Enzymological evidence for the function of a plastid-located pyruvate carboxylase in the haptophyte alga emiliania huxleyi: A novel pathway for the production of C 4 compounds

Plant and Cell Physiology

Volumn 53, Issue 6, 2012, Pages 1043-1052

  Tsuji, Yoshinori ^a,b   Suzuki, Iwane ^a,b   Shiraiwa, Yoshihiro ^a,b  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Carboxylation; Anaplerotic reaction; Emiliania huxleyi (Haptophyta); Phosphoenolpyruvate carboxylase (PEPC); Photosynthetic carbon metabolism; Pyruvate carboxylase (PYC)

Indexed keywords

ALGAL PROTEIN; ASPARTIC ACID; AVIDIN; CARBON; CHLOROPLAST PROTEIN; MALIC ACID DERIVATIVE; OXALOACETIC ACID; PYRUVATE CARBOXYLASE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; DRUG ANTAGONISM; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; HAPTOPHYTA; INTRACELLULAR MEMBRANE; LIGHT; METABOLISM; MITOCHONDRION; PHOTOSYNTHESIS; PLANT GENE; PLASTID; PROTEIN DEGRADATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STREPTOMYCES LIVIDANS;

ALGAL PROTEINS; AMINO ACID SEQUENCE; ASPARTIC ACID; AVIDIN; CARBON; CHLOROPLAST PROTEINS; ENZYME ACTIVATION; GENES, PLANT; HAPTOPHYTA; INTRACELLULAR MEMBRANES; LIGHT; MALATES; MITOCHONDRIA; OXALOACETATE; PHOTOSYNTHESIS; PLASTIDS; PROTEIN TRANSPORT; PROTEOLYSIS; PYRUVATE CARBOXYLASE; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STREPTOMYCES LIVIDANS;

EID: 84862208236     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs045     Document Type: Article

References (32)

1. Akagawa, H., Ikawa, T. and Nishizawa, K. (1972) The enzyme system for the entrance of 14CO2 in the dark CO2-fixation of brown algae. Plant Cell Physiol. 13: 999-1016.
2. Appleby, G., Colbeck, J., Holdsworth, E.S. and Wadman, H. (1980) b-Carboxylation enzymes in marine phytoplankton and isolation and purification of pyruvate carboxylase from Amphidinium carterae (Dinophyceae). J. Phycol. 16: 290-295.
3. Bibb, M.J., Ward, J.M. and Hopwood, D.A. (1978) Transformation of plasmid DNA into Streptomyces at high frequency. Nature 274: 398-400. (Pubitemid 8387348)
4. Branson, J.P., Nezic, M., Wallace, J.C. and Attwood, P.V. (2002) Kinetic characterization of yeast pyruvate carboxylase isozyme pyc1. Biochemistry 41: 4459-4466. (Pubitemid 34259891)
5. Cabello-Pasini, A., Smith, G.J. and Alberte, R.S. (2000) Phosphoenolpyruvate carboxykinase from the marine diatom Skeletonema costatum and the phaeophyte Laminaria setchellii. I. Isolation and biochemical characterization. Bot. Mar. 43: 559-568.
6. Cassar, N. and Laws, E.A. (2007) Potential contribution of b-carboxylases to photosynthetic carbon isotope fractionation in a marine diatom. Phycologia 46: 307-314. (Pubitemid 46910304)
7. Danbara, A. and Shiraiwa, Y. (1999) The requirement of selenium for the growth of marine coccolithophorids, Emiliania huxleyi, Gephyrocapsa oceanica and Helladosphaera sp. (Prymnesiophyceae). Plant Cell Physiol. 40: 762-766. (Pubitemid 29360691)
8. Descolas-Gros, C. and Oriol, L. (1992) Variations in carboxylase activity in marine phytoplankton cultures. b-Carboxylation in carbon flux studies. Mar. Ecol. Prog. Ser. 85: 163-169.
9. Herai, S., Hashimoto, Y., Higashibata, H., Maseda, H., Ikeda, H., Omura, S. et al. (2004) Hyper-inducible expression system for streptomycetes. Proc. Natl Acad. Sci. USA 101: 14031-14035. (Pubitemid 39305024)
10. Hirokawa, Y., Fujiwara, S., Suzuki, M., Akiyama, T., Sakamoto, M., Kobayashi, S. et al. (2008) Structural and physiological studies on the storage b-polyglucan of haptophyte Pleurochrysis haptonemofera. Planta 227: 589-599.
11. Ishida, K. (2005) Protein targeting into plastids: a key to understanding the symbiogenetic acquisitions of plastids. J. Plant Res. 118: 237-245. (Pubitemid 41407026)
12. Izui, K., Matsumura, H., Furumoto, T. and Kai, Y. (2004) Phosphoenolpyruvate carboxylase: a new era of structural biology. Annu. Rev. Plant Biol. 55: 69-84. (Pubitemid 38940926)
13. Jiao, J.A. and Chollet, R. (1991) Posttranslational regulation of phosphoenolpyruvate carboxylase in C4 and Crassulacean acid metabolism plants. Plant Physiol. 95: 981-985. (Pubitemid 21913912)
14. Jitrapakdee, S., St Maurice, M., Rayment, I., Cleland, W.W., Wallace, J.C. and Attwood, P.V. (2008) Structure, mechanism and regulation of pyruvate carboxylase. Biochem. J 413: 369-387.
15. Jitrapakdee, S., Walker, M.E. and Wallace, J.C. (1999) Functional expression, purification, and characterization of recombinant human pyruvate carboxylase. Biochem. Biophys. Res. Commun. 266: 512-517. (Pubitemid 30028698)
16. Kremer, B.P. and Küppers, U. (1977) Carboxylating enzymes and pathway of photosynthetic carbon assimilation in different marine algae-evidence for the C4-pathway? Planta 133: 191-196.
17. Kroth, P.G., Chiovitti, A., Gruber, A., Martin-Jezequel, V., Mock, T., Parker, M.S. et al. (2008) A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3: e1426.
18. Lai, H., Kraszewski, J.L., Purwantini, E. and Mukhopadhyay, B. (2006) Identification of pyruvate carboxylase genes in Pseudomonas aeruginosa PAO1 and development of a P. aeruginosa-based overexpression system for alpha4-and alpa4beta4-type pyruvate carboxylases. Appl. Environ. Microbiol. 72: 7785-7792. (Pubitemid 44927685)
19. Libor, S.M., Sundaram, T.K. and Scrutton, M.C. (1978) Pyruvate carboxylase from a thermophilic Bacillus. Studies on the specificity of activation by acyl derivatives of coenzyme A and on the properties of catalysis in the absence of activator. Biochem. J. 169: 543-558. (Pubitemid 8281759)
20. Maberly, S.C., Courcelle, C., Groben, R. and Gontero, B. (2010) Phylogenetically-based variation in the regulation of the Calvin cycle enzymes, phosphoribulokinase and glyceraldehyde-3-phosphate dehydrogenase, in algae. J. Exp. Bot. 61: 735-745.
21. Marin-Valencia, I., Roe, C.R. and Pascual, J.M. (2010) Pyruvate carboxylase deficiency: mechanisms, mimics and anaplerosis. Mol. Genet. Metab. 101: 9-17.
22. Masumoto, C., Miyazawa, S., Ohkawa, H., Fukuda, T., Taniguchi, Y., Murayama, S. et al. (2010) Phosphoenolpyruvate carboxylase intrinsically located in the chloroplast of rice plays a crucial role in ammonium assimilation. Proc. Natl Acad. Sci. USA 107: 5226-5231.
23. Moellering, E.R., Ouyang, Y., Mamedov, T.G. and Chollet, R. (2007) The two divergent PEP-carboxylase catalytic subunits in the green microalga Chlamydomonas reinhardtii respond reversibly to inorganic-N supply and co-exist in the high-molecular-mass, hetero-oligomeric Class-2 PEPC complex. FEBS Lett. 581: 4871-4876. (Pubitemid 47531757)
24. Portis, A.R. and Heldt, H.W. (1976) Light-dependent changes of the Mg2+ concentration in the stroma in relation to the Mg2+ dependency of CO2 fixation in intact chloroplasts. Biochim. Biophys. Acta 449: 434-446.
25. Reinfelder, J.R., Kraepiel, A.M. and Morel, F.M. (2000) Unicellular C4 photosynthesis in a marine diatom. Nature 407: 996-999.
26. Reyes-Prieto, A., Weber, A.P. and Bhattacharya, D. (2007) The origin and establishment of the plastid in algae and plants. Annu. Rev. Genet. 41: 147-168.
27. Roberts, K., Granum, E., Leegood, R.C. and Raven, J.A. (2007) C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol. 145: 230-235. (Pubitemid 47416477)
28. Siedow, J.N. and Day, D.A. (2000) Respiration and photorespiration. In Biochemistry and Molecular Biology of Plants. Edited by Buchanan, B.B., Gruissem, W. and Jones, R.L. pp. 676-784. American Society of Plant Physiologists, Rockville, MD.
29. Stitt, M., Lilley, R.M. and Heldt, H.W. (1982) Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol. 70: 971-977.
30. Stucka, R., Dequin, S., Salmon, J.M. and Gancedo, C. (1991) DNA sequences in chromosomes II and VII code for pyruvate carboxylase isoenzymes in Saccharomyces cerevisiae: analysis of pyruvate carboxylase-deficient strains. Mol. Gen. Genet. 229: 307-315.
31. Tsuji, Y., Suzuki, I. and Shiraiwa, Y. (2009) Photosynthetic carbon assimilation in the coccolithophorid Emiliania huxleyi (Haptophyta): evidence for the predominant operation of the C3 cycle and the contribution of b-carboxylases to the active anaplerotic reaction. Plant Cell Physiol. 50: 318-329.
32. Varum, K.M., Kvam, B.J. and Myklestad, S. (1986) Structure of a food-reserve b-glucan produced by the haptophyte alga Emiliania huxleyi (Lohmann) Hay and Mohler. Carbohydr. Res. 152: 243-248.