • Ramazanov ZM, Semenenko VE (1986) Participation of photorespiratory products in induction of the CO2-dependent form of carbonic anhydrase. Sov Plant Physiol 33: 659–666

    Google Scholar 

  • Ramazanov Z, Semenenko VE (1988) Content of the CO2-dependent form of carbonic anhydrase is depending on the light intensity and photosynthesis. Sov Plant Physiol 35: 340–344

    Google Scholar 

  • Ramazanov Z, Mason C, Geraghty A, Spalding M, Moroney J (1993) The low CO2-inducible 36-kilodalton protein is localized in the chloroplast envelope of Chlamydomonas reinhardtii. Plant Physiol 101: 1195–1199

    Google Scholar 

  • Ramazanov Z, Rawat M, Henk C, Mason C, Mathews S, Moroney J (1994) The induction of the CO2-concentrating mechanism is correlated with the formation of the starch sheath around the pyrenoid of Chlamydomonas reinhardtii. Planta 195: 210–216

    Google Scholar 

  • Samuelsson G, Palmqvist K, Ramazanov Z, Sundbland LG (1990) Photosynthetic acclimation to low carbon concentrations in Chlamydomonas reinhardtii. In: Baltscheffsky M (ed) Current research in photosynthesis, vol. 4. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 18441–18448

    Google Scholar 

  • Shiraiwa Y, Miyachi S (1983) Factors controlling induction of carbonic anhydrase and efficiency of photosynthesis in Chlorella vulgaris 11 h cells. Plant Cell Physiol 24: 919–923

    Google Scholar 

  • Spalding MH, Ogren WL (1982) Photosynthesis is required for induction of the CO2-concentrating mechanism in Chlamydomonas reinhardtii. FEBS Lett 145: 41–44

    Google Scholar 

  • Spalding MH, Spreitzer RJ, Ogren WL (1983) Genetic and physiologycal analysis of the CO2-concentrating system of Chlamydomonas reinhardtii. Planta 159: 261–266

    Google Scholar 

  • Spalding MH, Jeffrey M (1989) Membrane-associated polypeptides induced in Chlamydomonas by limiting CO2 concentrations. Plant Physiol 89: 133–137

    Google Scholar 

  • Spalding MH, Winder TL, Anderson JC, Geraghty AM, Marek LF (1991) Changes in protein and gene expression during induction of the CO2-concentrating mechanism in wild-type and mutant Chlamydomonas. Can J Bot 69: 1008–1016

    Google Scholar 

  • Spencer KG, Kimpel DL, Fisher ML, Togasaki RK, Miyachi S (1983) Carbonic anhydrase in Chlamydomonas reinhardtii. II: requirements for carbonic anhydrase induction. Plant Cell Physiol 24: 301–304

    Google Scholar 

  • Spreitzer RL, Jordan DB, Ogren WL (1982) Biochemical and genetic analysis of ribulosebisphosphate carboxylase/oxygenase deficient mutants and revenants of Chlamydomonas reinhardtii. FEBS Lett 148: 117–121

    Google Scholar 

  • Spreitzer RJ, Goldschmidt-Clermont M, Rahiré M, Rochaix JD (1985) Nonsense mutations in the Chlamydomonas chloroplast gene that codes for the large subunit of ribulosebisphosphate carboxylase/oxygenase. Proc Natl Acad Sci USA 82: 5460–5464

    Google Scholar 

  • Sueoka N (1960) Mitotic replication of deoxyribonucleic acids in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 46: 83–91

    Google Scholar 

  • Wintermans JF, De Mots A (1965) Spectrophotometric characteristics of chlorophyll a and b and their pheophytins in ethanol. Biochim Biophys Acta 109: 448–453

    Google Scholar 

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Correspondence to Ziyadin Ramazanov.

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The authors thank Prof. M. Spalding (Iowa State University, USA) for providing antisera to LIP-21 and LIP-36. We thank Prof. S. Bartlett and Dr. J. Moroney (Louisiana State University, USA) for providing antibodies to C. reinhardtii, Rubisco and 37-kDa pCA, respectively. This work was supported by the Instituto Tecnologico de Canarias.

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Villarejo, A., Reina, G.G. & Ramazanov, Z. Regulation of the low-CO2-inducible polypeptides in Chlamydomonas reinhardtii . Planta 199, 481–485 (1996). https://doi.org/10.1007/BF00195176

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  • DOI: https://doi.org/10.1007/BF00195176

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