Isolation and characterization of mutants corresponding to the MENA, MENB, MENC, and MENE enzymatic steps of 5'-monohydroxyphylloquinone biosynthesis in Chlamydomonas reinhardtii.

Emonds-Alt, Barbara; Coosemans, Nadine; Gerards, Thomas; Remacle, Claire; Cardol, Pierre

doi:10.1111/tpj.13352

Article (Scientific journals)

Isolation and characterization of mutants corresponding to the MENA, MENB, MENC, and MENE enzymatic steps of 5'-monohydroxyphylloquinone biosynthesis in Chlamydomonas reinhardtii.

Emonds-Alt, Barbara; Coosemans, Nadine; Gerards, Thomas et al.

2016 • In Plant Journal

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/203206

DOI
10.1111/tpj.13352

PubMed
27612091

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

TPJ Revised 04082016.pdf

Author preprint (3.36 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Disciplines :

Biochemistry, biophysics & molecular biology
Phytobiology (plant sciences, forestry, mycology...)

Author, co-author :

Emonds-Alt, Barbara ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues

Coosemans, Nadine ; Université de Liège > Département des sciences de la vie > Département des sciences de la vie

Gerards, Thomas ; Université de Liège > Labo de Bioénergétique

Remacle, Claire ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues

Cardol, Pierre ; Université de Liège > Département des sciences de la vie > Génétique et physiologie des microalgues

Language :

English

Title :

Isolation and characterization of mutants corresponding to the MENA, MENB, MENC, and MENE enzymatic steps of 5'-monohydroxyphylloquinone biosynthesis in Chlamydomonas reinhardtii.

Publication date :

09 September 2016

Journal title :

Plant Journal

ISSN :

0960-7412

eISSN :

1365-313X

Publisher :

Blackwell, Oxford, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://onlinelibrary.wiley.com/doi/10.1111/tpj.13352/epdf

European Projects :

H2020 - 682580 - BEAL - Bioenergetics in microalgae : regulation modes of mitochondrial respiration, photosynthesis, and fermentative pathways, and their interactions in secondary algae

Funders :

CE - Commission Européenne

Available on ORBi :

since 07 November 2016

Statistics

Number of views

100 (19 by ULiège)

Number of downloads

137 (10 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Babujee, L., Wurtz, V., Ma, C., Lueder, F., Soni, P., Van Dorsselaer, A. and Reumann, S. (2010) The proteome map of spinach leaf peroxisomes indicates partial compartmentalization of phylloquinone (vitamin K1) biosynthesis in plant peroxisomes. J. Exp. Bot. 61, 1441–1453.
Bailleul, B., Cardol, P., Breyton, C. and Finazzi, G. (2010) Electrochromism: a useful probe to study algal photosynthesis. Photosynth. Res. 106, 179–189.
Barbieri, M.R., Larosa, V., Nouet, C., Subrahmanian, N., Remacle, C. and Hamel, P.P. (2011) A forward genetic screen identifies mutants deficient for mitochondrial complex I assembly in Chlamydomonas reinhardtii. Genetics, 188, 349–358.
Berthold, P., Schmitt, R. and Mages, W. (2002) An engineered Streptomyces hygroscopicus aph 7” gene mediates dominant resistance against hygromycin B in Chlamydomonas reinhardtii. Protist, 153, 401–412.
Cardol, P., Gloire, G., Havaux, M., Remacle, C., Matagne, R. and Franck, F. (2003) Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol. 133, 2010–2020.
Chen, M., Ma, X., Chen, X., Jiang, M., Song, H. and Guo, Z. (2013) Identification of a hotdog fold thioesterase involved in the biosynthesis of menaquinone in Escherichia coli. J. Bacteriol. 195, 2768–2775.
Clowez, S., Godaux, D., Cardol, P., Wollman, F.-A. and Rappaport, F. (2015) The involvement of hydrogen-producing and ATP-dependent NADPH-consuming pathways in setting the redox poise in the chloroplast of Chlamydomonas reinhardtii in anoxia. J. Biol. Chem. 290, 8666–8676.
Dent, R.M., Haglund, C.M., Chin, B.L., Kobayashi, M.C. and Niyogi, K.K. (2005) Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii. Plant Physiol. 137, 545–556.
Depège, N., Bellafiore, S. and Rochaix, J.-D. (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science, 299, 1572–1575.
Desplats, C., Mus, F., Cuiné, S., Billon, E., Cournac, L. and Peltier, G. (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in chlamydomonas chloroplasts. J. Biol. Chem. 284, 4148–4157.
Drop, B., Webber-Birungi, M., Fusetti, F., Kouřil, R., Redding, K.E., Boekema, E.J. and Croce, R. (2011) Photosystem I of Chlamydomonas reinhardtii contains nine light-harvesting complexes (Lhca) located on one side of the core. J. Biol. Chem. 286, 44878–44887.
Duby, F. and Matagne, R.F. (1999) Alteration of dark respiration and reduction of phototrophic growth in a mitochondrial DNA deletion mutant of Chlamydomonas lacking cob, nd4, and the 3’ end of nd5. Plant Cell, 11, 115–125.
Edson, K.Z., Prasad, B., Unadkat, J.D., Suhara, Y., Okano, T., Guengerich, F.P. and Rettie, A.E. (2013) Cytochrome P450-dependent catabolism of vitamin K: ω-hydroxylation catalyzed by human CYP4F2 and CYP4F11. Biochemistry, 52, 8276–8285.
Fatihi, A., Latimer, S., Schmollinger, S., Block, A., Dussault, P.H. and Vermaas, W.F.J. (2015) A dedicated type II NADPH dehydrogenase performs the penultimate step in the biosynthesis of vitamin K1 in Synechocystis and Arabidopsis. Plant Cell, 27, 1730–1741.
Furt, F., Allen, W.J., Widhalm, J.R., Madzelan, P., Rizzo, R.C., Basset, G. and Wilson, M.A. (2013) Functional convergence of structurally distinct thioesterases from cyanobacteria and plants involved in phylloquinone biosynthesis. Acta. Crystallogr. Sect. D. Biol. Crystallogr. 69, 1876–1888.
Furuya, K., Hayashi, M. and Yabushita, Y. (1998) HPLC determination of phytoplankton pigments using N, N-dimethylformamide. J. Oceanogr. 54, 199–203.
Garcion, C., Lohmann, A., Lamodie, E., Catinot, J., Buchala, A., Doermann, P. and Métraux, J.-P. (2008) Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol. 147, 1279–1287.
Genty, B., Briantais, J.-M. and Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87–92.
Ghysels, B., Godaux, D., Matagne, R.F., Cardol, P. and Franck, F. (2013) Function of the chloroplast hydrogenase in the microalga Chlamydomonas: the role of hydrogenase and state transitions during photosynthetic activation in anaerobiosis. PLoS One, 8, e64161.
Godaux, D., Emonds-Alt, B., Berne, N., Ghysels, B., Alric, J., Remacle, C. and Cardol, P. (2013) A novel screening method for hydrogenase-deficient mutants in Chlamydomonas reinhardtii based on in vivo chlorophyll fluorescence and photosystem II quantum yield. Int. J. Hydrogen Energy 38, 1826–1836.
Godaux, D., Bailleul, B., Berne, N. and Cardol, P. (2015) Induction of photosynthetic carbon fixation in anoxia relies on hydrogenase activity and PGRL1-mediated cyclic electron flow in Chlamydomonas reinhardtii. Plant Physiol. 168, 648–658.
Gross, J., Won, K.C., Lezhneva, L., Falk, J., Krupinska, K., Shinozaki, K., Seki, M., Herrmann, R.G. and Meurer, J. (2006) A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes. J. Biol. Chem. 281, 17189–17196.
Guergova-Kuras, M., Boudreaux, B., Joliot, A., Joliot, P. and Redding, K. (2001) Evidence for two active branches for electron transfer in photosystem I. Proc. Natl Acad. Sci. USA 98, 4437–4442.
Harris, E.H., Burkhart, B.D., Gillham, N.W. and Boynton, J.E. (1989) Antibiotic resistance mutations in the chloroplast 16S and 23S rRNA genes of Chlamydomonas reinhardtii: correlation of genetic and physical maps of the chloroplast genome. Genetics, 123, 281–292.
Hippler, M., Redding, K. and Rochaix, J.D. (1998) Chlamydomonas genetics, a tool for the study of bioenergetic pathways. Biochim. Biophys. Acta 1367, 1–62.
Ikeda, Y., Komura, M., Watanabe, M., Minami, C., Koike, H., Itoh, S., Kashino, Y. and Satoh, K. (2008) Photosystem I complexes associated with fucoxanthin-chlorophyll-binding proteins from a marine centric diatom, Chaetoceros gracilis. Biochim. Biophys. Acta – Bioenerg. 1777, 351–361.
Jiang, M., Cao, Y., Guo, Z., Chen, M., Chen, X. and Guo, Z. (2007) Menaquinone biosynthesis in Escherichia coli: identification of 2-Succinyl-5-enolpyruvyl-6-hydroxy-3-cyclohexene-1-carboxylate as a novel intermediate and re-evaluation of MenD activity†. Biochemistry, 46, 10979–10989.
Jiang, M., Chen, X., Guo, Z., Cao, Y., Chen, M. and Guo, Z. (2008) Identification and characterization of (1R, 6R) -2-Succinyl-6-hydroxy-2,4-cyclohexadiene-1-carboxylate synthase in the menaquinone biosynthesis of Escherichia coli. Biochemistry, 47, 3426–3434.
Johnson, T.W., Shen, G., Zybailov, B. et al. (2000) Recruitment of a foreign quinone into the A1 site of photosystem I. I. genetic and physiological characterization of phylloquinone biosynthetic pathway mutants in Synechocystis sp. PCC 6803. J. Biol. Chem. 275, 8523–8530.
Johnson, T.W., Zybailov, B., Jones, A.D., Bittl, R., Zech, S., Stehlik, D., Golbeck, J.H. and Chitnis, P.R. (2001) Recruitment of a foreign quinone into the A1 site of photosystem I: in vivo replacement of plastoquinone-9 by media-supplemented naphthoquinones in phylloquinone biosynthetic pathway mutants of synechocystis sp. PCC 6803. J. Biol. Chem. 276, 39512–39521.
Johnson, T.W., Naithani, S., Stewart, C., Zybailov, B., Jones, A.D., Golbeck, J.H. and Chitnis, P.R. (2003) The menD and menE homologs code for 2-succinyl-6-hydroxyl-2,4-cyclohexadiene-1-carboxylate synthase and O-succinylbenzoic acid-CoA synthase in the phylloquinone biosynthetic pathway of Synechocystis sp. PCC 6803. Biochim. Biophys. Acta – Bioenerg. 1557, 67–76.
Joliot, P. and Joliot, A. (1999) In vivo analysis of the electron transfer within photosystem I: are the two phylloquinones involved? Biochemistry, 38, 11130–11136.
Kim, H.U. (2008) The AAE14 gene encodes the Arabidopsis o-succinylbenzoyl- CoA ligase that is essential for phylloquinone synthesis and photosystem-I function. Plant J. 54, 272–283.
Kurosu, M. and Begari, E. (2010) Vitamin K2 in electron transport system: are enzymes involved in vitamin K2 biosynthesis promising drug targets? Molecules, 15, 1531–1553.
Lauersen, K.J., Willamme, R., Coosemans, N., Joris, M., Kruse, O. and Remacle, C. (2016) Peroxisomal microbodies are at the crossroads of acetate assimilation in the green microalga Chlamydomonas reinhardtii. Algal Res. 16, 266–274.
Law, A., Thomas, G. and Threlfall, D.R. (1973) 5′-Monohydroxyphylloquinone from Anacystis and Euglena. Phytochemistry, 12, 1999–2004.
Lefebvre-Legendre, L., Rappaport, F., Finazzi, G., Ceol, M., Grivet, C., Hopfgartner, G. and Rochaix, J.D. (2007) Loss of phylloquinone in Chlamydomonas affects plastoquinone pool size and photosystem II synthesis. J. Biol. Chem. 282, 13250–13263.
Liu, Y.G., Mitsukawa, N., Oosumi, T. and Whittier, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457–463.
Lohmann, A., Schöttler, M.A., Bréhélin, C., Kessler, F., Bock, R., Cahoon, E.B. and Dörmann, P. (2006) Deficiency in phylloquinone (vitamin K1) methylation affects prenyl quinone distribution, photosystem I abundance, and anthocyanin accumulation in the Arabidopsis AtmenG mutant. J. Biol. Chem. 281, 40461–40472.
McConnell, M.D., Cowgill, J.B., Baker, P.L., Rappaport, F. and Redding, K.E. (2011) Double reduction of plastoquinone to plastoquinol in Photosystem 1. Biochemistry, 50, 11034–11046.
Meganathan, R. (2001) Biosynthesis of menaquinone (vitamin K2) and ubiquinone (coenzyme Q): a perspective on enzymatic mechanisms. Vitam. Horm. 61, 173–218.
Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M. and Shikanai, T. (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell, 110, 361–371.
Nakagawa, K., Hirota, Y., Sawada, N., Yuge, N., Watanabe, M., Uchino, Y., Okuda, N., Shimomura, Y., Suhara, Y. and Okano, T. (2010) Identification of UBIAD1 as a novel human menaquinone-4 biosynthetic enzyme. Nature, 468, 117–121.
Newman, S.M., Boynton, J.E., Gillham, N.W., Randolph-Anderson, B.L., Johnson, A.M. and Harris, E.H. (1990) Transformation of chloroplast ribosomal RNA genes in Chlamydomonas: molecular and genetic characterization of integration events. Genetics, 126, 875–888.
Omata, T. and Murata, N. (1984) Cytochromes and prenylquinones in preparations of cytoplasmic and thylakoid membranes from the cyanobacterium (blue-green alga) Anacystis nidulans. Biochim. Biophys. Acta 766, 395–402.
Ozawa, S.I., Kosugi, M., Kashino, Y., Sugimura, T. and Takahashi, Y. (2012) 5’-monohydroxyphylloquinone is the dominant naphthoquinone of PSI in the green alga Chlamydomonas reinhardtii. Plant Cell Physiol. 53, 237–243.
Reumann, S., Babujee, L., Ma, C., Wienkoop, S., Siemsen, T., Antonicelli, G.E., Rasche, N., Lüder, F., Weckwerth, W. and Jahn, O. (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell, 19, 3170–3193.
Roberty, S., Bailleul, B., Berne, N., Franck, F. and Cardol, P. (2014) PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol. 204, 81–91.
Rochaix, J.-D. (2002) Chlamydomonas, a model system for studying the assembly and dynamics of photosynthetic complexes. FEBS Lett. 529, 34–38.
Sakuragi, Y., Zybailov, B., Shen, G. et al. (2002) Insertional inactivation of the menG Gene, encoding 2-Phytyl-1, 4-naphthoquinone methyltransferase of Synechocystis sp. PCC 6803, results in the incorporation of 2-phytyl-1, 4-naphthoquinone into the A 1 site and alteration of the equilibrium constant between A1 and FX in photosystem I. Biochemistry 41, 394–405.
Semenov, A.Y., Vassiliev, I.R., Van Der Est, A., Mamedov, M.D., Zybailov, B., Shen, G., Stehlik, D., Diner, B.A., Chitnis, P.R. and Golbeck, J.H. (2000) Recruitment of a foreign qiunone into the a(1) site of photosystem I: Altered kinetics of electron transfer in phylloquinone biosynthetic pathway mutants studied by time-resolved optical, EPR, and electrometric techniques. J. Biol. Chem. 275, 23429–23438.
Shimada, H., Ohno, R., Shibata, M., Ikegami, I., Onai, K., Ohto, M.A. and Takamiya, K.I. (2005) Inactivation and deficiency of core proteins of photosystems I and II caused by genetical phylloquinone and plastoquinone deficiency but retained lamellar structure in a T-DNA mutant of Arabidopsis. Plant J. 41, 627–637.
Shimogawara, K., Fujiwara, S., Grossman, A. and Usuda, H. (1998) High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics, 148, 1821–1828.
Sommer, F., Hippler, M., Biehler, K., Fischer, N. and Rochaix, J.-D. (2003) Comparative analysis of photosensitivity in photosystem I donor and acceptor side mutants of Chlamydomonas reinhardtii. Plant, Cell Environ. 26, 1881–1892.
Stauber, E.J., Busch, A., Naumann, B., Svatos, A. and Hippler, M. (2009) Proteotypic profiling of LHCI from Chlamydomonas reinhardtii provides new insights into structure and function of the complex. Proteomics, 9, 398–408.
Takahashi, H., Clowez, S., Wollman, F.-A., Vallon, O. and Rappaport, F. (2013) Cyclic electron flow is redox-controlled but independent of state transition. Nat. Commun. 4, 1954. doi:10.1038/ncomms2954.
Tikkanen, M., Rantala, S. and Aro, E.-M. (2015) Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. Front. Plant. Sci. 6, 521. doi:10.3389/fpls.2015.00521.
Widhalm, J.R., van Oostende, C., Furt, F. and Basset, G.J.C. (2009) A dedicated thioesterase of the Hotdog-fold family is required for the biosynthesis of the naphthoquinone ring of vitamin K1. Proc. Natl Acad. Sci. USA 106, 5599–5603.
Widhalm, J.R., Ducluzeau, A.L., Buller, N.E., Elowsky, C.G., Olsen, L.J. and Basset, G.J.C. (2012) Phylloquinone (vitamin K1) biosynthesis in plants: two peroxisomal thioesterases of lactobacillales origin hydrolyze 1,4-dihydroxy-2-naphthoyl-coa. Plant J. 71, 205–215.
Wollman, F.A. (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20, 3623–3630.
Yoshida, E., Nakamura, A. and Watanabe, T. (2003) Reversed-phase HPLC determination of chlorophyll a’ and naphthoquinones in photosystem I of red algae: existence of two menaquinone-4 molecules in photosystem I of Cyanidium caldarium. Anal. Sci. 19, 1001–1005.
Ziegler, K., Maldener, I. and Lockau, W. (1989) 5′-monohydroxyphylloquinone as a component of photosystem I. Zeitschrift fur Naturforsch – Sect. C. J. Biosci. 44, 468–472.