CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii
Abstract
In bacteria and energy generating organelles, c-type cytochromes are a class of universal electron carriers with a heme cofactor covalently linked via one or two thioether bonds to a heme binding site. The covalent attachment of heme to apocytochromes is a catalyzed process, taking place via three evolutionarily distinct assembly pathways (Systems I, II, III). System II was discovered in the green alga Chlamydomonas reinhardtii through the genetic analysis of the ccs mutants (cytochrome c synthesis), which display a block in the apo- to holo- form conversion of cytochrome f and c6, the thylakoid lumen resident c-type cytochromes functioning in photosynthesis. Here we show that the gene corresponding to the CCS2 locus encodes a 1,719 amino acid polypeptide and identify the molecular lesions in the ccs2-1 to ccs2-5 alleles. The CCS2 protein displays seven degenerate amino acid repeats, which are variations of the octatricopeptide-repeat motif (OPR) recently recognized in several nuclear-encoded proteins controlling the maturation, stability, or translation of chloroplast transcripts. A plastid site of action for CCS2 is inferred from the finding that GFP fused to the first 100 amino acids of the algal protein localizes to chloroplasts in Nicotiana benthamiana. Here, we discuss the possible functions of CCS2more »
- Authors:
-
- The Ohio State Univ., Columbus, OH (United States). Dept. of Molecular Genetics, Dept. of Biological Chemistry and Pharmacology, and Plant Cellular and Molecular Biology Graduate Program; Athens State Univ., Athens, AL (United States). Dept. of Mathematics, Computer and Natural Sciences
- The Ohio State Univ., Columbus, OH (United States). Dept. of Molecular Genetics, Dept. of Biological Chemistry and Pharmacology
- The Ohio State Univ., Columbus, OH (United States). Dept. of Molecular Genetics, Dept. of Biological Chemistry and Pharmacology, and Plant Cellular and Molecular Biology Graduate Program
- Publication Date:
- Research Org.:
- The Ohio State Univ., Columbus, OH (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1463691
- Grant/Contract Number:
- SC0014562
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 8; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; plastid; photosynthesis; cytochrome c; heme; assembly factor; OPR
Citation Formats
Cline, Sara G., Laughbaum, Isaac A., and Hamel, Patrice P. CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii. United States: N. p., 2017.
Web. doi:10.3389/fpls.2017.01306.
Cline, Sara G., Laughbaum, Isaac A., & Hamel, Patrice P. CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii. United States. https://doi.org/10.3389/fpls.2017.01306
Cline, Sara G., Laughbaum, Isaac A., and Hamel, Patrice P. Thu .
"CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii". United States. https://doi.org/10.3389/fpls.2017.01306. https://www.osti.gov/servlets/purl/1463691.
@article{osti_1463691,
title = {CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii},
author = {Cline, Sara G. and Laughbaum, Isaac A. and Hamel, Patrice P.},
abstractNote = {In bacteria and energy generating organelles, c-type cytochromes are a class of universal electron carriers with a heme cofactor covalently linked via one or two thioether bonds to a heme binding site. The covalent attachment of heme to apocytochromes is a catalyzed process, taking place via three evolutionarily distinct assembly pathways (Systems I, II, III). System II was discovered in the green alga Chlamydomonas reinhardtii through the genetic analysis of the ccs mutants (cytochrome c synthesis), which display a block in the apo- to holo- form conversion of cytochrome f and c6, the thylakoid lumen resident c-type cytochromes functioning in photosynthesis. Here we show that the gene corresponding to the CCS2 locus encodes a 1,719 amino acid polypeptide and identify the molecular lesions in the ccs2-1 to ccs2-5 alleles. The CCS2 protein displays seven degenerate amino acid repeats, which are variations of the octatricopeptide-repeat motif (OPR) recently recognized in several nuclear-encoded proteins controlling the maturation, stability, or translation of chloroplast transcripts. A plastid site of action for CCS2 is inferred from the finding that GFP fused to the first 100 amino acids of the algal protein localizes to chloroplasts in Nicotiana benthamiana. Here, we discuss the possible functions of CCS2 in the heme attachment reaction.},
doi = {10.3389/fpls.2017.01306},
journal = {Frontiers in Plant Science},
number = ,
volume = 8,
place = {United States},
year = {Thu Aug 03 00:00:00 EDT 2017},
month = {Thu Aug 03 00:00:00 EDT 2017}
}
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Works referenced in this record:
Maturation of Plastid c-type Cytochromes
journal, July 2017
- Gabilly, Stéphane T.; Hamel, Patrice P.
- Frontiers in Plant Science, Vol. 8
Identification of an OPR protein involved in the translation initiation of the PsaB subunit of photosystem I
journal, September 2012
- Rahire, Michèle; Laroche, Fabrice; Cerutti, Lorenzo
- The Plant Journal, Vol. 72, Issue 4
Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii
journal, June 2002
- Auchincloss, Andrea H.; Zerges, William; Perron, Karl
- The Journal of Cell Biology, Vol. 157, Issue 6
ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites
journal, January 1999
- Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von
- Protein Science, Vol. 8, Issue 5
Two Chlamydomonas OPR proteins stabilize chloroplast mRNAs encoding small subunits of photosystem II and cytochrome b 6 f
journal, May 2015
- Wang, Fei; Johnson, Xenie; Cavaiuolo, Marina
- The Plant Journal, Vol. 82, Issue 5
The biosynthesis of membrane and soluble plastidic c-type cytochromes of Chlamydomonas reinhardtii is dependent on multiple common gene products.
journal, August 1992
- Howe, G.; Merchant, S.
- The EMBO Journal, Vol. 11, Issue 8
High-Efficiency Transformation of Chlamydomonas reinhardtii by Electroporation
journal, April 1998
- Shimogawara, Kosuke; Fujiwara, Shoko; Grossman, Arthur
- Genetics, Vol. 148, Issue 4
Cytochrome c maturation system on the negative side of bioenergetic membranes: CCB or System IV: Cytochrome c maturation System IV
journal, October 2011
- de Vitry, Catherine
- FEBS Journal, Vol. 278, Issue 22
Biogenesis of respiratory cytochromes in bacteria.
journal, January 1997
- Thöny-Meyer, L.
- Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 3
Structural and Functional Discussion of the Tetra-Trico-Peptide Repeat, a Protein Interaction Module
journal, March 2012
- Zeytuni, Natalie; Zarivach, Raz
- Structure, Vol. 20, Issue 3
A Novel Component of the Disulfide-Reducing Pathway Required for Cytochrome c Assembly in Plastids
journal, January 2011
- Gabilly, Stéphane T.; Kropat, Janette; Karamoko, Mohamed
- Genetics, Vol. 187, Issue 3
Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum
journal, April 2005
- Levitan, A.; Trebitsh, T.; Kiss, V.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 17
I-TASSER: a unified platform for automated protein structure and function prediction
journal, March 2010
- Roy, Ambrish; Kucukural, Alper; Zhang, Yang
- Nature Protocols, Vol. 5, Issue 4
Biochemical requirements for the maturation of mitochondrial c-type cytochromes
journal, January 2009
- Hamel, Patrice; Corvest, Vincent; Giegé, Philippe
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1793, Issue 1
Cytochrome c biogenesis System I: An intricate process catalyzed by a maturase supercomplex?
journal, July 2014
- Verissimo, Andreia F.; Daldal, Fevzi
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7
Cytochrome c biogenesis: the Ccm system
journal, June 2010
- Sanders, Carsten; Turkarslan, Serdar; Lee, Dong-Woo
- Trends in Microbiology, Vol. 18, Issue 6
Genes required for cytochrome c synthesis inBacillus subtilis: B. subtilis cytochrome c synthesis
journal, May 2000
- Le Brun, Nick E.; Bengtsson, Jenny; Hederstedt, Lars
- Molecular Microbiology, Vol. 36, Issue 3
Cytochrome c assembly
journal, January 2013
- Mavridou, Despoina A. I.; Ferguson, Stuart J.; Stevens, Julie M.
- IUBMB Life, Vol. 65, Issue 3
New Insights into the Unique Structure of the F 0 F 1 -ATP Synthase from the Chlamydomonad Algae Polytomella sp. and Chlamydomonas reinhardtii
journal, April 2007
- van Lis, Robert; Mendoza-Hernández, Guillermo; Groth, Georg
- Plant Physiology, Vol. 144, Issue 2
I-TASSER server for protein 3D structure prediction
journal, January 2008
- Zhang, Yang
- BMC Bioinformatics, Vol. 9, Issue 1
Evolution of an atypical de-epoxidase for photoprotection in the green lineage
journal, September 2016
- Li, Zhirong; Peers, Graham; Dent, Rachel M.
- Nature Plants, Vol. 2, Issue 10
Structural basis for specific single-stranded RNA recognition by designer pentatricopeptide repeat proteins
journal, April 2016
- Shen, Cuicui; Zhang, Delin; Guan, Zeyuan
- Nature Communications, Vol. 7, Issue 1
Cytochrome c Biogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control
journal, August 2009
- Kranz, R. G.; Richard-Fogal, C.; Taylor, J. -S.
- Microbiology and Molecular Biology Reviews, Vol. 73, Issue 3
Pentatricopeptide Repeat Proteins in Plants
journal, April 2014
- Barkan, Alice; Small, Ian
- Annual Review of Plant Biology, Vol. 65, Issue 1
Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast
journal, May 2007
- Raynaud, C.; Loiselay, C.; Wostrikoff, K.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 21
Identification of a Chlamydomonas plastidial 2-lysophosphatidic acid acyltransferase and its use to engineer microalgae with increased oil content
journal, May 2016
- Yamaoka, Yasuyo; Achard, Dorine; Jang, Sunghoon
- Plant Biotechnology Journal, Vol. 14, Issue 11
The Octatricopeptide Repeat Protein Raa8 Is Required for Chloroplast trans Splicing
journal, July 2015
- Marx, Christina; Wünsch, Christiane; Kück, Ulrich
- Eukaryotic Cell, Vol. 14, Issue 10
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
journal, September 2004
- Pollock, Steve V.; Prout, Davey L.; Godfrey, Ashley C.
- Plant Molecular Biology, Vol. 56, Issue 1
Structure of human mitochondrial RNA polymerase
journal, September 2011
- Ringel, Rieke; Sologub, Marina; Morozov, Yaroslav I.
- Nature, Vol. 478, Issue 7368
Subunit–subunit interactions and overall topology of the dimeric mitochondrial ATP synthase of Polytomella sp.
journal, August 2010
- Cano-Estrada, Araceli; Vázquez-Acevedo, Miriam; Villavicencio-Queijeiro, Alexa
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 8
Incorporation of glutamine repeats makes protein oligomerize: implications for neurodegenerative diseases.
journal, July 1995
- Stott, K.; Blackburn, J. M.; Butler, P. J.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 14
I-TASSER server for protein 3D structure prediction
journal, January 2008
- Zhang, Yang
- BMC Bioinformatics, Vol. 9, Issue 1
A Homolog of Prokaryotic Thiol Disulfide Transporter CcdA Is Required for the Assembly of the Cytochrome b 6 f Complex in Arabidopsis Chloroplasts
journal, May 2004
- Page, M. L. Dudley; Hamel, Patrice P.; Gabilly, Stéphane T.
- Journal of Biological Chemistry, Vol. 279, Issue 31
The FLP proteins act as regulators of chlorophyll synthesis in response to light and plastid signals in Chlamydomonas
journal, January 2005
- Falciatore, A.
- Genes & Development, Vol. 19, Issue 1
The flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii
journal, April 2001
- Fischer, N.; Rochaix, J. -D.
- Molecular Genetics and Genomics, Vol. 265, Issue 5
Analysis of Sp1 in vivo reveals mutiple transcriptional domains, including a novel glutamine-rich activation motif
journal, December 1988
- Courey, Albert J.; Tjian, Robert
- Cell, Vol. 55, Issue 5
TPR proteins: the versatile helix
journal, December 2003
- D'Andrea, L.
- Trends in Biochemical Sciences, Vol. 28, Issue 12
Complementation of a Chlamydomonas reinhardtii mutant using a genomic cosmid library
journal, February 1994
- Purton, Saul; Rochaix, Jean-David
- Plant Molecular Biology, Vol. 24, Issue 3
New Insights into the Unique Structure of the F 0 F 1 -ATP Synthase from the Chlamydomonad Algae Polytomella sp. and Chlamydomonas reinhardtii
journal, April 2007
- van Lis, Robert; Mendoza-Hernández, Guillermo; Groth, Georg
- Plant Physiology, Vol. 144, Issue 2
Identification and Expression Analysis of cDNA Encoding a Chloroplast Recombination Protein REC1, the Chloroplast RecA Homologue in Chlamydomonas reinhardtii
journal, January 2003
- Nakazato, Emi; Fukuzawa, Hideya; Tabata, Satoshi
- Bioscience, Biotechnology, and Biochemistry, Vol. 67, Issue 12
The chemistry and biochemistry of heme c: functional bases for covalent attachment
journal, January 2008
- Bowman, Sarah E. J.; Bren, Kara L.
- Natural Product Reports, Vol. 25, Issue 6
Dual functions of the nucleus-encoded factor TDA1 in trapping and translation activation of atpA transcripts in Chlamydomonas reinhardtii chloroplasts: Trapping and translation of chloroplast atpA transcripts
journal, July 2011
- Eberhard, Stephan; Loiselay, Christelle; Drapier, Dominique
- The Plant Journal, Vol. 67, Issue 6
Maturation of thylakoid lumen proteins proceeds post-translationally through an intermediate in vivo.
journal, March 1993
- Howe, G.; Merchant, S.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 5
Spontaneous Dominant Mutations in Chlamydomonas Highlight Ongoing Evolution by Gene Diversification
journal, March 2015
- Boulouis, Alix; Drapier, Dominique; Razafimanantsoa, Hélène
- The Plant Cell, Vol. 27, Issue 4
The Nucleus-Encoded trans -Acting Factor MCA1 Plays a Critical Role in the Regulation of Cytochrome f Synthesis in Chlamydomonas Chloroplasts
journal, January 2011
- Boulouis, Alix; Raynaud, Cécile; Bujaldon, Sandrine
- The Plant Cell, Vol. 23, Issue 1
WoLF PSORT: protein localization predictor
journal, May 2007
- Horton, P.; Park, K. -J.; Obayashi, T.
- Nucleic Acids Research, Vol. 35, Issue Web Server
The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions
journal, March 1998
- Das, A. K.
- The EMBO Journal, Vol. 17, Issue 5
A novel multifunctional factor involved in trans-splicing of chloroplast introns in Chlamydomonas
journal, January 2006
- Merendino, L.
- Nucleic Acids Research, Vol. 34, Issue 1
Two adjacent nuclear genes are required for functional complementation of a chloroplast trans-splicing mutant from Chlamydomonas reinhardtii: C. reinhardtii chloroplast trans-splicing
journal, July 2005
- Balczun, Carsten; Bunse, Astrid; Hahn, Daniela
- The Plant Journal, Vol. 43, Issue 5
Cytochrome c biogenesis: the Ccm system
journal, June 2010
- Sanders, Carsten; Turkarslan, Serdar; Lee, Dong-Woo
- Trends in Microbiology, Vol. 18, Issue 6
The biosynthesis of membrane and soluble plastidic c-type cytochromes of Chlamydomonas reinhardtii is dependent on multiple common gene products.
journal, August 1992
- Howe, G.; Merchant, S.
- The EMBO Journal, Vol. 11, Issue 8
Biogenesis of respiratory cytochromes in bacteria.
journal, January 1997
- Thöny-Meyer, L.
- Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 3
Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast
journal, May 2007
- Raynaud, C.; Loiselay, C.; Wostrikoff, K.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 21
Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii
journal, June 2002
- Auchincloss, Andrea H.; Zerges, William; Perron, Karl
- The Journal of Cell Biology, Vol. 157, Issue 6
An overview of pentatricopeptide repeat proteins and their applications
text, January 2015
- Manna, Sam
- figshare
Functional Analysis of a Divergent System II Protein, Ccs1, Involved in c -Type Cytochrome Biogenesis
journal, November 2002
- Dreyfuss, Beth Welty; Hamel, Patrice P.; Nakamoto, Stacie S.
- Journal of Biological Chemistry, Vol. 278, Issue 4
Maturation of Plastid c-type Cytochromes
journal, July 2017
- Gabilly, Stéphane T.; Hamel, Patrice P.
- Frontiers in Plant Science, Vol. 8
Evolution of an atypical de-epoxidase for photoprotection in the green lineage
journal, September 2016
- Li, Zhirong; Peers, Graham; Dent, Rachel M.
- Nature Plants, Vol. 2, Issue 10
Continuous evolution of base editors with expanded target compatibility and improved activity
journal, July 2019
- Thuronyi, Benjamin W.; Koblan, Luke W.; Levy, Jonathan M.
- Nature Biotechnology, Vol. 37, Issue 9
A Novel Component of the Disulfide-Reducing Pathway Required for Cytochrome c Assembly in Plastids
journal, January 2011
- Gabilly, Stéphane T.; Kropat, Janette; Karamoko, Mohamed
- Genetics, Vol. 187, Issue 3
Structural and Functional Discussion of the Tetra-Trico-Peptide Repeat, a Protein Interaction Module
journal, March 2012
- Zeytuni, Natalie; Zarivach, Raz
- Structure, Vol. 20, Issue 3
Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum
journal, April 2005
- Levitan, A.; Trebitsh, T.; Kiss, V.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 17
Two Chlamydomonas OPR proteins stabilize chloroplast mRNAs encoding small subunits of photosystem II and cytochrome b 6 f
journal, May 2015
- Wang, Fei; Johnson, Xenie; Cavaiuolo, Marina
- The Plant Journal, Vol. 82, Issue 5
ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites
journal, January 1999
- Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von
- Protein Science, Vol. 8, Issue 5
Cytochrome c biogenesis in mitochondria - Systems III and V: Cytochrome c biogenesis in mitochondria
journal, August 2011
- Allen, James W. A.
- FEBS Journal, Vol. 278, Issue 22
Variant c-type cytochromes as probes of the substrate specificity of the E. coli cytochrome c maturation (Ccm) apparatus
journal, March 2009
- Allen, James W. A.; Sawyer, Elizabeth B.; Ginger, Michael L.
- Biochemical Journal, Vol. 419, Issue 1
Mutations in Cytochrome Assembly and Periplasmic Redox Pathways in Bordetella pertussis
journal, June 2005
- Feissner, R. E.; Beckett, C. S.; Loughman, J. A.
- Journal of Bacteriology, Vol. 187, Issue 12
GATEWAY™ vectors for Agrobacterium-mediated plant transformation
journal, May 2002
- Karimi, Mansour; Inzé, Dirk; Depicker, Ann
- Trends in Plant Science, Vol. 7, Issue 5, p. 193-195
An overview of pentatricopeptide repeat proteins and their applications
journal, June 2015
- Manna, Sam
- Biochimie, Vol. 113
A novel multifunctional factor involved in trans-splicing of chloroplast introns in Chlamydomonas
journal, January 2006
- Merendino, L.
- Nucleic Acids Research, Vol. 34, Issue 1
CcsBA is a cytochrome c synthetase that also functions in heme transport
journal, June 2009
- Frawley, E. R.; Kranz, R. G.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 25
Cytochrome c assembly
journal, January 2013
- Mavridou, Despoina A. I.; Ferguson, Stuart J.; Stevens, Julie M.
- IUBMB Life, Vol. 65, Issue 3
Redox Processes Controlling the Biogenesis of c -Type Cytochromes
journal, November 2010
- Bonnard, Géraldine; Corvest, Vincent; Meyer, Etienne H.
- Antioxidants & Redox Signaling, Vol. 13, Issue 9
WoLF PSORT: protein localization predictor
journal, May 2007
- Horton, P.; Park, K. -J.; Obayashi, T.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation
journal, July 2007
- Nakagawa, Tsuyoshi; Kurose, Takayuki; Hino, Takeshi
- Journal of Bioscience and Bioengineering, Vol. 104, Issue 1
Identification and Expression Analysis of cDNA Encoding a Chloroplast Recombination Protein REC1, the Chloroplast RecA Homologue in Chlamydomonas reinhardtii
journal, January 2003
- Nakazato, Emi; Fukuzawa, Hideya; Tabata, Satoshi
- Bioscience, Biotechnology, and Biochemistry, Vol. 67, Issue 12
The Nucleus-Encoded trans -Acting Factor MCA1 Plays a Critical Role in the Regulation of Cytochrome f Synthesis in Chlamydomonas Chloroplasts
journal, January 2011
- Boulouis, Alix; Raynaud, Cécile; Bujaldon, Sandrine
- The Plant Cell, Vol. 23, Issue 1
Maturation of thylakoid lumen proteins proceeds post-translationally through an intermediate in vivo.
journal, March 1993
- Howe, G.; Merchant, S.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 5
The Plastid-encoded ccsA Gene Is Required for Heme Attachment to Chloroplast c-type Cytochromes
journal, March 1996
- Merchant, S.
- Journal of Biological Chemistry, Vol. 271, Issue 9
WebLogo: A Sequence Logo Generator
journal, May 2004
- Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
- Genome Research, Vol. 14, Issue 6, p. 1188-1190
Cytochrome c biogenesis System I: An intricate process catalyzed by a maturase supercomplex?
journal, July 2014
- Verissimo, Andreia F.; Daldal, Fevzi
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7
The flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii
journal, April 2001
- Fischer, N.; Rochaix, J. -D.
- Molecular Genetics and Genomics, Vol. 265, Issue 5
Genetic Analysis of Chloroplast c-Type Cytochrome Assembly in Chlamydomonas reinhardtii: One Chloroplast Locus and at Least Four Nuclear Loci Are Required for Heme Attachment
journal, February 1998
- Xie, Zhiyi; Culler, Duane; Dreyfuss, Beth Welty
- Genetics, Vol. 148, Issue 2
Gene isolation through genomic complementation using an indexed library of Chlamydomonas reinhardtii DNA
journal, February 1994
- Zhang, Hongtao; Herman, Patricia L.; Weeks, Donald P.
- Plant Molecular Biology, Vol. 24, Issue 4
A Gamete-specific, Sex-limited Homeodomain Protein in Chlamydomonas
journal, December 1998
- Kurvari, Venkatesh; Grishin, Nick V.; Snell, William J.
- The Journal of Cell Biology, Vol. 143, Issue 7
A Gamete-specific, Sex-limited Homeodomain Protein in Chlamydomonas
journal, December 1998
- Kurvari, Venkatesh; Grishin, Nick V.; Snell, William J.
- The Journal of Cell Biology, Vol. 143, Issue 7
Ccs1 , a Nuclear Gene Required for the Post-translational Assembly of Chloroplast c -Type Cytochromes
journal, December 1997
- Inoue, Kaori; Dreyfuss, Beth Welty; Kindle, Karen L.
- Journal of Biological Chemistry, Vol. 272, Issue 50
Cytochrome c Biogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control
journal, August 2009
- Kranz, R. G.; Richard-Fogal, C.; Taylor, J. -S.
- Microbiology and Molecular Biology Reviews, Vol. 73, Issue 3
Structural basis for specific single-stranded RNA recognition by designer pentatricopeptide repeat proteins
journal, April 2016
- Shen, Cuicui; Zhang, Delin; Guan, Zeyuan
- Nature Communications, Vol. 7, Issue 1
Increased Efficiency of Cloning Large DNA Fragments Using a Lower Copy Number Plasmid
journal, May 2002
- Feng, T.; Li, Z.; Jiang, W.
- BioTechniques, Vol. 32, Issue 5
Operation of trans-thylakoid thiol-metabolizing pathways in photosynthesis
journal, January 2013
- Karamoko, Mohamed; Gabilly, Stéphane T.; Hamel, Patrice P.
- Frontiers in Plant Science, Vol. 4
Incorporation of glutamine repeats makes protein oligomerize: implications for neurodegenerative diseases.
journal, July 1995
- Stott, K.; Blackburn, J. M.; Butler, P. J.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 14
RAP, the Sole Octotricopeptide Repeat Protein in Arabidopsis , Is Required for Chloroplast 16S rRNA Maturation
journal, February 2014
- Kleinknecht, Laura; Wang, Fei; Stübe, Roland
- The Plant Cell, Vol. 26, Issue 2
Subunit–subunit interactions and overall topology of the dimeric mitochondrial ATP synthase of Polytomella sp.
journal, August 2010
- Cano-Estrada, Araceli; Vázquez-Acevedo, Miriam; Villavicencio-Queijeiro, Alexa
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 8
Composition and function of cytochrome c biogenesis System II: Cytochrome c biogenesis System II
journal, October 2011
- Simon, Jörg; Hederstedt, Lars
- FEBS Journal, Vol. 278, Issue 22
Spontaneous Dominant Mutations in Chlamydomonas Highlight Ongoing Evolution by Gene Diversification
journal, March 2015
- Boulouis, Alix; Drapier, Dominique; Razafimanantsoa, Hélène
- The Plant Cell, Vol. 27, Issue 4
CCS5, a Thioredoxin-like Protein Involved in the Assembly of Plastid c -Type Cytochromes
journal, July 2010
- Gabilly, Stéphane T.; Dreyfuss, Beth Welty; Karamoko, Mohamed
- Journal of Biological Chemistry, Vol. 285, Issue 39
RAP, the Sole Octotricopeptide Repeat Protein in Arabidopsis , Is Required for Chloroplast 16S rRNA Maturation
journal, February 2014
- Kleinknecht, Laura; Wang, Fei; Stübe, Roland
- The Plant Cell, Vol. 26, Issue 2
Four genes are required for the system II cytochrome c biogenesis pathway in Bordetella pertussis , a unique bacterial model : A bacterial model for system II cytochrome
journal, November 2000
- Beckett, Caroline S.; Loughman, Jennifer A.; Karberg, Katherine A.
- Molecular Microbiology, Vol. 38, Issue 3
The Octatricopeptide Repeat Protein Raa8 Is Required for Chloroplast trans Splicing
journal, July 2015
- Marx, Christina; Wünsch, Christiane; Kück, Ulrich
- Eukaryotic Cell, Vol. 14, Issue 10
Increased Efficiency of Cloning Large DNA Fragments Using a Lower Copy Number Plasmid
journal, May 2002
- Feng, T.; Li, Z.; Jiang, W.
- BioTechniques, Vol. 32, Issue 5
CcsBA is a cytochrome c synthetase that also functions in heme transport
journal, June 2009
- Frawley, E. R.; Kranz, R. G.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 25
Pentatricopeptide Repeat Proteins in Plants
journal, April 2014
- Barkan, Alice; Small, Ian
- Annual Review of Plant Biology, Vol. 65, Issue 1
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation
journal, July 2007
- Nakagawa, Tsuyoshi; Kurose, Takayuki; Hino, Takeshi
- Journal of Bioscience and Bioengineering, Vol. 104, Issue 1
Redox Processes Controlling the Biogenesis of c -Type Cytochromes
journal, November 2010
- Bonnard, Géraldine; Corvest, Vincent; Meyer, Etienne H.
- Antioxidants & Redox Signaling, Vol. 13, Issue 9
The FLP proteins act as regulators of chlorophyll synthesis in response to light and plastid signals in Chlamydomonas
journal, January 2005
- Falciatore, A.
- Genes & Development, Vol. 19, Issue 1
The chemistry and biochemistry of heme c: functional bases for covalent attachment
journal, January 2008
- Bowman, Sarah E. J.; Bren, Kara L.
- Natural Product Reports, Vol. 25, Issue 6
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
journal, September 2004
- Pollock, Steve V.; Prout, Davey L.; Godfrey, Ashley C.
- Plant Molecular Biology, Vol. 56, Issue 1
Structure of human mitochondrial RNA polymerase
journal, September 2011
- Ringel, Rieke; Sologub, Marina; Morozov, Yaroslav I.
- Nature, Vol. 478, Issue 7368
TPR proteins: the versatile helix
journal, December 2003
- D'Andrea, L.
- Trends in Biochemical Sciences, Vol. 28, Issue 12
Mechanistic Insight into Pentatricopeptide Repeat Proteins as Sequence-Specific RNA-Binding Proteins for Organellar RNAs in Plants
journal, May 2012
- Nakamura, T.; Yagi, Y.; Kobayashi, K.
- Plant and Cell Physiology, Vol. 53, Issue 7
Identification of a Chlamydomonas plastidial 2-lysophosphatidic acid acyltransferase and its use to engineer microalgae with increased oil content
journal, May 2016
- Yamaoka, Yasuyo; Achard, Dorine; Jang, Sunghoon
- Plant Biotechnology Journal, Vol. 14, Issue 11
Biochemical requirements for the maturation of mitochondrial c-type cytochromes
journal, January 2009
- Hamel, Patrice; Corvest, Vincent; Giegé, Philippe
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1793, Issue 1
Role of heme in the biosynthesis of cytochrome c6.
journal, February 1994
- Howe, G.; Merchant, S.
- Journal of Biological Chemistry, Vol. 269, Issue 8
High-Efficiency Transformation of Chlamydomonas reinhardtii by Electroporation
journal, April 1998
- Shimogawara, Kosuke; Fujiwara, Shoko; Grossman, Arthur
- Genetics, Vol. 148, Issue 4
Genetic Analysis of Chloroplast c-Type Cytochrome Assembly in Chlamydomonas reinhardtii: One Chloroplast Locus and at Least Four Nuclear Loci Are Required for Heme Attachment
journal, February 1998
- Xie, Zhiyi; Culler, Duane; Dreyfuss, Beth Welty
- Genetics, Vol. 148, Issue 2
Works referencing / citing this record:
GreenCut protein CPLD49 of Chlamydomonas reinhardtii associates with thylakoid membranes and is required for cytochrome b 6 f complex accumulation
journal, May 2018
- Wittkopp, Tyler M.; Saroussi, Shai; Yang, Wenqiang
- The Plant Journal, Vol. 94, Issue 6