Orchestration of algal metabolism by protein disorder
Open accessAbstract
Intrinsically disordered proteins (IDPs) are proteins that provide many functional advantages in a large number of metabolic and signalling pathways. Because of their high flexibility that endows them with pressure-, heat- and acid-resistance, IDPs are valuable metabolic regulators that help algae to cope with extreme conditions of pH, temperature, pressure and light. They have, however, been overlooked in these organisms. In this review, we present some well-known algal IDPs, including the conditionally disordered CP12, a protein involved in the regulation of CO 2 assimilation, as probably the best known example, whose disorder content is strongly dependent on the redox conditions, and the essential pyrenoid component 1 that serves as a scaffold for ribulose-1, 5-bisphosphate carboxylase/oxygenase. We also describe how some enzymes are regulated by protein regions, called intrinsically disordered regions (IDRs), such as ribulose-1, 5-bisphosphate carboxylase/oxygenase activase, the A 2 B 2 form of glyceraldehyde-3-phosphate dehydrogenase and the adenylate kinase. Several molecular chaperones, which are crucial for cell proteostasis, also display significant disorder propensities such as the algal heat shock proteins HSP33, HSP70 and HSP90. This review confirms the wide distribution of IDPs in algae but highlights that further studies are needed to uncover their full role in orchestrating algal metabolism.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Unlike many structured protein domains, the function of IDPs/IDRs can persist in extreme environmental conditions.
“Unlike many structured protein domains, the function of IDPs/IDRs can persist in extreme environmental conditions.”
From Intrinsically disordered proteins play diverse roles in cell signaling (2022) · cites this paper as [26]
Cites
Primary production of the biosphere: Integrating terrestrial and oceanic components
Field, C. B., Behrenfeld, M. J., Randerson, J. T., & Falkowski, P. (1998) · Science · doi:10.1126/science.281.5374.237 · Cited by 6,371 · see citing works
Intrinsically unstructured proteins and their functions
Dyson, H. J., & Wright, P. E. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1589 · Cited by 3,871 · see citing works
Rothschild, L. J., & Mancinelli, R. L. (2001) · Nature · doi:10.1038/35059215 · Cited by 2,245 · see citing works
Prediction and Functional Analysis of Native Disorder in Proteins from the Three Kingdoms of Life
Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., & Jones, D. T. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.02.002 · Cited by 2,010 · see citing works
Protein Phase Separation: A New Phase in Cell Biology
Boeynaems, S., Alberti, S., Fawzi, N. L., Mittag, T., Polymenidou, M., Rousseau, F., Schymkowitz, J. W. H., Shorter, J., Wolozin, B. L., Bosch, L. V. D., et al. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.02.004 · Cited by 1,954 · see citing works
Pratt, W., & Toft, D. (2003) · Experimental biology and medicine · doi:10.1177/153537020322800201 · Cited by 1,539 · see citing works
Mészáros, B., Erdős, G., & Dosztányi, Z. (2018) · Nucleic Acids Res. · doi:10.1093/nar/gky384 · Cited by 1,376 · see citing works
PONDR-FIT: A meta-predictor of intrinsically disordered amino acids
Xue, B., Dunbrack, R. L., Williams, R. W., Dunker, A. K., & Uversky, V. N. (2010) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2010.01.011 · Cited by 1,208 · see citing works
Mechanism of coupled folding and binding of an intrinsically disordered protein
Sugase, K., Dyson, H. J., & Wright, P. E. (2007) · Nature · doi:10.1038/nature05858 · Cited by 1,040 · see citing works
HOW MANY SPECIES OF ALGAE ARE THERE?
Guiry, M. D. (2012) · Journal of Phycology · doi:10.1111/j.1529-8817.2012.01222.x · Cited by 1,002 · see citing works
THE ORGANIZATION AND REGULATION OF PLANT GLYCOLYSIS
Plaxton, W. C. (1996) · Annual Review of Plant Physiology and Plant Molecular Biology · doi:10.1146/annurev.arplant.47.1.185 · Cited by 946 · see citing works
Introducing Protein Intrinsic Disorder
Habchi, J., Tompa, P., Longhi, S., & Uversky, V. N. (2014) · Chemical Reviews · doi:10.1021/cr400514h · Cited by 744 · see citing works
Marsh, J. A., Singh, V. K., Jia, Z., & Forman-Kay, J. D. (2006) · Protein Science · doi:10.1110/ps.062465306 · Cited by 730 · see citing works
Phase separation in biology; functional organization of a higher order
Mitrea, D. M., & Kriwacki, R. W. (2016) · Cell Communication and Signaling · doi:10.1186/s12964-015-0125-7 · Cited by 723 · see citing works
Alberti, S. (2017) · Current Biology · doi:10.1016/j.cub.2017.08.069 · Cited by 654 · see citing works
Extreme disorder in an ultrahigh-affinity protein complex
Borgia, A., Borgia, M. B., Bugge, K., Kissling, V. M., Heidarsson, P. O., Fernandes, C. B., Sottini, A., Soranno, A., Buholzer, K. J., Nettels, D., et al. (2018) · Nature · doi:10.1038/nature25762 · Cited by 653 · see citing works
Sarmiento, J., & Gruber, N. (2006) · Princeton University Press eBooks · doi:10.2307/j.ctt3fgxqx · Cited by 613 · see citing works
Intrinsically disordered proteins: regulation and disease
Babu, M. M., van der Lee, R., de Groot, N. S., & Gsponer, J. A. (2011) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2011.03.011 · Cited by 597 · see citing works
Xue, B., Dunker, A. K., & Uversky, V. N. (2012) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2012.675145 · Cited by 557 · see citing works
Modulation of Intrinsically Disordered Protein Function by Post-translational Modifications
Bah, A., & Forman-Kay, J. D. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.695056 · Cited by 556 · see citing works
Wandinger, S. K., Richter, K., & Büchner, J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.r800007200 · Cited by 548 · see citing works
Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism
Thompson, L., Zeng, Q., Kelly, L., Huang, K. H., Singer, A. U., Stubbe, J., & Chisholm, S. W. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102164108 · Cited by 514 · see citing works
Membrane heredity and early chloroplast evolution
Cavalier-Smith, T. (2000) · Trends in Plant Science · doi:10.1016/s1360-1385(00)01598-3 · Cited by 482 · see citing works
Assessing protein disorder and induced folding
Receveur‐Brechot, V., Bourhis, J., Uversky, V. N., Canard, B., & Longhi, S. (2005) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.20750 · Cited by 442 · see citing works
The Eukaryotic CO2-Concentrating Organelle Is Liquid-like and Exhibits Dynamic Reorganization
Rosenzweig, E. S. F., Xu, B., Cuellar, L. K., Martínez-Sánchez, A., Schaffer, M., Strauss, M., Cartwright, H. N., Ronceray, P., Plitzko, J. M., Förster, F. G., et al. (2017) · Cell · doi:10.1016/j.cell.2017.08.008 · Cited by 402 · see citing works
Peng, Z., Yan, J. R., Fan, X., Mizianty, M. J., Xue, B., Wang, K., Hu, G., Uversky, V. N., & Kurgan, L. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1661-9 · Cited by 382 · see citing works
Native architecture of the Chlamydomonas chloroplast revealed by in situ cryo-electron tomography
Engel, B. D., Schaffer, M., Cuellar, L. K., Villa, E., Plitzko, J. M., & Baumeister, W. P. (2015) · eLife · doi:10.7554/elife.04889 · Cited by 377 · see citing works
How Random are Intrinsically Disordered Proteins? A Small Angle Scattering Perspective
Receveur‐Brechot, V., & Christiane, D. D. (2012) · Current Protein and Peptide Science · doi:10.2174/138920312799277901 · Cited by 357 · see citing works
Ozenne, V., Bauer, F., Salmon, L., Huang, J., Jensen, M. R., Segard, S., Bernadó, P., Charavay, C., & Blackledge, M. J. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts172 · Cited by 356 · see citing works
Principles of protein structural ensemble determination
Bonomi, M., Heller, G. T., Camilloni, C., & Vendruscolo, M. (2017) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2016.12.004 · Cited by 347 · see citing works
Extremophilic micro-algae and their potential contribution in biotechnology
Varshney, P., Mikulic, P., Vonshak, A., Beardall, J., & Wangikar, P. P. (2014) · Bioresource Technology · doi:10.1016/j.biortech.2014.11.040 · Cited by 330 · see citing works
Sirover, M. A. (2011) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2011.05.010 · Cited by 326 · see citing works
What’s in a name? Why these proteins are intrinsically disordered
Dunker, A. K., Babu, M. M., Barbar, E. J., Blackledge, M. J., Bondos, S. E., Dosztányi, Z., Dyson, H. J., Forman-Kay, J. D., Fuxreiter, M., Gsponer, J. A., et al. (2013) · Intrinsically Disordered Proteins · doi:10.4161/idp.24157 · Cited by 308 · see citing works
Holzinger, A., & Karsten, U. (2013) · Frontiers in Plant Science · doi:10.3389/fpls.2013.00327 · Cited by 307 · see citing works
Patil, A., & Nakamura, H. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.03.003 · Cited by 297 · see citing works
A repeat protein links Rubisco to form the eukaryotic carbon-concentrating organelle
Mackinder, L. C. M., Meyer, M. T., Mettler‐Altmann, T., Chen, V. K., Mitchell, M. C., Caspari, O. D., Rosenzweig, E. S. F., Pallesen, L. J., Reeves, G., Itakura, A. K., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1522866113 · Cited by 278 · see citing works
Lorimer, G. H., & Miziorko, H. M. (1980) · Biochemistry · doi:10.1021/bi00564a027 · Cited by 272 · see citing works
Advances in the Production of High-Value Products by Microalgae
Leu, S., & Boussiba, S. (2014) · Industrial Biotechnology · doi:10.1089/ind.2013.0039 · Cited by 253 · see citing works
(2006) · Choice Reviews Online · doi:10.5860/choice.44-2124 · Cited by 253 · see citing works
Arai, M., Sugase, K., Dyson, H. J., & Wright, P. E. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512799112 · Cited by 250 · see citing works
Ubiquitous healthy diatoms in the deep sea confirm deep carbon injection by the biological pump
Agustı́, S., González-Gordillo, J. I., Vaqué, D., Estrada, M., Cerezo, M. I., Salazar, G., Gasol, J. M., & Duarte, C. M. (2015) · Nature Communications · doi:10.1038/ncomms8608 · Cited by 243 · see citing works
Fuzzy Complexes: A More Stochastic View of Protein Function
Fuxreiter, M., & Tompa, P. (2012) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4614-0659-4_1 · Cited by 240 · see citing works
Carmo-Silva, A. E., & Salvucci, M. E. (2013) · Plant Physiology · doi:10.1104/pp.112.213348 · Cited by 225 · see citing works
Evolutionary and ecological perspectives on carbon acquisition in phytoplankton
Tortell, P. D. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.3.0744 · Cited by 224 · see citing works
Jakob, U., Kriwacki, R. W., & Uversky, V. N. (2014) · Chemical Reviews · doi:10.1021/cr400459c · Cited by 216 · see citing works
A phosphoglycolate phosphatase-deficient mutant of Arabidopsis
Somerville, C. R., & Ogren, W. L. (1979) · Nature · doi:10.1038/280833a0 · Cited by 198 · see citing works
Yao, J. S., Chung, J., Eliezer, D., Wright, P. E., & Dyson, H. J. (2001) · Biochemistry · doi:10.1021/bi002776i · Cited by 195 · see citing works
Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase
Mueller-Cajar, O., Stotz, M., Wendler, P., Hartl, F. U., Bracher, A., & Hayer-Hartl, M. (2011) · Nature · doi:10.1038/nature10568 · Cited by 190 · see citing works
Cell signaling, post-translational protein modifications and NMR spectroscopy
Theillet, F., Smet‐Nocca, C., Liokatis, S., Thongwichian, R., Kosten, J., Yoon, M., Kriwacki, R. W., Landrieu, I., Lippens, G. M., & Selenko, P. (2012) · Journal of Biomolecular NMR · doi:10.1007/s10858-012-9674-x · Cited by 188 · see citing works
Portis, A. R., Salvucci, M. E., & Ogren, W. L. (1986) · PLANT PHYSIOLOGY · doi:10.1104/pp.82.4.967 · Cited by 183 · see citing works
The redox-switch domain of Hsp33 functions as dual stress sensor
Ilbert, M., Horst, J., Ahrens, S., Winter, J., Graf, P. C. F., Lilie, H., & Jakob, U. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1244 · Cited by 182 · see citing works
Comprehensive review of methods for prediction of intrinsic disorder and its molecular functions
Meng, F., Uversky, V. N., & Kurgan, L. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2555-4 · Cited by 176 · see citing works
Osmotic Acclimation and Turgor Pressure Regulation in Algae
Bisson, M. A., & Kirst, G. O. (1995) · Die Naturwissenschaften · doi:10.1007/bf01131597 · Cited by 170 · see citing works
Liu, Y., Wang, X., & Liu, B. (2017) · Briefings in Bioinformatics · doi:10.1093/bib/bbx126 · Cited by 163 · see citing works
The phase separation underlying the pyrenoid-based microalgal Rubisco supercharger
Wunder, T., Cheng, S. L. H., Lai, S.-K., Li, H., & Mueller‐Cajar, O. (2018) · Nature Communications · doi:10.1038/s41467-018-07624-w · Cited by 159 · see citing works
Glutathionylation in the Photosynthetic Model Organism Chlamydomonas reinhardtii: A Proteomic Survey
Zaffagnini, M., Bedhomme, M., Groni, H., Marchand, C. H., Puppo, C., Gontero, B., Cassier‐Chauvat, C., Decottignies, P., & Lemaire, S. D. (2011) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.014142 · Cited by 158 · see citing works
Self-citationPaila, Y. D., Richardson, L. G. L., & Schnell, D. J. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.08.016 · Cited by 156 · see citing works
Characterization of disordered proteins with ENSEMBLE
Krzeminski, M., Marsh, J. A., Neale, C., Choy, W., & Forman-Kay, J. D. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts701 · Cited by 154 · see citing works
Intrinsically disordered proteins and multicellular organisms
Dunker, A. K., Bondos, S. E., Huang, F., & Oldfield, C. J. (2015) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2014.09.025 · Cited by 150 · see citing works
Niklas, K. J., Bondos, S. E., Dunker, A. K., & Newman, S. A. (2015) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2015.00008 · Cited by 132 · see citing works
Order out of Disorder: Working Cycle of an Intrinsically Unfolded Chaperone
Reichmann, D., Xu, Y., Cremers, C. M., Ilbert, M., Mittelman, R., Fitzgerald, M. C., & Jakob, U. (2012) · Cell · doi:10.1016/j.cell.2012.01.045 · Cited by 131 · see citing works
Conditional disorder in chaperone action
Bardwell, J. C. A., & Jakob, U. (2012) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2012.08.006 · Cited by 130 · see citing works
Expanding the Paradigm: Intrinsically Disordered Proteins and Allosteric Regulation
Berlow, R. B., Dyson, H. J., & Wright, P. E. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.04.003 · Cited by 129 · see citing works
Finding Our Way in the Dark Proteome
Bhowmick, A., Brookes, D. H., Yost, S. R., Dyson, H. J., Forman-Kay, J. D., Gunter, D., Head-Gordon, M., Hura, G. L., Pande, V. S., Wemmer, D. E., et al. (2016) · Journal of the American Chemical Society · doi:10.1021/jacs.6b06543 · Cited by 128 · see citing works
Genest, O., Hoskins, J. R., Camberg, J. L., Doyle, S. M., & Wickner, S. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104703108 · Cited by 124 · see citing works
The Small Protein CP12: A Protein Linker for Supramolecular Complex Assembly
Graciet, E., Gans, P., Wedel, N., Lebreton, S., Camadro, J., & Gontero, B. (2003) · Biochemistry · doi:10.1021/bi034474x · Cited by 119 · see citing works
Self-citationStructure of green-type Rubisco activase from tobacco
Stotz, M., Mueller‐Cajar, O., Ciniawsky, S., Wendler, P., Hartl, F. U., Bracher, A., & Hayer-Hartl, M. K. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2171 · Cited by 118 · see citing works
Simultaneous quantification of protein order and disorder
Sormanni, P., Piovesan, D., Heller, G. T., Bonomi, M., Kukić, P., Camilloni, C., Fuxreiter, M., Dosztányi, Z., Pappu, R. V., Babu, M. M., et al. (2017) · Nature Chemical Biology · doi:10.1038/nchembio.2331 · Cited by 118 · see citing works
Lessons from pressure denaturation of proteins
Roche, J., & Royer, C. A. (2018) · Journal of The Royal Society Interface · doi:10.1098/rsif.2018.0244 · Cited by 118 · see citing works
Wang, H., Gau, B. C., Slade, W. O., Juergens, M., Li, P., & Hicks, L. M. (2014) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.038281 · Cited by 115 · see citing works
The emerging roles of protein glutathionylation in chloroplasts
Zaffagnini, M., Bedhomme, M., Lemaire, S. D., & Trost, P. (2012) · Plant Science · doi:10.1016/j.plantsci.2012.01.005 · Cited by 110 · see citing works
Sparla, F., Pupillo, P., & Trost, P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206873200 · Cited by 109 · see citing works
Trost, P., Fermani, S., Marri, L., Zaffagnini, M., Falini, G., Scagliarini, S., Pupillo, P., & Sparla, F. (2006) · Photosynthesis Research · doi:10.1007/s11120-006-9099-z · Cited by 106 · see citing works
The CP12 protein family: a thioredoxin-mediated metabolic switch?
López‐Calcagno, P. E., Howard, T. P., & Raines, C. A. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00009 · Cited by 103 · see citing works
Quality and bias of protein disorder predictors
Nielsen, J. T., & Mulder, F. A. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-41644-w · Cited by 85 · see citing works
The GapA/B Gene Duplication Marks the Origin of Streptophyta (Charophytes and Land Plants)
Petersen, J., Teich, R., Becker, B., Cerff, R., & Brinkmann, H. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msj123 · Cited by 84 · see citing works
Fifty years in the thioredoxin field and a bountiful harvest
Buchanan, B. B., Holmgren, A., Jacquot, J., & Scheibe, R. (2012) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2012.07.006 · Cited by 80 · see citing works
An intrinsically disordered protein, CP12: jack of all trades and master of the Calvin cycle
Gontero, B., & MABERLY, S. C. (2012) · Biochemical Society Transactions · doi:10.1042/bst20120097 · Cited by 78 · see citing works
Self-citationBaalmann, E., Scheibe, R., Cerff, R., & Martin, W. F. (1996) · Plant Molecular Biology · doi:10.1007/bf00019102 · Cited by 78 · see citing works
Marri, L., Trost, P., Trivelli, X., Gonnelli, L., Pupillo, P., & Sparla, F. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705650200 · Cited by 76 · see citing works
Hsp70 and Hsp90 of E. coli Directly Interact for Collaboration in Protein Remodeling
Genest, O., Hoskins, J. R., Kravats, A. N., Doyle, S. M., & Wickner, S. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.10.010 · Cited by 76 · see citing works
Pyrenoid functions revealed by proteomics in Chlamydomonas reinhardtii
Zhan, Y., Marchand, C. H., Maes, A., Mauriès, A., Sun, Y., Dhaliwal, J. S., Uniacke, J., Arragain, S., Jiang, H., Gold, N. D., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0185039 · Cited by 76 · see citing works
Structure of a Product Complex of Spinach Ribulose-1,5-bisphosphate Carboxylase/Oxygenase,
Taylor, T. C., & Andersson, I. (1997) · Biochemistry · doi:10.1021/bi962818w · Cited by 74 · see citing works
CP12-mediated protection of Calvin–Benson cycle enzymes from oxidative stress
Marri, L., Thieulin‐Pardo, G., Lebrun, R., Puppo, R., Zaffagnini, M., Trost, P., Gontero, B., & Sparla, F. (2013) · Biochimie · doi:10.1016/j.biochi.2013.10.018 · Cited by 74 · see citing works
Self-citationGroben, R., Kaloudas, D., Raines, C. A., Offmann, B., MABERLY, S. C., & Gontero, B. (2010) · Photosynthesis Research · doi:10.1007/s11120-010-9542-z · Cited by 72 · see citing works
Self-citationUncovering the Unfoldome: Enriching Cell Extracts for Unstructured Proteins by Acid Treatment
Cortese, M. S., Baird, J. P., Uversky, V. N., & Dunker, A. K. (2005) · Journal of Proteome Research · doi:10.1021/pr050119c · Cited by 72 · see citing works
Willmund, F., & Schroda, M. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.063578 · Cited by 71 · see citing works
Igamberdiev, A. U., & Kleczkowski, L. A. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00010 · Cited by 70 · see citing works
Turkina, M. V., Blanco-Rivero, A., Vainonen, J. P., Vener, A. V., & Villarejo, A. (2006) · PROTEOMICS · doi:10.1002/pmic.200500461 · Cited by 68 · see citing works
Yruela, I., Oldfield, C. J., Niklas, K. J., & Dunker, A. K. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx073 · Cited by 67 · see citing works
Mechanism of Enzyme Repair by the AAA+ Chaperone Rubisco Activase
Bhat, J. Y., Miličić, G., Thieulin‐Pardo, G., Bracher, A., Maxwell, A. T., Ciniawsky, S., Mueller‐Cajar, O., Engen, J. R., Hartl, F. U., Wendler, P., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.07.004 · Cited by 67 · see citing works
Niklas, K. J., Dunker, A. K., & Yruela, I. (2018) · Journal of Experimental Botany · doi:10.1093/jxb/erx493 · Cited by 67 · see citing works
Drzymalla, C., Schroda, M., & Beck, C. F. (1996) · Plant Molecular Biology · doi:10.1007/bf00040835 · Cited by 65 · see citing works
Redox Regulation of Chloroplast Enzymes in Galdieria sulphuraria in View of Eukaryotic Evolution
Oesterhelt, C., Klocke, S., Holtgrefe, S., Linke, V., Weber, A. P. M., & Scheibe, R. (2007) · Plant and Cell Physiology · doi:10.1093/pcp/pcm108 · Cited by 64 · see citing works
A comprehensive assessment of long intrinsic protein disorder from the DisProt database
Necci, M., Piovesan, D., Dosztányi, Z., Tompa, P., & Tosatto, S. C. E. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx590 · Cited by 64 · see citing works
MABERLY, S. C., Courcelle, C., Groben, R., & Gontero, B. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp337 · Cited by 62 · see citing works
Self-citationStanley, D. N., Raines, C. A., & Kerfeld, C. A. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.210542 · Cited by 60 · see citing works
Jensen, E. L., Clément, R., MABERLY, S. C., & Gontero, B. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0401 · Cited by 59 · see citing works
Self-citationMaintaining photosynthetic CO2 fixation via protein remodelling: the Rubisco activases
Mueller‐Cajar, O., Stotz, M., & Bracher, A. (2013) · Photosynthesis Research · doi:10.1007/s11120-013-9819-0 · Cited by 57 · see citing works
Membrane-induced folding of the plant-stress protein Lti30.
Eriksson, S. K., Eremina, N., Barth, A., Danielsson, J., & Harryson, P. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01531 · Cited by 55 · see citing works
Evolution of Rubisco activase gene in plants
Nagarajan, R., & Gill, K. S. (2017) · Plant Molecular Biology · doi:10.1007/s11103-017-0680-y · Cited by 54 · see citing works
Characterization of native and recombinant A4 glyceraldehyde 3‐phosphate dehydrogenase
Graciet, E., Lebreton, S., Camadro, J., & Gontero, B. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2003.03372.x · Cited by 53 · see citing works
Self-citationProtein transport in organelles: The Toc complex way of preprotein import
Agne, B., & Kessler, F. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.06873.x · Cited by 51 · see citing works
Cremers, C. M., Reichmann, D., Hausmann, J., Ilbert, M., & Jakob, U. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.084350 · Cited by 51 · see citing works
Lebreton, S., Graciet, E., & Gontero, B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m213096200 · Cited by 51 · see citing works
Self-citationRoche, J., Ying, J., Maltsev, A. S., & Bax, A. (2013) · ChemBioChem · doi:10.1002/cbic.201300244 · Cited by 49 · see citing works
The potential for co-evolution of CO2-concentrating mechanisms and Rubisco in diatoms
Young, J. N., & Hopkinson, B. M. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erx130 · Cited by 49 · see citing works
Erales, J., Lignon, S., & Gontero, B. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808254200 · Cited by 48 · see citing works
Self-citationThe HSP70 chaperone machines of Chlamydomonas are induced by cold stress
Maikova, A., Михайловна, З. Ж., Lapina, T., & Ermilova, E. (2016) · Journal of Plant Physiology · doi:10.1016/j.jplph.2016.07.012 · Cited by 46 · see citing works
Erales, J., Avilán, L., Lebreton, S., & Gontero, B. (2008) · FEBS Journal · doi:10.1111/j.1742-4658.2008.06284.x · Cited by 44 · see citing works
Self-citationConstruction of a 3D model of CP12, a protein linker
Gardebien, F., Thangudu, R. R., Gontero, B., & Offmann, B. (2006) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2005.12.003 · Cited by 43 · see citing works
Self-citationOPAL+: Length‐Specific MoRF Prediction in Intrinsically Disordered Protein Sequences
Sharma, R., Sharma, A. K., Raicar, G., Tsunoda, T., & Patil, A. (2018) · PROTEOMICS · doi:10.1002/pmic.201800058 · Cited by 43 · see citing works
Correlations between predicted protein disorder and post-translational modifications in plants
Kurotani, A., Tokmakov, A. A., Kuroda, Y., Fukami, Y., Shinozaki, K., & Sakurai, T. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btt762 · Cited by 42 · see citing works
Norén, L., Kindgren, P., Stachula, P., Rühl, M., Eriksson, M. E., Hurry, V., & Strand, A. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00374 · Cited by 41 · see citing works
CO 2 ‐fixing liquid droplets: Towards a dissection of the microalgal pyrenoid
Wunder, T., Oh, Z. G., & Mueller‐Cajar, O. (2019) · Traffic · doi:10.1111/tra.12650 · Cited by 40 · see citing works
Order in Disorder as Observed by the “Hydrophobic Cluster Analysis” of Protein Sequences
Bitard‐Feildel, T., Lamiable, A., Mornon, J., & Callebaut, I. (2018) · PROTEOMICS · doi:10.1002/pmic.201800054 · Cited by 38 · see citing works
Protein disorder in plants: a view from the chloroplast
Yruela, I., & Contreras‐Moreira, B. (2012) · BMC Plant Biology · doi:10.1186/1471-2229-12-165 · Cited by 34 · see citing works
Exploring intrinsically disordered proteins in Chlamydomonas reinhardtii
Zhang, Y., Launay, H. M. M., Schramm, A., Lebrun, R., & Gontero, B. (2018) · Scientific Reports · doi:10.1038/s41598-018-24772-7 · Cited by 34 · see citing works
Self-citationMileo, E., Lorenzi, M., Erales, J., Lignon, S., Puppo, C., Breton, N. L., Étienne, É., Marque, S. R. A., Guigliarelli, B., Gontero, B., et al. (2013) · Molecular BioSystems · doi:10.1039/c3mb70190e · Cited by 32 · see citing works
Self-citationA review of multi-domain and flexible molecular chaperones studies by small-angle X-ray scattering
Borges, J. C., Seraphim, T. V., Dores-Silva, P. R., & Barbosa, L. R. S. (2016) · Biophysical Reviews · doi:10.1007/s12551-016-0194-x · Cited by 32 · see citing works
Delobel, A., Graciet, E., Andreescu, S., Gontero, B., Halgand, F., & Laprévôte, O. (2005) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.2192 · Cited by 31 · see citing works
Self-citationChaperones: needed for both the good times and the bad times
Quinlan, R. A., & Ellis, R. J. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0091 · Cited by 31 · see citing works
Kurotani, A., & Sakurai, T. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms160819812 · Cited by 27 · see citing works
Thieulin‐Pardo, G., Avilán, L., Kojadinovic, M., & Gontero, B. (2015) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2015.00023 · Cited by 26 · see citing works
Self-citationGontero, B., & Salvucci, M. E. (2014) · Aquatic Botany · doi:10.1016/j.aquabot.2014.05.011 · Cited by 26 · see citing works
Self-citationDifferent pressure–temperature behavior of the structured and unstructured regions of titin
Somkuti, J., Mártonfalvi, Z., Kellermayer, M., & Smeller, L. (2012) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2012.10.001 · Cited by 23 · see citing works
Identification of CP12 as a Novel Calcium-Binding Protein in Chloroplasts
Rocha, A. G., & Vothknecht, U. C. (2013) · Plants · doi:10.3390/plants2030530 · Cited by 22 · see citing works
Towards Proteomic Approaches for the Identification of Structural Disorder
Csizmók, V., Dosztányi, Z., Simon, I., & Tompa, P. (2007) · Current Protein and Peptide Science · doi:10.2174/138920307780363479 · Cited by 22 · see citing works
A ‘foldosome’ in the chloroplast?
Schroda, M., & Mühlhaus, T. (2009) · Plant Signaling & Behavior · doi:10.4161/psb.4.4.7758 · Cited by 21 · see citing works
Genetic recombination is associated with intrinsic disorder in plant proteomes
Yruela, I., & Contreras‐Moreira, B. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-772 · Cited by 21 · see citing works
Disulfide driven folding for a conditionally disordered protein
Fraga, H., Pujols, J., Gil-García, M., Roque, A., Bernardo‐Seisdedos, G., Santambrogio, C., Bech‐Serra, J. J., Canals, F., Bernadó, P., Grandori, R., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-17259-4 · Cited by 21 · see citing works
Launay, H., Barré, P., Puppo, C., Zhang, Y., Maneville, S., Gontero, B., & Receveur‐Brechot, V. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.02.020 · Cited by 21 · see citing works
Self-citationLaunay, H., Barré, P., Puppo, C., Maneville, S., Gontero, B., & Receveur‐Brechot, V. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.06.014 · Cited by 19 · see citing works
Self-citationKaaki, W., Woudstra, M., Gontero, B., & Halgand, F. (2012) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.6442 · Cited by 18 · see citing works
Self-citationThe intriguing CP12‐like tail of adenylate kinase 3 fromChlamydomonas reinhardtii
Thieulin‐Pardo, G., Schramm, A., Lignon, S., Lebrun, R., Kojadinovic, M., & Gontero, B. (2016) · FEBS Journal · doi:10.1111/febs.13814 · Cited by 18 · see citing works
Self-citationControl of Carbon Fixation in Chloroplasts
Gontero, B., Avilán, L., & Lebreton, S. (2007) · Blackwell Publishing Ltd eBooks · doi:10.1002/9780470988640.ch7 · Cited by 17 · see citing works
Self-citationFRET analysis of CP12 structural interplay by GAPDH and PRK
Moparthi, S. B., Thieulin‐Pardo, G., de Torres, J., Ghenuche, P., Gontero, B., & Wenger, J. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.01.135 · Cited by 17 · see citing works
Self-citationHSP 33 in eukaryotes – an evolutionary tale of a chaperone adapted to photosynthetic organisms
Segal, N., & Shapira, M. (2015) · The Plant Journal · doi:10.1111/tpj.12855 · Cited by 17 · see citing works
Zhang, Y., Launay, H., Liu, F., Lebrun, R., & Gontero, B. (2018) · FEBS Journal · doi:10.1111/febs.14494 · Cited by 17 · see citing works
Self-citationMoparthi, S. B., Thieulin‐Pardo, G., Mansuelle, P., Rigneault, H., Gontero, B., & Wenger, J. (2014) · FEBS Journal · doi:10.1111/febs.12854 · Cited by 16 · see citing works
Self-citationGay, G. D. P., Paladini, A. A., Stein, M., & Wolosiuk, R. A. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)54797-9 · Cited by 11 · see citing works
Interfacial Properties of NTAIL, an Intrinsically Disordered Protein
Bénarouche, A., Habchi, J., Cagna, A., Maniti, O., Girard-Egrot, A., Cavalier, J., Longhi, S., & Carrière, F. (2017) · Biophysical Journal · doi:10.1016/j.bpj.2017.10.010 · Cited by 10 · see citing works
Self-citationSena, L., & Uversky, V. N. (2016) · Intrinsically Disordered Proteins · doi:10.1080/21690707.2016.1253526 · Cited by 7 · see citing works
Proteomic Methods for the Identification of Intrinsically Disordered Proteins
Tantos, Á., & Tompa, P. (2012) · Springer eBooks · doi:10.1007/978-1-4614-3704-8_29 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Intrinsically disordered proteins play diverse roles in cell signaling
Bondos, S. E., Dunker, A. K., & Uversky, V. N. (2022) · Cell Communication and Signaling · doi:10.1186/s12964-022-00821-7 · Cited by 222 · see citing works
Intrinsically disordered regions are poised to act as sensors of cellular chemistry
MOSES, D. C., Ginell, G. M., Holehouse, A. S., & Sukenik, S. (2023) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2023.08.001 · Cited by 133 · see citing works
Aquatic toxicity and mode of action of CdS and ZnS nanoparticles in four microalgae species
Pikula, K., Mintcheva, N., Kulinich, S. A., Zakharenko, A. M., Markina, Z., Чайка, В., Orlova, T. Y., Mezhuev, Y. O., Kokkinakis, M., Tsatsakis, A. M., et al. (2020) · Environmental Research · doi:10.1016/j.envres.2020.109513 · Cited by 76 · see citing works
Neira, J. L., Rizzuti, B., Jiménez-Alesanco, A., Palomino‐Schätzlein, M., Abián, O., Velázquez‐Campoy, A., & Iovanna, J. (2020) · Biomolecules · doi:10.3390/biom10091313 · Cited by 26 · see citing works
Kim, S. Y., Stessman, D. J., Wright, D. A., Spalding, M. H., Huber, S. C., & Ort, D. R. (2020) · The Plant Journal · doi:10.1111/tpj.14897 · Cited by 19 · see citing works
A new type of flexible CP12 protein in the marine diatom Thalassiosira pseudonana
Shao, H., Huang, W., Avilán, L., Receveur‐Brechot, V., Puppo, C., Puppo, R., Lebrun, R., Gontero, B., & Launay, H. (2021) · Cell Communication and Signaling · doi:10.1186/s12964-021-00718-x · Cited by 15 · see citing works
Self-citationGérard, C., Carrière, F., Receveur‐Brechot, V., Launay, H., & Gontero, B. (2022) · Biomolecules · doi:10.3390/biom12081047 · Cited by 15 · see citing works
Self-citationPikula, K., Kirichenko, K. Y., Vakhniuk, I. A., Kalantzi, O., Холодов, А. С., Orlova, T. Y., Markina, Z., Tsatsakis, A. M., & Golokhvast, K. S. (2021) · Toxicology Reports · doi:10.1016/j.toxrep.2021.04.004 · Cited by 9 · see citing works
Launay, H., Shao, H., Bornet, O., Cantrelle, F., Lebrun, R., Receveur‐Brechot, V., & Gontero, B. (2021) · Biomolecules · doi:10.3390/biom11050701 · Cited by 8 · see citing works
Self-citationIntrinsically disordered proteins in biology: One for all, all for one
Yruela, I., & Neira, J. L. (2020) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2020.108328 · Cited by 8 · see citing works
Bezerra, R. P., Conniff, A. S., & Uversky, V. N. (2022) · Biochimie · doi:10.1016/j.biochi.2022.07.004 · Cited by 7 · see citing works
Launay, H., Avilán, L., Gérard, C., Parsiegla, G., Receveur‐Brechot, V., Gontero, B., & Carrière, F. (2023) · FEBS Letters · doi:10.1002/1873-3468.14754 · Cited by 5 · see citing works
Self-citationDisordered but rhythmic—the role of intrinsic protein disorder in eukaryotic circadian timing
Usher, E. T., & Pelham, J. F. (2025) · FEBS Letters · doi:10.1002/1873-3468.70238 · Cited by 2 · see citing works
Proteomic profiling of cryopreserved Trichormus variabilis using various cryoprotectants
Bae, J.-W., Park, M., Lee, C. S., & Kwon, W. (2021) · Cryobiology · doi:10.1016/j.cryobiol.2021.11.175 · Cited by 1 · see citing works
Screening clusters of charged residues in plants’ mitochondrial proteins and biological significance
Nebli, S., Rebaï, A., & Ayadi, I. (2024) · Mitochondrion · doi:10.1016/j.mito.2024.101938 · Cited by 1 · see citing works
Shao, H., Huang, W., Avilán, L., Receveur‐Brechot, V., Puppo, C., Puppo, R., Lebrun, R., Gontero, B., & Launay, H. (2021) · Figshare · doi:10.6084/m9.figshare.14299987
Self-citation
- Authors
- Launay, H., Receveur-Bréchot, V., Carrière, F., & Gontero, B.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Gontero, Brigitte
- Venue
- Archives of Biochemistry and Biophysics
- Publisher
- Elsevier BV
- Published
- 2019-09
- Volume
- 672
- Pages
- 108070
- ISSN
- 0003-9861 (ISSN-L)
- OpenAlex
- W2968553586
- Cited by
- 16
- References
- 144
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 2 · 2022: 3 · 2021: 5 · 2020: 4
- FWCI
- 0.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Archives of Biochemistry and Biophysics (acceptedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- HAL AMU (submittedVersion)
- Funders
- Centre National de la Recherche Scientifique
- Aix-Marseille Université (ANR-15-CE05-0021-03)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Keywords
- intrinsically disordered proteins, intrinsically disordered regions, algae, algal metabolism, CP12, redox regulation, pyrenoid, Rubisco activase, glyceraldehyde-3-phosphate dehydrogenase, adenylate kinase, molecular chaperones, heat shock proteins, proteostasis, carbon assimilation, protein disorder
- MeSH terms
- Chlorophyta, Photosynthesis, Molecular Chaperones, Algal Proteins, Microalgae, Intrinsically Disordered Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review