{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T18:22:22Z","timestamp":1784744542292,"version":"3.55.0"},"reference-count":95,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2022,7,28]],"date-time":"2022-07-28T00:00:00Z","timestamp":1658966400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the Minist\u00e8re de la Recherche, de l\u2019Enseignement sup\u00e9rieur et de l\u2019Innovation","award":["ANR-21-CE20-0029"],"award-info":[{"award-number":["ANR-21-CE20-0029"]}]},{"name":"the Centre National de la Recherche Scientifique (CNRS)","award":["ANR-21-CE20-0029"],"award-info":[{"award-number":["ANR-21-CE20-0029"]}]},{"name":"Aix-Marseille Universit\u00e9","award":["ANR-21-CE20-0029"],"award-info":[{"award-number":["ANR-21-CE20-0029"]}]},{"name":"Agence Nationale de la Recherche","award":["ANR-21-CE20-0029"],"award-info":[{"award-number":["ANR-21-CE20-0029"]}]},{"name":"the Federation of European Biochemical Societies","award":["ANR-21-CE20-0029"],"award-info":[{"award-number":["ANR-21-CE20-0029"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biomolecules"],"abstract":"<jats:p>The chloroplast protein CP12, which is widespread in photosynthetic organisms, belongs to the intrinsically disordered proteins family. This small protein (80 amino acid residues long) presents a bias in its composition; it is enriched in charged amino acids, has a small number of hydrophobic residues, and has a high proportion of disorder-promoting residues. More precisely, CP12 is a conditionally disordered proteins (CDP) dependent upon the redox state of its four cysteine residues. During the day, reducing conditions prevail in the chloroplast, and CP12 is fully disordered. Under oxidizing conditions (night), its cysteine residues form two disulfide bridges that confer some stability to some structural elements. Like many CDPs, CP12 plays key roles, and its redox-dependent conditional disorder is important for the main function of CP12: the dark\/light regulation of the Calvin-Benson-Bassham (CBB) cycle responsible for CO2 assimilation. Oxidized CP12 binds to glyceraldehyde-3-phosphate dehydrogenase and phosphoribulokinase and thereby inhibits their activity. However, recent studies reveal that CP12 may have other functions beyond the CBB cycle regulation. In this review, we report the discovery of this protein, its features as a disordered protein, and the many functions this small protein can have.<\/jats:p>","DOI":"10.3390\/biom12081047","type":"journal-article","created":{"date-parts":[[2022,7,28]],"date-time":"2022-07-28T20:49:28Z","timestamp":1659041368000},"page":"1047","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["A Trajectory of Discovery: Metabolic Regulation by the Conditionally Disordered Chloroplast Protein, CP12"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0917-3074","authenticated-orcid":false,"given":"Cassy","family":"G\u00e9rard","sequence":"first","affiliation":[{"name":"Aix Marseille Univ, CNRS, BIP, UMR 7281, IMM, FR3479, 31 Chemin J. Aiguier, CEDEX 9, 13 402 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4848-9418","authenticated-orcid":false,"given":"Fr\u00e9d\u00e9ric","family":"Carri\u00e8re","sequence":"additional","affiliation":[{"name":"Aix Marseille Univ, CNRS, BIP, UMR 7281, IMM, FR3479, 31 Chemin J. Aiguier, CEDEX 9, 13 402 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"V\u00e9ronique","family":"Receveur-Br\u00e9chot","sequence":"additional","affiliation":[{"name":"Aix Marseille Univ, CNRS, BIP, UMR 7281, IMM, FR3479, 31 Chemin J. Aiguier, CEDEX 9, 13 402 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0639-2642","authenticated-orcid":false,"given":"H\u00e9l\u00e8ne","family":"Launay","sequence":"additional","affiliation":[{"name":"Aix Marseille Univ, CNRS, BIP, UMR 7281, IMM, FR3479, 31 Chemin J. Aiguier, CEDEX 9, 13 402 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1731-712X","authenticated-orcid":false,"given":"Brigitte","family":"Gontero","sequence":"additional","affiliation":[{"name":"Aix Marseille Univ, CNRS, BIP, UMR 7281, IMM, FR3479, 31 Chemin J. Aiguier, CEDEX 9, 13 402 Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/bs.pmbts.2019.05.003","article-title":"Protein Intrinsic Disorder and Structure-Function Continuum","volume":"166","author":"Uversky","year":"2019","journal-title":"Prog. Mol. Biol. Transl. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1110\/ps.4210102","article-title":"Natively Unfolded Proteins: A Point Where Biology Waits for Physics","volume":"11","author":"Uversky","year":"2002","journal-title":"Protein Sci. Publ. Protein Soc."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Yruela, I., and Contreras-Moreira, B. (2013). Genetic Recombination Is Associated with Intrinsic Disorder in Plant Proteomes. BMC Genom., 14.","DOI":"10.1186\/1471-2164-14-772"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1007\/978-1-0716-0524-0_26","article-title":"Determining the Protective Activity of IDPs Under Partial Dehydration and Freeze-Thaw Conditions","volume":"2141","author":"Reyes","year":"2020","journal-title":"Methods Mol. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"6805","DOI":"10.1038\/s41598-018-24772-7","article-title":"Exploring Intrinsically Disordered Proteins in Chlamydomonas reinhardtii","volume":"8","author":"Zhang","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1111\/febs.13814","article-title":"The Intriguing CP12-like Tail of Adenylate Kinase 3 from Chlamydomonas reinhardtii","volume":"283","author":"Schramm","year":"2016","journal-title":"FEBS J."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"e1253526","DOI":"10.1080\/21690707.2016.1253526","article-title":"Comparison of the Intrinsic Disorder Propensities of the RuBisCO Activase Enzyme from the Motile and Non-Motile Oceanic Green Microalgae","volume":"4","author":"Sena","year":"2016","journal-title":"Intrinsically Disord. Proteins"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"108070","DOI":"10.1016\/j.abb.2019.108070","article-title":"Orchestration of Algal Metabolism by Protein Disorder","volume":"672","author":"Launay","year":"2019","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1042\/BST20120097","article-title":"An Intrinsically Disordered Protein, CP12: Jack of All Trades and Master of the Calvin Cycle","volume":"40","author":"Gontero","year":"2012","journal-title":"Biochem. Soc. Trans."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"5958","DOI":"10.1073\/pnas.1522866113","article-title":"A Repeat Protein Links Rubisco to Form the Eukaryotic Carbon-Concentrating Organelle","volume":"113","author":"Mackinder","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"6303","DOI":"10.1038\/s41467-020-20132-0","article-title":"Condensation of Rubisco into a Proto-Pyrenoid in Higher Plant Chloroplasts","volume":"11","author":"Atkinson","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1480","DOI":"10.1038\/s41477-020-00811-y","article-title":"The Structural Basis of Rubisco Phase Separation in the Pyrenoid","volume":"6","author":"He","year":"2020","journal-title":"Nat. Plants"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5076","DOI":"10.1038\/s41467-018-07624-w","article-title":"The Phase Separation Underlying the Pyrenoid-Based Microalgal Rubisco Supercharger","volume":"9","author":"Wunder","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.cell.2017.08.044","article-title":"A Spatial Interactome Reveals the Protein Organization of the Algal CO2-Concentrating Mechanism","volume":"171","author":"Mackinder","year":"2017","journal-title":"Cell"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1007\/BF00020493","article-title":"CP12: A Small Nuclear-Encoded Chloroplast Protein Provides Novel Insights into Higher-Plant GAPDH Evolution","volume":"32","author":"Pohlmeyer","year":"1996","journal-title":"Plant Mol. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"10479","DOI":"10.1073\/pnas.94.19.10479","article-title":"CP12 Provides a New Mode of Light Regulation of Calvin Cycle Activity in Higher\u2009Plants","volume":"94","author":"Wedel","year":"1997","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1111\/j.1432-1033.1988.tb14018.x","article-title":"A Functional Five-Enzyme Complex of Chloroplasts Involved in the Calvin Cycle","volume":"173","author":"Gontero","year":"1988","journal-title":"Eur. J. Biochem."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1075","DOI":"10.1111\/j.1432-1033.1993.tb18339.x","article-title":"Structural and Functional Properties of a Multi-Enzyme Complex from Spinach Chloroplasts. II: Modulation of the Kinetic Properties of Enzymes in the Aggregated State","volume":"217","author":"Gontero","year":"1993","journal-title":"Eur. J. Biochem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1111\/j.1432-1033.1991.tb15973.x","article-title":"Thioredoxin Activation of Phosphoribulokinase in a Chloroplast Multi-Enzyme Complex","volume":"197","author":"Rault","year":"1991","journal-title":"Eur. J. Biochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1111\/j.1432-1033.1997.00078.x","article-title":"Memory and Imprinting Effects in Multienzyme Complexes","volume":"246","author":"Avilan","year":"1997","journal-title":"Eur. J. Biochem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1111\/j.1432-1033.1997.0296a.x","article-title":"Information Transfer in Multienzyme Complexes.2. The Role of Arg64 of Chlamydomonas reinhardtii Phosphoribulokinase in the Information Transfer between Glyceraldehyde-3-Phosphate Dehydrogenase and Phosphoribulokinase","volume":"250","author":"Avilan","year":"1997","journal-title":"Eur. J. Biochem."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1111\/j.1432-1033.1997.t01-2-00085.x","article-title":"Memory and Imprinting Effects in Multienzyme Complexes.2. Kinetics of the Bienzyme Complex from Chlamydomonas reinhardtii and Hysteretic Activation of Chloroplast Oxidized Phosphoribulokinase","volume":"246","author":"Lebreton","year":"1997","journal-title":"Eur. J. Biochem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1111\/j.1432-1033.1997.0286a.x","article-title":"Information Transfer in Multienzyme Complexes.1. Thermodynamics of Conformational Constraints and Memory Effects in the Bienzyme Glyceraldehyde-3-Phosphate-Dehydrogenase-Phosphoribulokinase Complex of Chlamydomonas reinhardtii Chloroplasts","volume":"250","author":"Lebreton","year":"1997","journal-title":"Eur. J. Biochem."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1046\/j.1432-1033.2003.03372.x","article-title":"Characterization of Native and Recombinant A4 Glyceraldehyde 3-Phosphate Dehydrogenase. Kinetic Evidence for Confromation Changes upon Association with the Small Protein CP12","volume":"270","author":"Graciet","year":"2003","journal-title":"Eur. J. Biochem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"8163","DOI":"10.1021\/bi034474x","article-title":"The Small Protein CP12: A Protein Linker for Supramolecular Complex Assembly","volume":"42","author":"Graciet","year":"2003","journal-title":"Biochemistry"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"6743","DOI":"10.1074\/jbc.M106401200","article-title":"Striking Conformational Change Suspected within the Phosphoribulokinase Dimer Induced by Interaction with GAPDH","volume":"277","author":"Mouche","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"12697","DOI":"10.1074\/jbc.M111121200","article-title":"Thermodynamic Analysis of the Emergence of New Regulatory Properties in a Phosphoribulokinase-Glyceraldehyde 3-Phosphate Dehydrogenase Complex","volume":"277","author":"Graciet","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"9699","DOI":"10.1073\/pnas.95.16.9699","article-title":"Evolutionary Conserved Light Regulation of Calvin Cycle Activity by NADPH-Mediated Reversible Phosphoribulokinase\/CP12\/Glyceraldehyde-3-Phosphate Dehydrogenase Complex Dissociation","volume":"95","author":"Wedel","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"5617","DOI":"10.1046\/j.1432-1033.2002.03269.x","article-title":"Co-Existence of Two Regulatory NADP-Glyceraldehyde 3-P Dehydrogenase Complexes in Higher Plant Chloroplasts","volume":"269","author":"Scheibe","year":"2002","journal-title":"Eur. J. Biochem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"3799","DOI":"10.1093\/jxb\/err057","article-title":"Inter-Species Variation in the Oligomeric States of the Higher Plant Calvin Cycle Enzymes Glyceraldehyde-3-Phosphate Dehydrogenase and Phosphoribulokinase","volume":"62","author":"Howard","year":"2011","journal-title":"J. Exp. Bot."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1111\/j.1432-1033.1991.tb16496.x","article-title":"Properties of Two High-Molecular-Mass Forms of Glyceraldehyde-3-Phosphate Dehydrogenase from Spinach Leaf, One of Which Also Possesses Latent Phosphoribulokinase Activity","volume":"202","author":"Clasper","year":"1991","journal-title":"Eur. J. Biochem."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1104\/pp.66.1.34","article-title":"Activation of Glyceraldehyde-Phosphate Dehydrogenase (NADP) and Phosphoribulokinase in Phaseolus vulgaris Leaf Extracts Involves the Dissociation of Oligomers","volume":"66","author":"Kemble","year":"1980","journal-title":"Plant Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.1074\/jbc.M705650200","article-title":"Spontaneous Assembly of Photosynthetic Supramolecular Complexes as Mediated by the Intrinsically Unstructured Protein CP12","volume":"283","author":"Marri","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1002\/rcm.6442","article-title":"Exploration of CP12 Conformational Changes and of Quaternary Structural Properties Using Electrospray Ionization Traveling Wave Ion Mobility Mass Spectrometry","volume":"27","author":"Kaaki","year":"2013","journal-title":"Rapid Commun. Mass Spectrom."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2881","DOI":"10.1021\/bi1020259","article-title":"Molecular Mechanism of NADPH-Glyceraldehyde-3-Phosphate Dehydrogenase Regulation through the C-Terminus of CP12 in Chlamydomonas reinhardtii","volume":"50","author":"Erales","year":"2011","journal-title":"Biochemistry"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1006\/jmbi.1999.3110","article-title":"Intrinsically Unstructured Proteins: Re-Assessing the Protein Structure-Function Paradigm","volume":"293","author":"Wright","year":"1999","journal-title":"J. Mol. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/S0959-440X(02)00289-0","article-title":"Coupling of Folding and Binding for Unstructured Proteins","volume":"12","author":"Dyson","year":"2002","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1016\/S0968-0004(02)02169-2","article-title":"Intrinsically Unstructured Proteins","volume":"27","author":"Tompa","year":"2002","journal-title":"Trends Biochem. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3206","DOI":"10.1111\/febs.12854","article-title":"Conformational Modulation and Hydrodynamic Radii of CP12 Protein and Its Complexes Probed by Fluorescence Correlation Spectroscopy","volume":"281","author":"Moparthi","year":"2014","journal-title":"FEBS J."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Vacic, V., Uversky, V.N., Dunker, A.K., and Lonardi, S. (2007). Composition Profiler: A Tool for Discovery and Visualization of Amino Acid Composition Differences. BMC Bioinform., 8.","DOI":"10.1186\/1471-2105-8-211"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.bbrc.2016.06.014","article-title":"Absence of Residual Structure in the Intrinsically Disordered Regulatory Protein CP12 in Its Reduced State","volume":"477","author":"Launay","year":"2016","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/j.bbrc.2015.01.135","article-title":"FRET Analysis of CP12 Structural Interplay by GAPDH and PRK","volume":"458","author":"Moparthi","year":"2015","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.jmgm.2005.12.003","article-title":"Construction of a 3D Model of CP12, a Protein Linker","volume":"25","author":"Gardebien","year":"2006","journal-title":"J. Mol. Graph. Model."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1218","DOI":"10.1016\/j.jmb.2018.02.020","article-title":"Cryptic Disorder Out of Disorder: Encounter between Conditionally Disordered CP12 and Glyceraldehyde-3-Phosphate Dehydrogenase","volume":"430","author":"Launay","year":"2018","journal-title":"J. Mol. Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"55","DOI":"10.2174\/138920312799277901","article-title":"How Random Are Intrinsically Disordered Proteins? A Small Angle Scattering Perspective","volume":"13","author":"Durand","year":"2012","journal-title":"Curr. Protein Pept. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1016\/j.sbi.2013.02.006","article-title":"The Roles of Conditional Disorder in Redox Proteins","volume":"23","author":"Reichmann","year":"2013","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"20984","DOI":"10.1073\/pnas.1906722116","article-title":"Structural Basis of Light-Induced Redox Regulation in the Calvin-Benson Cycle in Cyanobacteria","volume":"116","author":"McFarlane","year":"2019","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1556","DOI":"10.1105\/tpc.19.00642","article-title":"Photosynthetic Phosphoribulokinase Structures: Enzymatic Mechanisms and the Redox Regulation of the Calvin-Benson-Bassham Cycle","volume":"32","author":"Yu","year":"2020","journal-title":"Plant Cell"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1846","DOI":"10.1016\/j.str.2011.08.016","article-title":"Structure Basis for the Regulation of Glyceraldehyde-3-Phosphate Dehydrogenase Activity via the Intrinsically Disordered Protein CP12","volume":"19","author":"Matsumura","year":"2011","journal-title":"Structure"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s11120-006-9099-z","article-title":"Thioredoxin-Dependent Regulation of Photosynthetic Glyceraldehyde-3-Phosphate Dehydrogenase: Autonomous vs. CP12-Dependent Mechanisms","volume":"89","author":"Trost","year":"2006","journal-title":"Photosynth. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e1800070","DOI":"10.1002\/pmic.201800070","article-title":"Large-Scale Analysis of Redox-Sensitive Conditionally Disordered Protein Regions Reveals Their Widespread Nature and Key Roles in High-Level Eukaryotic Processes","volume":"19","author":"Reichmann","year":"2019","journal-title":"Proteomics"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/bs.pmbts.2020.06.001","article-title":"Disorder and Cysteines in Proteins: A Design for Orchestration of Conformational See-Saw and Modulatory Functions","volume":"174","author":"Bhopatkar","year":"2020","journal-title":"Prog. Mol. Biol. Transl. Sci."},{"key":"ref_53","first-page":"9","article-title":"The CP12 Protein Family: A Thioredoxin-Mediated Metabolic Switch?","volume":"5","author":"Howard","year":"2014","journal-title":"Front. Plant Sci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1007\/s11120-010-9542-z","article-title":"Comparative Sequence Analysis of CP12, a Small Protein Involved in the Formation of a Calvin Cycle Complex in Photosynthetic Organisms","volume":"103","author":"Groben","year":"2010","journal-title":"Photosynth. Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"2994","DOI":"10.1039\/c2mb25244a","article-title":"CP12 Residues Involved in the Formation and Regulation of the Glyceraldehyde-3-Phosphate Dehydrogenase\u2013CP12\u2013Phosphoribulokinase Complex in Chlamydomonas reinhardtii","volume":"8","author":"Avilan","year":"2012","journal-title":"Mol. Biosyst."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1359","DOI":"10.1093\/pcp\/pcm108","article-title":"Redox Regulation of Chloroplast Enzymes in Galdieria sulphuraria in View of Eukaryotic Evolution","volume":"48","author":"Oesterhelt","year":"2007","journal-title":"Plant Cell Physiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1111\/j.1365-313X.2005.02391.x","article-title":"The Calvin Cycle in Cyanobacteria Is Regulated by CP12 via the NAD(H)\/NADP(H) Ratio under Light\/Dark Conditions","volume":"42","author":"Tamoi","year":"2005","journal-title":"Plant J."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1104\/pp.112.210542","article-title":"Comparative Analysis of 126 Cyanobacterial Genomes Reveals Evidence of Functional Diversity among Homologs of the Redox-Regulated CP12 Protein","volume":"161","author":"Stanley","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1111\/nph.12820","article-title":"Glyceraldehyde-3-Phosphate Dehydrogenase Is Regulated by Ferredoxin-NADP Reductase in the Diatom Asterionella formosa","volume":"203","author":"Mekhalfi","year":"2014","journal-title":"New Phytol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1111\/j.1529-8817.2007.00409.x","article-title":"Regulation of Phosphoribulokinase and Glyceraldehyde 3-Phosphate Dehydrogenase in a Freshwater Diatom, Asterionella formosa","volume":"43","author":"Boggetto","year":"2007","journal-title":"J. Phycol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/s12964-021-00718-x","article-title":"A New Type of Flexible CP12 Protein in the Marine Diatom Thalassiosira pseudonana","volume":"19","author":"Shao","year":"2021","journal-title":"Cell Commun. Signal. CCS"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.protis.2006.02.003","article-title":"The Regulation of Carbon and Nutrient Assimilation in Diatoms Is Significantly Different from Green Algae","volume":"157","author":"Wilhelm","year":"2006","journal-title":"Protist"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1134","DOI":"10.1039\/C5MB00035A","article-title":"Phosphoribulokinase from Chlamydomonas reinhardtii: A Benson-Calvin Cycle Enzyme Enslaved to Its Cysteine Residues","volume":"11","author":"Remy","year":"2015","journal-title":"Mol. Biosyst."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"E757","DOI":"10.1073\/pnas.1102164108","article-title":"Phage Auxiliary Metabolic Genes and the Redirection of Cyanobacterial Host Carbon Metabolism","volume":"108","author":"Thompson","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"2495","DOI":"10.1111\/febs.14494","article-title":"Interaction between Adenylate Kinase 3 and Glyceraldehyde-3-phosphate Dehydrogenase from Chlamydomonas reinhardtii","volume":"285","author":"Zhang","year":"2018","journal-title":"FEBS J."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1016\/j.jplph.2010.02.008","article-title":"In Vitro Characterization of Arabidopsis CP12 Isoforms Reveals Common Biochemical and Molecular Properties","volume":"167","author":"Marri","year":"2010","journal-title":"J. Plant Physiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1007\/s00239-006-0159-y","article-title":"Unique Regulation of the Calvin Cycle in the Ultrasmall Green Alga Ostreococcus","volume":"64","author":"Robbens","year":"2007","journal-title":"J. Mol. Evol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"D969","DOI":"10.1093\/nar\/gkn654","article-title":"PPDB, the Plant Proteomics Database at Cornell","volume":"37","author":"Sun","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.plaphy.2020.11.022","article-title":"Effect of Sugar Feedback Regulation on Major Genes and Proteins of Photosynthesis in Sugarcane Leaves","volume":"158","author":"Marquardt","year":"2021","journal-title":"Plant Physiol. Biochem. PPB"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.pbiomolbio.2008.05.007","article-title":"Intrinsic Disorder in Scaffold Proteins: Getting More from Less","volume":"98","author":"Cortese","year":"2008","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1093\/mp\/ssn061","article-title":"Prompt and Easy Activation by Specific Thioredoxins of Calvin Cycle Enzymes of Arabidopsis thaliana Associated in the GAPDH\/CP12\/PRK Supramolecular Complex","volume":"2","author":"Marri","year":"2009","journal-title":"Mol. Plant"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"E8296","DOI":"10.1073\/pnas.1808284115","article-title":"Thioredoxin-Like2\/2-Cys Peroxiredoxin Redox Cascade Supports Oxidative Thiol Modulation in Chloroplasts","volume":"115","author":"Yoshida","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"9447","DOI":"10.1074\/jbc.275.13.9447","article-title":"Thioredoxin Activation of Phosphoribulokinase in a Bi-Enzyme Complex from Chlamydomonas reinhardtii Chloroplasts","volume":"275","author":"Avilan","year":"2000","journal-title":"J. Biol. Chem."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1433","DOI":"10.1104\/pp.105.068445","article-title":"Reconstitution and Properties of the Recombinant Glyceraldehyde-3-Phosphate Dehydrogenase\/CP12\/Phosphoribulokinase Supramolecular Complex of Arabidopsis","volume":"139","author":"Marri","year":"2005","journal-title":"Plant Physiol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1146\/annurev.pp.46.060195.002305","article-title":"Light-Regulated Transcription","volume":"46","author":"Terzaghi","year":"1995","journal-title":"Annu. Rev. Plant Physiol Plant Mol. Biol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2285","DOI":"10.1093\/jxb\/erx084","article-title":"Arabidopsis CP12 Mutants Have Reduced Levels of Phosphoribulokinase and Impaired Function of the Calvin-Benson Cycle","volume":"68","author":"Lawson","year":"2017","journal-title":"J. Exp. Bot."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"G\u00e9rard, C., Lebrun, R., Lemesle, E., Avilan, L., Chang, K.S., Jin, E., Carri\u00e8re, F., Gontero, B., and Launay, H. (2022). Reduction in Phosphoribulokinase Amount and Re-Routing Metabolism in Chlamydomonas reinhardtii CP12 Mutants. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23052710"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1104\/pp.111.183806","article-title":"Antisense Suppression of the Small Chloroplast Protein CP12 in Tobacco Alters Carbon Partitioning and Severely Restricts Growth","volume":"157","author":"Howard","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"2026","DOI":"10.4161\/psb.6.12.18055","article-title":"Antisense Suppression of the Small Chloroplast Protein CP12 in Tobacco: A Transcriptional Viewpoint","volume":"6","author":"Howard","year":"2011","journal-title":"Plant Signal. Behav."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1319","DOI":"10.3389\/fpls.2018.01319","article-title":"Chloroplast Protein 12 Expression Alters Growth and Chilling Tolerance in Tropical Forage Stylosanthes guianensis (Aublet) Sw","volume":"9","author":"Li","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.1111\/j.1742-4658.2008.06284.x","article-title":"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","volume":"275","author":"Erales","year":"2008","journal-title":"FEBS J."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1038\/s41586-022-04662-9","article-title":"Alternative Photosynthesis Pathways Drive the Algal CO2-Concentrating Mechanism","volume":"605","author":"Burlacot","year":"2022","journal-title":"Nature"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1016\/j.tplants.2021.11.007","article-title":"Physiological Functions of Malate Shuttles in Plants and Algae","volume":"27","author":"Dao","year":"2022","journal-title":"Trends Plant Sci."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"42333","DOI":"10.1038\/srep42333","article-title":"Responses of the Marine Diatom Thalassiosira pseudonana to Changes in CO2 Concentration: A Proteomic Approach","volume":"7","author":"Clement","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Tamoi, M., and Shigeoka, S. (2021). CP12 Is Involved in Protection against High Light Intensity by Suppressing the ROS Generation in Synechococcus elongatus PCC7942. Plants, 10.","DOI":"10.3390\/plants10071275"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"7141","DOI":"10.1073\/pnas.1806668115","article-title":"Structural and Functional Insights into the Unique CBS-CP12 Fusion Protein Family in Cyanobacteria","volume":"115","author":"Hackenberg","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.biochi.2013.10.018","article-title":"CP12-Mediated Protection of Calvin-Benson Cycle Enzymes from Oxidative Stress","volume":"97","author":"Marri","year":"2014","journal-title":"Biochimie"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"12735","DOI":"10.1074\/jbc.M808254200","article-title":"CP12 from Chlamydomonas reinhardtii, a Permanent Specific \u201cChaperone-like\u201d Protein of Glyceraldehyde-3-Phosphate Dehydrogenase","volume":"284","author":"Erales","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"2761","DOI":"10.3389\/fmicb.2018.02761","article-title":"Quantitative Proteomics Reveals Common and Specific Responses of a Marine Diatom Thalassiosira pseudonana to Different Macronutrient Deficiencies","volume":"9","author":"Chen","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1111\/jac.12529","article-title":"Leaf Transcriptome Analysis of Lancaster versus Other Heterotic Groups\u2019 Maize Inbred Lines Revealed Different Regulation of Cold-Responsive Genes","volume":"208","author":"Bozic","year":"2022","journal-title":"J. Agron. Crop Sci."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"2950","DOI":"10.1021\/bi802072u","article-title":"Metal Binding Kinetics of Bi-Histidine Sites Used in Psi Analysis: Evidence of High-Energy Protein Folding Intermediates","volume":"48","author":"Bosco","year":"2009","journal-title":"Biochemistry"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"3379","DOI":"10.1002\/rcm.2192","article-title":"Mass Spectrometric Analysis of the Interactions between CP12, a Chloroplast Protein, and Metal Ions: A Possible Regulatory Role within a PRK\/GAPDH\/CP12 Complex","volume":"19","author":"Delobel","year":"2005","journal-title":"Rapid Commun. Mass Spectrom."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"7185","DOI":"10.1021\/bi972827k","article-title":"Prion Protein Selectively Binds Copper(II) Ions","volume":"37","author":"Safar","year":"1998","journal-title":"Biochemistry"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1104\/pp.117.4.1227","article-title":"Identification of a Functional Homolog of the Yeast Copper Homeostasis Gene ATX1 from Arabidopsis","volume":"117","author":"Himelblau","year":"1998","journal-title":"Plant Physiol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"530","DOI":"10.3390\/plants2030530","article-title":"Identification of CP12 as a Novel Calcium-Binding Protein in Chloroplasts","volume":"2","author":"Rocha","year":"2013","journal-title":"Plants"}],"container-title":["Biomolecules"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2218-273X\/12\/8\/1047\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:58:24Z","timestamp":1760140704000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2218-273X\/12\/8\/1047"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,28]]},"references-count":95,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["biom12081047"],"URL":"https:\/\/doi.org\/10.3390\/biom12081047","relation":{},"ISSN":["2218-273X"],"issn-type":[{"value":"2218-273X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,28]]}}}