Abstract
Glyceraldehyde-3-phosphate dehydrogenase (GapAB) and CP12 are two major players in controlling the inactivation of the Calvin cycle in land plants at night. GapB originated from a GapA gene duplication and differs from GapA by the presence of a specific C-terminal extension that was recruited from CP12. While GapA and CP12 are assumed to be generally present in the Plantae (glaucophytes, red and green algae, and plants), up to now GapB was exclusively found in Streptophyta, including the enigmatic green alga Mesostigma viride. However, here we show that two closely related prasinophycean green algae, Ostreococcus tauri and Ostreococcus lucimarinus, also possess a GapB gene, while CP12 is missing. This remarkable finding either antedates the GapA/B gene duplication or indicates a lateral recruitment. Moreover, Ostreococcus is the first case where the crucial CP12 function may be completely replaced by GapB-mediated GapA/B aggregation.
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Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86
Bassham JA (2003) Mapping the carbon reduction cycle: a personal retrospective. Photosynth Res 76:35–52
Brinkmann H, van der Giezen M, Zhou Y, Poncelin de Raucourt G, Philippe H (2005) An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. Syst Biol 54:743–757
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Cerff R (1979) Quaternary structure of higher plant glyceraldehyde-3-phosphate dehydrogenases. Eur J Biochem 94:243–247
Courties C, Vaquer A, Troussellier M, Lautier J, Chre´tiennot-Dinet MJ, Neveux J, Machado MC, Claustre H (1994) Smallest eukaryotic organism. Nature 370:255
Courties C, Perasso R, Chrétiennot-Dinet KJ, Guoy M, Guillou L, Troussellier M (1998) Phylogenetic analysis and genome size of Ostreococcus tauri (Chlorophyta, Prasinophyceae). J Phycol 34:844–849
Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y, Moreau H (2006) From the cover: genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103:11647–11652
Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 40:783–791
Figge RM, Cerff R (2001) GAPDH gene diversity in spirochetes: a paradigm for genetic promiscuity. Mol Biol Evol 18:2240–2249
Graham LE, Wilcox LW (2000) Green algae I-introduction and prasinophyceans. In: Graham LE, Wilcox LW (eds.). Algae, Upper Saddle River, Prentice Hall, pp 397–419
Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18
Klein U (1986) Compartmentation of glycolysis and of the oxidative pentose-phosphate pathway in Chlamydomonas reinhardtii. Planta 167:81–86
Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: How much, what happens, and why? Plant Physiol 118:9–17
Michels AK, Wedel N, Kroth PG (2005) Diatom plastids possess a phosphoribulokinase with an altered regulation and no oxidative pentose phosphate pathway. Plant Physiol 137:911–920
Petersen J, Teich R, Becker B, Cerff R, Brinkmann H (2006) The GapA/B gene duplication marks the origin of Streptophyta (charophytes and land plants). Mol Biol Evol 23:1109–1118
Philippe H (1993) MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Res 22:5264–5272
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
Qian Q, Keeling PJ (2001) Diplonemid glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and prokaryote-to-eukaryote lateral gene transfer. Protist 152:193–201
Rodríguez-Ezpeleta N, Philippe H, Brinkmann H, Becker B, Melkonian M (2007) Phylogenetic analyses of nuclear, mitochondrial, and plastid multi-gene datasets support the placement of Mesostigma in the Streptophyta. Mol Biol Evol 24:723–731
Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16:944–945
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
Schnarrenberger C, Flechner A, Martin W (1995) enzymatic evidence for a complete oxidative pentose phosphate pathway in chloroplasts and an incomplete pathway in the cytosol of spinach leaves. Plant Physiol 108:609–614
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
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
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
Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818
Acknowledgments
The authors would like to thank Igor Grigoriev, Brian Palenik, and the JGI for the prior access to the Ostreococcus lucimarinus data. S.R. is indebted to the Institute for the Promotion of Innovation by Science and Technology in Flanders for a predoctoral fellowship. The authors also want to thank two anonymous reviewers for careful reading of the manuscript and constructive criticisms.
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Steven Robbens, Jörn Petersen contributed equally to this work.
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Robbens, S., Petersen, J., Brinkmann, H. et al. Unique Regulation of the Calvin Cycle in the Ultrasmall Green Alga Ostreococcus . J Mol Evol 64, 601–604 (2007). https://doi.org/10.1007/s00239-006-0159-y
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DOI: https://doi.org/10.1007/s00239-006-0159-y