Systems and Synthetic Biology of Microalgae



Zaffagnini M, Marchand CH, Malferrari M, Murail S, Bonacchi S, Genovese D, Montalti M, Venturoli G, Falini G, Baaden M, Lemaire SD, Fermani S, Trost P (2019) Glutathionylation primes soluble glyceraldehyde-3-phosphate dehydrogenase for late collapse into insoluble aggregates. Proc. Natl. Acad. Sci. USA. 116 : 26057-26065.

De Carpentier F, Lemaire SD, Danon A. When unity is strength: the strategies used by Chlamydomonas to survive environmental stresses. Cells, 8(11), 1307

Zaffagnini M, Fermani S, Marchand CH, Costa A, Sparla F, Rouhier N, Geigenberger P, Lemaire SD, Trost P (2019) Redox homeostasis in photosynthetic organisms: novel and established thiol-based molecular mechanisms. Antioxid Redox Signal. 31(3): 155-210

Vavitsas K, Crozet P, Hamborg Vinde M, Davies F, Lemaire SD, Vickers CE (2019) The synthetic biology toolkit for photosynthetic microorganisms. Plant Physiol. 181: 14-27.

Gurrieri L., Del Giudice A, Demitri N, Falini G, Pavel N, Zaffagnini M, Polentarutti M, Crozet P, Marchand CH, Henri J, Trost P, Lemaire SD, Sparla F, Fermani S. (2019) Arabidopsis and Chlamydomonas phosphoribulokinase crystal structures complete the redox structural proteome of the Calvin-Benson cycle. Proc. Natl. Acad. Sci. USA. 116(16): 8048-8053 [SupData]

Shao Z, Borde C, Marchand CH, Lemaire SD, Busson P, Gozlan JM, Escargueil A, Maréchal V (2019) Detection of IgG directed against a recombinant form of Epstein-Barr virus BALF0/1 protein in patients with nasopharyngeal carcinoma. Protein Expr. Purif. 162:44-50

Eberhard S, Valuchova S, Ravat J, Fulneček J, Jolivet P, Bujaldon S, Lemaire SD, Wollman FA, Teixeira MT, Riha K, Xu Z. (2019). Molecular characterization of Chlamydomonas reinhardtii telomeres and telomerase mutants. Life Sci Alliance. Jun 3;2(3). pii: e201900315. doi: 10.26508/lsa.201900315

De Mia M, Lemaire SD, Choquet Y, Wollman FA (2019) Nitric oxide remodels the photosynthetic apparatus under sulfur starvation in Chlamydomonas reinhardtii Plant Physiol. 179: 718-731 [Supp]

Marchand CH, Fermani S, Rossi J, Gurrieri L, Tedesco D, Henri J, Sparla F, Trost P, Lemaire SD, Zaffagnini M. (2019) Structural and biochemical insights into the reactivity of thioredoxin h1 from Chlamydomonas reinhardtii. Antioxidants 8, E10.


Zaffagnini M, Michelet L, Sciabolini C, Di Giacinto N, Morisse S, Marchand CH, Trost P, Fermani S, Lemaire SD (2014) High resolution crystal structure and redox properties of chloroplastic triosephosphate isomerase from Chlamydomonas reinhardtii. Mol Plant. 7(1): 101-120.

Morisse S, Zaffagnini M, Gao XH, Lemaire SD, Marchand CH (2014) Insight into protein S-nitrosylation in Chlamydomonas reinhardtii. Antioxid Redox Signal. 21(9):1271-84.  [Sup Data]

Heyno E, Innocenti G, Lemaire SD, Issakidis-Bourguet E, Krieger-Liszkay A (2014) Putative role of the malate valve enzyme NADP-malate dehydrogenase in H2O2 signalling in Arabidopsis. Philos Trans R Soc Lond B Biol Sci. 369(1640):20130228.

Veyel D, Sommer F, Muranaka LS, Rütgers M, Lemaire SD, Schroda M (2014) In vitro characterization of bacterial and chloroplast Hsp70 systems reveals an evolutionary optimization of the co-chaperones for their Hsp70 partner. Biochem J. 460(1):13-24.

de Paepe R, Lemaire SD, Danon A (2014) Cardiolipin at the heart of stress response across kingdoms. Plant Signal Behav. 9(9):e29228.

Pérez-Pérez ME, Zaffagnini M, Marchand CH, Crespo JL, Lemaire SD (2014) The yeast autophagy protease Atg4 is regulated by thioredoxin. Autophagy 10(11), 1953-64

Pérez-Martin M, Pérez-Pérez ME, Lemaire SD, Crespo JL (2014) Oxidative stress contributes to autophagy induction in response to endoplasmic reticulum stress in Chlamydomonas. Plant Physiol. 166(2):997-1008

Morisse S, Michelet L, Bedhomme M, Marchand CH, Calvaresi M, Trost P, Fermani S, Zaffagnini M, Lemaire SD (2014). Thioredoxin-dependent Redox Regulation of Chloroplastic Phosphoglycerate Kinase from Chlamydomonas reinhardtii. J Biol Chem. 289: 30012-24 


Michelet L, Roach T, Fischer BB, Bedhomme M, Lemaire SD, Krieger-Liszkay A (2013) Down-regulation of catalase activity allows transient accumulation of a hydrogen peroxide signal in Chlamydomonas reinhardtii. Plant Cell Environ. 36(6):1204-1213.  [sup data]

Zaffagnini M, Morisse S, Bedhomme M, Marchand CH, Festa M, Rouhier N, Lemaire SD*, Trost P* (*: corresponding authors) (2013) Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J Biol Chem 288(31):22777-22789.

Marteyn B, Sakr S, Farci S, Bedhomme M, Chardonnet S, Decottignies P, Lemaire SD, Cassier-Chauvat C, Chauvat F (2013) The Synechocystis PCC6803 MerA-like enzyme operates in the reduction of both mercury and uranium, under the control of the glutaredoxin 1 enzyme. J Bacteriol. 195(18):4138-4145.

Sakr S, Dutheil J, Saenkham P, Bottin H, Leplat C, Ortega-Ramos M, Aude JC, Chapuis V, Guedeney G, Decottignies P, Lemaire S, Cassier-Chauvat C, Chauvat F (2013) The activity of the Synechocystis PCC6803 AbrB2 regulator of hydrogen production can be post-translationally controlled through glutathionylation. Int J Hydrogen Energ 38, 13547-13555.

Pineau B, Bourge M, Marion J, Mauve C, Gilard F, Maneta-Peyret L, Moreau P, Satiat-Jeunemaître B, Brown SC, De Paepe R, Danon A (2013) The importance of cardiolipin synthase for mitochondrial ultrastructure, respiratory function, plant development, and stress responses in Arabidopsis. Plant Cell. 25(10):4195-4208.

Zaffagnini M, Fermani S, Costa A, Lemaire SD, Trost P (2013) Plant cytoplasmic GAPDH: redox post-translational modifications and moonlighting properties. Front Plant Sci. 4:450.

Michelet L, Zaffagnini M, Morisse S, Sparla F, Pérez-Pérez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD (2013) Redox regulation of the Calvin-Benson cycle: something old, something new. Front. Plant Sci. 4:470.


Bedhomme M, Adamo M, Marchand CH, Couturier J, Rouhier N, Lemaire SD, Zaffagnini M, Trost P (2012) Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem J. 445:337-347. [supplementary data]

Pérez-Pérez ME, Lemaire SD, Crespo JL (2012) Reactive oxygen species and autophagy in plants and algae. Plant Physiol. 160:156-164. 

Ramos C, Chardonnet S, Marchand CH, Decottignies P, Ango F, Daniel H, Le Maréchal P (2012) Native Presynaptic Metabotropic Glutamate Receptor 4 (mGluR4) Interacts with Exocytosis Proteins in Rat Cerebellum. J Biol Chem. 287(24):20176-86.

Zaffagnini M, Bedhomme M, Lemaire SD, Trost P (2012) The emerging roles of protein glutathionylation in chloroplasts. Plant Sci. 185-186:86-96.

Marchand CH, Salmeron C, Bou Raad R, Méniche X, Chami M, Masi M, Blanot D, Daffé M, Tropis M, Huc E, Le Maréchal P, Decottignies P, Bayan N. (2012) Biochemical disclosure of the mycolate outer membrane of Corynebacterium glutamicum. J Bacteriol. 194(3):587-97.

Zaffagnini M, Bedhomme M, Marchand CH, Couturier J, Gao XH, Rouhier N, Trost P, Lemaire SD (2012) Glutaredoxin S12: unique properties for redox signaling. Antioxid Redox Signal 16: 17-32.

Zaffagnini M, Bedhomme M, Marchand CH, Morisse S, Trost P, Lemaire SD (2012) Redox Regulation in Photosynthetic Organisms: Focus on Glutathionylation. Antioxid Redox Signal. 16: 567-586.

Zaffagnini M, Bedhomme M, Groni H, Marchand CH, Puppo C, Gontero C, Cassier-Chauvat C, Decottignies P, Lemaire SD (2012) Glutathionylation in the photosynthetic model organism Chlamydomonas reinhardtii: a proteomic survey. Mol. Cell Proteomics. 11(2):M111.014142.  Figure supplémentaire S1


Couturier J, Koh CS, Zaffagnini M, Winger AM, Gualberto JM, Corbier C, Decottignies P, Jacquot JP, Lemaire SD, Didierjean C, Rouhier N (2009) Structure-function relationship of the chloroplastic glutaredoxin S12 with an atypical WCSYS active site. J Biol Chem 284: 9299-9310

Fischer BB, Dayer R, Schwarzenbach Y, Lemaire SD, Behra R, Liedtke A, Eggen RI (2009) Function and regulation of the glutathione peroxidase homologous gene GPXH/GPX5 in Chlamydomonas reinhardtii. Plant Mol Biol 71: 569-583

Bedhomme M, Zaffagnini M, Marchand CH, Gao XH, Moslonka-Lefebvre M, Michelet L, Decottignies P, Lemaire SD (2009) Regulation by glutathionylation of isocitrate lyase from Chlamydomonas reinhardtii. J Biol Chem 284: 36282-36291

Tarrago L, Laugier E, Zaffagnini M, Marchand C, Le Marechal P, Rouhier N, Lemaire SD, Rey P (2009) Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J Biol Chem 284: 18963-18971

Rolland N, Atteia A, Decottignies P, Garin J, Hippler M, Kreimer G, Lemaire SD, Mittag M, Wagner V (2009) Chlamydomonas proteomics. Curr Opin Microbiol 12: 285-291

Preger V, Tango N, Marchand C, Lemaire SD, Carbonera D, Di Valentin M, Costa A, Pupillo P, Trost P (2009) Auxin-responsive genes AIR12 code for a new family of plasma membrane b-type cytochromes specific to flowering plants. Plant Physiol 150: 606-620

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

Gao XH, Bedhomme M, Veyel D, Zaffagnini M, Lemaire SD (2009) Methods for Analysis of Protein Glutathionylation and their Application to Photosynthetic Organisms. Mol Plant 2: 218-235

Terauchi AM, Lu SF, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T, Merchant SS (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284: 25867-25878

Gao XH, Bedhomme M, Michelet L, Zaffagnini M, Lemaire SD(2009) Glutathionylation in Photosynthetic Organisms. In J-P Jacquot, ed, Advances in Botanical Research, Oxidative stress and redox regulation in plants, Vol 52. Academic Press, Burlington, pp 363-403


Zaffagnini M, Michelet L, Marchand C, Sparla F, Decottignies P, Le Marechal P, Miginiac-Maslow M, Noctor G, Trost P, Lemaire SD (2007) The thioredoxin-independent isoform of chloroplastic glyceraldehyde-3-phosphate dehydrogenase is selectively regulated by glutathionylation. FEBS J 274: 212-226

Lemaire SD, Michelet L, Zaffagnini M, Massot V, Issakidis-Bourguet E (2007) Thioredoxins in chloroplasts. Curr Genet 51: 343-365

Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martinez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318: 245-250


Lemaire SD (2004) The glutaredoxin family in oxygenic photosynthetic organisms. Photosynth Res 79: 305-318

Keryer E, Collin V, Lavergne D, Lemaire S, Issakidis-Bourguet E (2004) Characterization of Arabidopsis Mutants for the Variable Subunit of Ferredoxin:thioredoxin Reductase. Photosynth Res 79: 265-274

Lemaire SD, Miginiac-Maslow M (2004) The thioredoxin superfamily in Chlamydomonas reinhardtii. Photosynth Res 82: 203-220

Rouhier N, Gelhaye E, Gualberto JM, Jordy MN, De Fay E, Hirasawa M, Duplessis S, Lemaire SD, Frey P, Martin F, Manieri W, Knaff DB, Jacquot JP (2004) Poplar peroxiredoxin Q. A thioredoxin-linked chloroplast antioxidant functional in pathogen defense. Plant Physiol 134: 1027-1038

Lemaire SD, Guillon B, Le Maréchal P, Keryer E, Miginiac-Maslow M, Decottignies P (2004) New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 101: 7475-7480

Pollock SV, Prout DL, Godfrey AC, Lemaire SD, Moroney JV (2004) The Chlamydomonas reinhardtii proteins Ccp1 and Ccp2 are required for long-term growth, but are not necessary for efficient photosynthesis, in a low-CO2 environment. Plant Mol Biol 56: 125-132

Sicard-Roselli C, Lemaire S, Jacquot JP, Favaudon V, Marchand C, Houee-Levin C (2004) Thioredoxin Ch1 of Chlamydomonas reinhardtii displays an unusual resistance toward one-electron oxidation. Eur J Biochem 271: 3481-3487

Marchand C, Le Maréchal P, Meyer Y, Miginiac-Maslow M, Issakidis-Bourguet E, Decottignies P (2004) New targets of Arabidopsis thioredoxins revealed by proteomic analysis. Proteomics 4 : 2696-2706

Leduc D, Graziani S, Lipowski G, Marchand C, Le Maréchal P, Liebl U, Myllykallio H (2004) Functionnal evidence for active site location of tetrameric thymidylate synthase X at the interphase of three monomers. PNAS 101: 7252-7257.

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