An intrinsically disordered protein, CP12: Jack of all trades and master of the Calvin cycle

Biochemical Society Transactions

Volumn 40, Issue 5, 2012, Pages 995-999

  Gontero, Brigitte ^a   Maberly, Stephen C ^b  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

Author keywords

Calvin cycle; CP12; Intrinsically disordered protein; Protein protein interaction

Indexed keywords

CHLOROPLAST PROTEIN; COPPER; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INTRINSICALLY DISORDERED PROTEIN CP12; MALATE DEHYDROGENASE; NICKEL; PHOSPHORIBULOKINASE; UNCLASSIFIED DRUG;

ARABIDOPSIS; CARBON DIOXIDE FIXATION; CHLAMYDOMONAS REINHARDTII; CYANOPHAGE; CYANOPHORA; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INACTIVATION; HYDROPHOBICITY; NONHUMAN; OXIDATION REDUCTION STATE; PLANT METABOLISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS; SYNECHOCOCCUS;

AMINO ACID SEQUENCE; CHLOROPLAST PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOTOSYNTHESIS;

EID: 84866673529     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120097     Document Type: Review

References (49)

1. Babu, M.M., van der Lee, R., de Groot, N.S. and Gsponer, J. (2011) Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol. 21, 432-440
2. Dunker, A.K., Lawson, J.D., Brown, C.J., Williams, R.M., Romero, P., Oh, J.S., Oldfield, C.J., Campen, A.M., Ratliff, C.M., Hipps, K.W. et al. (2001) Intrinsically disordered protein. J. Mol. Graphics Modell. 19, 26-59
3. Dyson, H.J. and Wright, P.E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208
4. Tompa, P. (2002) Intrinsically unstructured proteins. Trends Biochem. Sci. 27, 527-533
5. Tompa, P. (2011) Unstructural biology coming of age. Curr. Opin. Struct. Biol. 21, 419-425
6. Uversky, V.N. and Dunker, A.K. (2010) Understanding protein non-folding. Biochim. Biophys. Acta 1804, 1231-1264
7. Kovacs, D., Kalmar, E., Torok, Z. and Tompa, P. (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol. 147, 381-390
8. Lisse, T., Bartels, D., Kalbitzer, H.R. and Jaenicke, R. (1996) The recombinant dehydrin-like desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. Biol. Chem. 377, 555-561
9. Lydakis-Simantiris, N., Hutchison, R.S., Betts, S.D., Barry, B.A. and Yocum, C.F. (1999) Manganese stabilizing protein of photosystem II is a thermostable, natively unfolded polypeptide. Biochemistry 38, 404-414
10. Graciet, E., Gans, P., Wedel, N., Lebreton, S., Camadro, J.M. and Gontero, B. (2003) The small protein CP12: a protein linker for supramolecular assembly. Biochemistry 42, 8163-8170
11. 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
12. 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. U.S.A. 95, 9699-9704
13. 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. U.S.A. 94, 10479-10484
14. Groben, R., Kaloudas, D., Raines, C.A., Offmann, B., Maberly, S.C. and Gontero, B. (2010) Comparative sequence analysis of CP12, a small protein involved in the formation of a Calvin cycle complex in photosynthetic organisms. Photosynth. Res. 103, 183-194
15. Boggetto, N., Gontero, B. and Maberly, S.C. (2007) Regulation of phosphoribulokinase and glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). J. Phycol. 43, 1227-1234
16. Marri, L., Trost, P., Pupillo, P. and Sparla, F. (2005) Reconstitution and properties of the recombinant glyceraldehyde-3-phosphate dehydrogenase/CP12/phosphoribulokinase supramolecular complex of Arabidopsis. Plant Physiol. 139, 1433-1443
17. Oesterhelt, C., Klocke, S., Holtgrefe, S., Linke, V., Weber, A.P. and Scheibe, R. (2007) Redox regulation of chloroplast enzymes in Galdieria sulphuraria in view of eukaryotic evolution. Plant Cell Physiol. 48, 1359-1373
18. 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 J. 42, 504-513
19. Thompson, L.R., Zeng, Q., Kelly, L., Huang, K.H., Singer, A.U., Stubbe, J. and Chisholm, S.W. (2011) Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc. Natl. Acad. Sci. U.S.A. 108, 757-764
20. Marri, L., Pesaresi, A., Valerio, C., Lamba, D., Pupillo, P., Trost, P. and Sparla, F. (2010) In vitro characterization of Arabidopsis CP12 isoforms reveals common biochemical and molecular properties. J. Plant Physiol. 167, 939-950
21. 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). Mol. Biol. Evol. 23, 1109-1118
22. Marri, L., Sparla, F., Pupillo, P. and Trost, P. (2005) Co-ordinated gene expression of photosynthetic glyceraldehyde-3-phosphate dehydrogenase, phosphoribulokinase, and CP12 in Arabidopsis thaliana. J. Exp. Bot. 56, 73-80
23. Graciet, E., Lebreton, S. and Gontero, B. (2004) Emergence of new regulatory mechanisms in the Benson-Calvin pathway via protein-protein interactions: a glyceraldehyde-3-phosphate dehydrogenase/CP12/ phosphoribulokinase complex. J. Exp. Bot. 55, 1245-1254
24. Hegyi, H. and Tompa, P. (2008) Intrinsically disordered proteins display no preference for chaperone binding in vivo. PLoS Comput. Biol. 4, e100001
25. Gardebien, F., Thangudu, R.R., Gontero, B. and Offmann, B. (2006) Construction of a 3D model of CP12, a protein linker. J. Mol. Graphics Modell. 25, 186-195
26. Lebreton, S., Andreescu, S., Graciet, E. and Gontero, B. (2006) Mapping of the interaction site of CP12 with glyceraldehyde-3-phosphate dehydrogenase from Chlamydomonas reinhardtii: functional consequences for glyceraldehyde-3- phosphate dehydrogenase. FEBS J. 273, 3358-3369
27. Lebreton, S., Graciet, E. and Gontero, B. (2003) Modulation, via protein-protein interactions, of glyceraldehyde-3-phosphate dehydrogenase activity through redox phosphoribulokinase regulation. J. Biol. Chem. 278, 12078-12084
28. Marri, L., Trost, P., Trivelli, X., Gonnelli, L., Pupillo, P. and Sparla, F. (2008) Spontaneous assembly of photosynthetic supramolecular complexes as mediated by the intrinsically unstructured protein CP12. J. Biol. Chem. 283, 1831-1838
29. Scheibe, R., Wedel, N., Vetter, S., Emmerlich, V. and Sauermann, S.M. (2002) Co-existence of two regulatory NADP-glyceraldehyde 3-P dehydrogenase complexes in higher plant chloroplasts. Eur. J. Biochem. 269, 5617-5624
30. Schurmann, P. and Buchanan, B.B. (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid. Redox Signaling 10, 1235-1274
31. Werdan, K., Heldt, H.W. and Milovancev, M. (1975) The role of pH in the regulation of carbon fixation in the chloroplast stroma: studies on CO2 fixation in the light and dark. Biochim. Biophys. Acta 396, 276-292
32. Howard, T.P., Metodiev, M., Lloyd, J.C. and Raines, C.A. (2008) Thioredoxin-mediated reversible dissociation of a stromal multiprotein complex in response to changes in light availability. Proc. Natl. Acad. Sci. U.S.A. 105, 4056-4061
33. Marri, L., Zaffagnini, M., Collin, V., Issakidis-Bourguet, E., Lemaire, S.D., Pupillo, P., Sparla, F., Miginiac-Maslow, M. and Trost, P. (2009) Prompt and easy activation by specific thioredoxins of Calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH/CP12/PRK supramolecular complex. Mol. Plant 2, 259-269
34. Howard, T.P., Lloyd, J.C. and Raines, C.A. (2011) Inter-species variation in the oligomeric states of the higher plant Calvin cycle enzymes glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase. J. Exp. Bot. 62, 3799-3805
35. Erales, J., Gontero, B. and Maberly, S.C. (2008) Specificity and function of glyceraldehyde-3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). J. Phycol. 44, 1455-1464
36. 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
37. 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. Photosynth. Res. 89, 1-13
38. Erales, J., Avilan, L., Lebreton, S. and Gontero, B. (2008) Exploring CP12 binding proteins revealed aldolase as a new partner for the phosphoribulokinase/glyceraldehyde 3-phosphate dehydrogenase/CP12 complex: purification and kinetic characterization of this enzyme from Chlamydomonas reinhardtii. FEBS J. 275, 1248-1259
39. Fuxreiter, M. and Tompa, P. (2012) Fuzzy complexes: a more stochastic view of protein function. Adv. Exp. Med. Biol. 725, 1-14
40. Gontero, B. and Avilan, L. (2011) Creating order out of disorder: structural imprint of GAPDH on CP12. Structure 19, 1728-1729
41. Matsumura, H., Kai, A., Maeda, T., Tamoi, M., Satoh, A., Tamura, H., Hirose, M., Ogawa, T., Kizu, N., Wadano, A. et al. (2011) Structure basis for the regulation of glyceraldehyde-3-phosphate dehydrogenase activity via the intrinsically disordered protein CP12. Structure 19, 1846-1854
42. Erales, J., Mekhalfi, M., Woudstra, M. and Gontero, B. (2011) Molecular mechanism of NADPH-glyceraldehyde-3-phosphate dehydrogenase regulation through the C-terminus of CP12 in Chlamydomonas reinhardtii. Biochemistry 50, 2881-2888
43. Lorenzi, M., Puppo, C., Lebrun, R., Lignon, S., Roubaud, V., Martinho, M., Mileo, E., Tordo, P., Marque, S.R., Gontero, B. et al. (2011) Tyrosine-targeted spin labeling and EPR spectroscopy: an alternative strategy for studying structural transitions in proteins. Angew. Chem. Int. Ed. 50, 9108-9111
44. Singh, P., Kaloudas, D. and Raines, C.A. (2008) Expression analysis of the Arabidopsis CP12 gene family suggests novel roles for these proteins in roots and floral tissues. J. Exp. Bot. 59, 3975-3985
45. Howard, T.P., Fryer, M.J., Singh, P., Metodiev, M., Lytovchenko, A., Obata, T., Fernie, A.R., Kruger, N.J., Quick, W.P., Lloyd, J.C. et al. (2011) Antisense suppression of the small chloroplast protein CP12 in tobacco alters carbon partitioning and severely restricts growth. Plant Physiol. 157, 620-631
46. Howard, T.P., Upton, G.J., Lloyd, J.C. and Raines, C.A. (2011) Antisense suppression of the small chloroplast protein CP12 in tobacco: a transcriptional viewpoint. Plant Signaling Behav. 6, 1-5
47. Erales, J., Lignon, S. and Gontero, B. (2009) CP12 from Chlamydomonas reinhardtii, a permanent specific "chaperone-like" protein of glyceraldehyde-3-phosphate dehydrogenase. J. Biol. Chem. 284, 12735-12744
48. Delobel, A., Graciet, E., Andreescu, S., Gontero, B., Halgand, F. and Laprevote, O. (2005) Mass spectrometric analysis of the interactions between CP12, a chloroplast protein, and metal ions: a possible regulatory role within a PRK/GAPDH/CP12 complex. Rapid Commun. Mass Spectrom. 19, 3379-3388
49. Erales, J., Gontero, B., Whitelegge, J. and Halgand, F. (2009) Mapping of a copper-binding site on the small CP12 chloroplastic protein of Chlamydomonas reinhardtii using top-down mass spectrometry and site-directed mutagenesis. Biochem. J. 419, 75-82