Skip to main content
Log in

Comparative sequence analysis of CP12, a small protein involved in the formation of a Calvin cycle complex in photosynthetic organisms

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

CP12, a small intrinsically unstructured protein, plays an important role in the regulation of the Calvin cycle by forming a complex with phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH). An extensive search in databases revealed 129 protein sequences from, higher plants, mosses and liverworts, different groups of eukaryotic algae and cyanobacteria. CP12 was identified throughout the Plantae, apart from in the Prasinophyceae. Within the Chromalveolata, two putative CP12 proteins have been found in the genomes of the diatom Thalassiosira pseudonana and the haptophyte Emiliania huxleyi, but specific searches in further chromalveolate genomes or EST datasets did not reveal any CP12 sequences in other Prymnesiophyceae, Dinophyceae or Pelagophyceae. A species from the Euglenophyceae within the Excavata also appeared to lack CP12. Phylogenetic analysis showed a clear separation into a number of higher taxonomic clades and among different forms of CP12 in higher plants. Cyanobacteria, Chlorophyceae, Rhodophyta and Glaucophyceae, Bryophyta, and the CP12-3 forms in higher plants all form separate clades. The degree of disorder of CP12 was higher in higher plants than in the eukaryotic algae and cyanobacteria apart from the green algal class Mesostigmatophyceae, which is ancestral to the streptophytes. This suggests that CP12 has evolved to become more flexible and possibly take on more general roles. Different features of the CP12 sequences in the different taxonomic groups and their potential functions and interactions in the Calvin cycle are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105

    Article  CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  CAS  PubMed  Google Scholar 

  • Avilan L, Gontero B, Lebreton S, 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. Eur J Biochem 246:78–84

    Article  CAS  PubMed  Google Scholar 

  • Boggetto N, Gontero B, Maberly SC (2007) Regulation of phosphoribulokinase and glyceraldehyde 3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). J Phycol 43:1227–1234

    Article  CAS  Google Scholar 

  • Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  CAS  PubMed  Google Scholar 

  • Daugbjerg N, Moestrup O, Arctander P (1995) Phylogeny of genera of Prasinophyceae and Pedinophyceae (Chlorophyta) deduced from molecular analysis of the rbcL gene. Phycol Res 43:203–213

    Article  Google Scholar 

  • Dunker AK (2007) Another window into disordered protein function. Structure 15:1026–1028

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, Von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Prot Sci 8:978–984

    Article  CAS  Google Scholar 

  • Erales J, Avilan L, Lebreton S, Gontero B (2008a) 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

    Article  CAS  PubMed  Google Scholar 

  • Erales J, Gontero B, Maberly SC (2008b) Specificity and function of glyceraldehyde-3-phosphate dehydrogenase in a freshwater diatom, Asterionella formosa (Bacillariophyceae). J Phycol 44:1455–1464

    Article  CAS  Google Scholar 

  • Erales J, Lignon S, Gontero B (2009) CP12 from Chlamydomonas reinhardtii, a permanent specific “chaperone-like” protein of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 284:12735–12744

    Article  CAS  PubMed  Google Scholar 

  • Fermani S, Sparla F, Falini G, Martelli PL, Casadio R, Pupillo P, Ripamonti A, Trost P (2007) Molecular mechanism of thioredoxin regulation in photosynthetic A2B2-glyceraldehyde-3-phosphate dehydrogenase. Proc Natl Acad Sci USA 104:11109–11114

    Article  CAS  PubMed  Google Scholar 

  • Gardebien F, Thangudu RR, Gontero B, Offmann B (2006) Construction of a 3D model of CP12, a protein linker. J Mol Graph Model 25:186–195

    Article  CAS  PubMed  Google Scholar 

  • Graciet E, Gans P, Wedel N, Lebreton S, Camadro JM, Gontero B (2003a) The small protein CP12: a protein linker for supramolecular complex assembly. Biochemistry 42:8163–8170

    Article  CAS  PubMed  Google Scholar 

  • Graciet E, Lebreton S, Camadro JM, Gontero B (2003b) Characterization of native and recombinant A4 glyceraldehyde-3-phosphate dehydrogenase. Eur J Biochem 270:129–136

    Article  CAS  PubMed  Google Scholar 

  • Graciet E, Lebreton S, 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

    Article  CAS  PubMed  Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Howard TP, Metodiev M, Lloyd JC, Raines CA (2008) Thioredoxin-mediated reversible dissociation of a stromal multiprotein complex in response to changes in light availability. Proc Natl Acad Sci USA 105:4056–4061

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jeffery CJ (1999) Moonlighting proteins. Trends Biochem Sci 24:8–11

    Article  CAS  PubMed  Google Scholar 

  • Kapraun DF (2007) Nuclear DNA content estimates in green algal lineages: chlorophyta and streptophyta. Ann Bot (Lond) 99:677–701

    Article  CAS  Google Scholar 

  • Keeling PJ, Burger G, Durnford DG, Lang BF, Lee RW, Pearlman RE, Roger AJ, Gray MW (2005) The tree of eukaryotes. Trends Ecol Evol 20:670–676

    Article  PubMed  Google Scholar 

  • Lebreton S, Andreescu S, Graciet E, 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

    Article  CAS  PubMed  Google Scholar 

  • Lemieux C, Otis C, Turmel M (2000) Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature 403:649–652

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128

    Article  CAS  PubMed  Google Scholar 

  • Li X, Romero P, Rani M, Dunker AK, Obradovic Z (1999) Predicting protein disorder for N-, C-, and internal regions. Genome Inform Ser Workshop Genome Inform 10:30–40

    CAS  PubMed  Google Scholar 

  • Maberly SC, Courcelle C, Groben R, 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

    Article  CAS  PubMed  Google Scholar 

  • Marri L, Sparla F, Pupillo P, Trost P (2005a) Co-ordinated gene expression of photosynthetic glyceraldehyde-3-phosphate dehydrogenase, phosphoribulokinase, and CP12 in Arabidopsis thaliana. J Exp Bot 56:73–80

    CAS  PubMed  Google Scholar 

  • Marri L, Trost P, Pupillo P, Sparla F (2005b) Reconstitution and properties of the recombinant glyceraldehyde-3-phosphate dehydrogenase/CP12/phosphoribulokinase supramolecular complex of Arabidopsis. Plant Physiol 139:1433–1443

    Article  CAS  PubMed  Google Scholar 

  • Marri L, Zaffagnini M, Collin V, Issakidis-Bourguet E, Lemaire SD, Pupillo P, Sparla F, Miginiac-Maslow M, 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

    Article  CAS  PubMed  Google Scholar 

  • Matsuzaki M et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pohlmeyer K, Paap BK, Soll J, 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  CAS  PubMed  Google Scholar 

  • Raines CA, Paul MJ (2006) Products of leaf primary carbon metabolism modulate the developmental programme determining plant morphology. J Exp Bot 57:1857–1862

    Article  CAS  PubMed  Google Scholar 

  • Robbens S, Petersen J, Brinkmann H, Rouze P, Van de Peer Y (2007) Unique regulation of the Calvin cycle in the ultrasmall green alga Ostreococcus. J Mol Evol 64:601–604

    Article  CAS  PubMed  Google Scholar 

  • Romero P, Obradovic Z, Dunker K (1997) Sequence data analysis for long disordered regions prediction in the calcineurin family. Genome Inform Ser Workshop Genome Inform 8:110–124

    CAS  PubMed  Google Scholar 

  • Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK (2001) Sequence complexity of disordered protein. Proteins 42:38–48

    Article  CAS  PubMed  Google Scholar 

  • Rumpho ME, Pochareddya S, Worfula JM, Summerb J, Bhattacharyac D, Pelletreaua KN, Tylerd MS, Leee J, Manhartf JR, Soulea KM (2009) Molecular characterization of the Calvin cycle enzyme phosphoribulokinase in the stramenopile alga Vaucheria litorea and the plastid hosting mollusc Elysia chlorotica. Mol Plant 2:1384–1396

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schneider TD, Stephens RM (1990) Sequence logos: a new way to display consensus sequences. Nucl Acids Res 18:6097–6100

    Article  CAS  PubMed  Google Scholar 

  • Shaw J, Renzaglia K (2004) Phylogeny and diversification of bryophytes. Am J Bot 91:1557–1581

    Article  Google Scholar 

  • Singh P, Kaloudas D, Raines CA (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

    Article  CAS  PubMed  Google Scholar 

  • Smith RF, Wiese BA, Wojzynski MK, Davison DB, Worley KC (1996) BCM Search Launcher—an integrated interface to molecular biology data base search and analysis services available on the World Wide Web. Genome Res 6:454–462

    Article  CAS  PubMed  Google Scholar 

  • Tamoi M, Miyazaki T, Fukamizo T, 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

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527–533

    Article  CAS  PubMed  Google Scholar 

  • Tompa P, Szasz C, Buday L (2005) Structural disorder throws new light on moonlighting. Trends Biochem Sci 30:484–489

    Article  CAS  PubMed  Google Scholar 

  • Trost P, Fermani S, Marri L, Zaffagnini M, Falini G, Scagliarini S, Pupillo P, Sparla F (2006) Thioredoxin-dependent regulation of photosynthetic glyceraldehyde-3-phosphate dehydrogenase: autonomous vs. CP12-dependent mechanisms. Photosynth Res 89:1–13

    Article  Google Scholar 

  • Uversky VN (2002) What does it mean to be natively unfolded? Eur J Biochem 269:2–12

    Article  CAS  PubMed  Google Scholar 

  • Wedel N, 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  CAS  PubMed  Google Scholar 

  • Wedel N, Soll J, Paap BK (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  CAS  PubMed  Google Scholar 

  • Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Michael W. Gray (Dalhousie University) for his help in analysing unpublished data from the Protist EST Program. This research was partially funded by the Franco-British Research Partnership Programme Alliance funded by the British Council and Egide.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brigitte Gontero.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Groben, R., Kaloudas, D., Raines, C.A. et al. 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 (2010). https://doi.org/10.1007/s11120-010-9542-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-010-9542-z

Keywords

Navigation