Regulation of glyceraldehyde-3-phosphate dehydrogenase in the eustigmatophyte Pseudocharaciopsis ovalis is intermediate between a chlorophyte and a diatom

European Journal of Phycology

Volumn 47, Issue 3, 2012, Pages 207-215

  Avilan, Luisana ^a   Maberly, Stephen C ^b   Mekhalfi, Malika ^a   Plateau, Julia ^a   Puppo, Carine ^a   Gontero, Brigitte ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

Author keywords

Asterionella formosa; Bacillariophyceae; Calvin cycle; Chlamydomonas reinhardtii; Chlorophyta; chromalveolates; CP12; enzyme regulation; Eustigmatophyceae; GAPDH; Plantae; regulation by pH

Indexed keywords

BIOCHEMISTRY; DIATOM; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GREEN ALGA; INHIBITION; LIGHT EFFECT; MOLECULAR ANALYSIS; PH; PLASTID;

ASTERIONELLA FORMOSA; BACILLARIOPHYCEAE; BACILLARIOPHYTA; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; CHROMALVEOLATA; EUSTIGMATOPHYCEAE; PLANTAE; PSEUDOCHARACIOPSIS;

EID: 84865813701     PISSN: 09670262     EISSN: 14694433     Source Type: Journal    
DOI: 10.1080/09670262.2012.687459     Document Type: Article

References (48)

1. Avilan, L, Gontero, B, Lebreton, S and Ricard, J. 1997. Memory and imprinting effects in multienzyme complexes-I. Isolation, dissociation, and reassociation of a phosphoribulokinase-glyceraldehyde-3-phosphate dehydrogenase complex from Chlamydomonas reinhardtii chloroplasts. European Journal of Biochemistry, 246: 78-84.
2. Baalmann, E, Backhausen, JE, Kitzmann, C and Scheibe, R. 1994. Regulation of NADP-dependent glyceraldehyde 3-phosphate dehydrogenase activity in spinach chloroplast. Botanica Acta, 107: 313-320.
3. Baalmann, E, Backhausen, JE, Rak, C, Vetter, S and Scheibe, R. 1995. Reductive modification and nonreductive activation of purified spinach chloroplast NADP-dependent glyceraldehyde-3-phosphate dehydrogenase. Archives of Biochemistry and Biophysics, 324: 201-208.
4. Baier, D and Latzko, E. 1975. Properties and regulation of C-1-fructose-1,6-diphosphatase from spinach chloroplasts. Biochimica et Biophysica Acta, 396: 141-148.
5. Beakes, G, Canter, HM and Jaworski, GHM. 1988. Zoospores ultrastructure of Zygorhizidium affluens and Z. planktonicum, two chytrids parasitizing the diatom Asterionella formosa. Canadian Journal of Botany, 66: 1054-1067.
6. Boggetto, N, Gontero, B and Maberly, SC. 2007. Regulation of phosphoribulokinase and glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). Journal of Phycology, 43: 1227-1234.
7. Bradford, MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-254.
8. Brinkmann, H, Cerff, R, Salomon, M and Soll, J. 1989. Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach. Plant Molecular Biology, 13: 81-94.
9. Buchanan, BB. 1980. Role of light in the regulation of chloroplast enzymes. Annual Review of Plant Physiology, 31: 341-374.
10. Cerff, R. 1979. Quaternary structure of higher plant glyceraldehyde-3-phosphate dehydrogenases. European Journal of Biochemistry, 94: 243-247.
11. Coleman, JR and Rotatore, C. 1995. Photosynthetic inorganic carbon uptake and accumulation in two marine diatoms. Plant, Cell and Environment, 18: 918-624.
12. Cseke, C, Nishizawa, AN and Buchanan, BB. 1982. Modulation of chloroplast phosphofructokinase by NADPH: a mechanism for linking light to the regulation of glycolysis. Plant Physiology, 70: 658-661.
13. Erales, J, Gontero, B and Maberly, SC. 2008. Specificity and function of glyceraldehyde-3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). Journal of Phycology, 44: 1455-1464.
14. Falkowski, PG, Katz, ME, Knoll, AH, Quigg, A, Raven, JA, Schofield, O and Taylor, FJ. 2004. The evolution of modern eukaryotic phytoplankton. Science, 305: 354-360.
15. Field, CB, Behrenfeld, MJ, Randerson, JT and Falkowski, P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science, 281: 237-240.
16. Gontero, B, Avilan, L and Lebreton, S. 2006. "Control of carbon fixation in chloroplasts". In Annual Plant Reviews, Edited by: Plaxton, WC and McManus, MT. 187-218. Oxford: Blackwell Publishing.
17. Gontero, B, Lebreton, S and Graciet, E. 2001. "Multienzyme complexes involved in the Benson-Calvin cycle and in fatty acid metabolism". In Annual Plant Reviews, Edited by: McManus, MT, Laing, WA and Allan, AC. 120-150. Sheffield: Sheffield Academic Press.
18. Graciet, E, Lebreton, S, Camadro, JM and Gontero, B. 2003. Characterization of native and recombinant A4 glyceraldehyde 3-phosphate dehydrogenase. European Journal of Biochemistry, 270: 129-136.
19. Green, BR. 2011. After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynthesis Research, 107: 103-115.
20. Groben, R, Kaloudas, D, Raines, CA, Offmann, B, Maberly, SC and Gontero, B. 2010. Comparative sequence analysis of CP12, a small protein involved in the formation of a Calvin cycle complex in photosynthetic organisms. Photosynthesis Research, 103: 183-194.
21. HALLIWELL, B. (editor) (1984). Chloroplast Metabolism: The Structure and Function of Chloroplasts in Green Leaf Cells. Oxford University Press, New York
22. Heineke, D, Burgi, R, Heike, G, Hoferichter, P, Peter, U, Flügge, UI and Heldt, HW. 1991. Redox transfer across the inner chloroplast envelope membrane. Plant Physiology, 95: 1131-1137.
23. Heldt, WH, Werdan, K, Milovancev, M and Geller, G. 1973. Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochimica et Biophysica Acta, 314: 224-241.
24. Hibberd, DJ and Leedale, GF. 1971. A new algal class-the Eustigmatophyceae. Taxon, 20: 523-525.
25. Kroth, PG, Chiovitti, A, Gruber, A, Martin-Jezequel, V, Mock, T, Parker, MS, Stanley, MS, Kaplan, A, Caron, L, Weber, T, Maheswari, U, Armbrust, EV and Bowler, C. 2008. A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS ONE, 3: e1426
26. Lazaro, JJ, Sutton, CW, Nicholson, S and Powls, R. 1986. Characterisation of two forms of phosphoribulokinase isolated from the green alga, Scenedesmus obliquus. European Journal of Biochemistry, 156: 423-429.
27. Liaud, MF, Brandt, U, Scherzinger, M and Cerff, R. 1997. Evolutionary origin of cryptomonad microalgae: two novel chloroplast/cytosol-specific GAPDH genes as potential markers of ancestral endosymbiont and host cell components. Journal of Molecular Evolution, 44: S28-37.
28. Maberly, SC, 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. Journal of Experimental Botany, 61: 735-745.
29. Mead, R and Curnow, RN. 1983. Statistical Methods in Agriculture and Experimental Biology Chapman and Hall, London
30. Michels, AK, Wedel, N and Kroth, PG. 2005. Diatom plastids possess a phosphoribulokinase with an altered regulation and no oxidative pentose phosphate pathway. Plant Physiology, 137: 911-920.
31. Moustafa, A, Beszteri, B, Maier, UG, Bowler, C, Valentin, K and Bhattacharya, D. 2009. Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science, 324: 1724-1726.
32. Nicholson, S, Easterby, JS and Powls, R. 1987. Properties of a multimeric protein complex from chloroplasts possessing potential activities of NADPH-dependent glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. European Journal of Biochemistry, 162: 423-431.
33. O'Brien, MJ, Easterby, JS and Powls, R. 1977. Glyceraldehyde-3-phosphate dehydrogenase of Scenedesmus obliquus. Effects of dithiothreitol and nucleotide on coenzyme specificity. Biochimica et Biophysica Acta, 481: 348-358.
34. Petersen, J, Teich, R, Becker, B, Cerff, R and Brinkmann, H. 2006. The GapA/B gene duplication marks the origin of Streptophyta (charophytes and land plants). Molecular Biology and Evolution, 23: 1109-1118.
35. Pohlmeyer, K, Paap, BK, Soll, J and Wedel, N. 1996. CP12: a small nuclear-encoded chloroplast protein provides novel insights into higher-plant GAPDH evolution. Plant Molecular Biology, 32: 969-978.
36. 2 fixation in intact chloroplasts. Biochimica et Biophysica Acta, 449: 434-436.
37. Pupillo, P and Piccari, GG. 1973. The effect of NADP on the subunit structure and activity of spinach chloroplast glyceraldehyde-3-phosphate dehydrogenase. Archives of Biochemistry and Biophysics, 154: 324-331.
38. Schurmann, P and Jacquot, JP. 2000. Plant thioredoxin systems revisited. Annual Review of Plant Physiology and Plant Molecular Biology, 51: 371-400.
39. Sparla, F, Pupillo, P and Trost, P. 2002. The C-terminal extension of glyceraldehyde-3-phosphate dehydrogenase subunit B acts as an autoinhibitory domain regulated by thioredoxins and nicotinamide adenine dinucleotide. Journal of Biological Chemistry, 277: 44946-44952.
40. Takishita, K, Yamaguchi, H, Maruyama, T and Inagaki, Y. 2009. A hypothesis for the evolution of nuclear-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase genes in 'chromalveolate' members. PLoS One, 4: e4737
41. Tamoi, M, Miyazaki, T, Fukamizo, T and Shigeoka, S. 2005. The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. Plant Journal, 42: 504-513.
42. Trost, P, Fermani, S, Marri, L, Zaffagnini, M, Falini, G, Scagliarini, S, Pupillo, P and Sparla, F. 2006. Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase: autonomous vs. CP12-dependent mechanisms. Photosynthesis Research, 89: 1-13.
43. Weber, T, Gruber, A and Kroth, PG. 2009. The presence and localization of thioredoxins in diatoms, unicellular algae of secondary endosymbiotic origin. Molecular Plant, 2: 468-477.
44. 2 fixation in the light and dark. Biochimica et Biophysica Acta, 396: 276-292.
45. Wilhelm, C, Buchel, C, Fisahn, J, Goss, R, Jakob, T, Laroche, J, Lavaud, J, Lohr, M, Riebesell, U, Stehfest, K, Valentin, K and Kroth, PG. 2006. The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist, 157: 91-124.
46. Wittpoth, C, Kroth, PG, Weyrauch, K, Kowallik, KV and Strotmann, H. 1998. Functional characterization of isolated plastids from two marine diatoms. Planta, 206: 79-85.
47. Wolosiuk, RA and Buchanan, BB. 1976. Studies on the regulation of chloroplast NADP-linked glyceraldehyde-3-phosphate dehydrogenase. Journal of Biological Chemistry, 251: 6456-6461.
48. Zimmermann, G, Kelly, GJ and Latzko, E. 1976. Efficient purification and molecular properties of spinach chloroplast fructose 1,6-bisphosphatase. European Journal of Biochemistry, 70: 361-367.