PL EN


Preferences help
enabled [disable] Abstract
Number of results
2008 | 55 | 3 | 417-433
Article title

Proteins involved in maturation pathways of plant mitochondrial and plastid c-type cytochromes

Authors
Content
Title variants
Languages of publication
EN
Abstracts
EN
c-type cytochromes are characterized by the presence of two covalent bonds linking heme to apocytochrome and by the heme attachment motif in the apoprotein. Several molecular systems for the maturation of c-type cytochromes have evolved in different organisms. The best characterized are three of them: system I, system II and system III. Heme is synthesized in bacterial cytoplasm, in plastids, and in animal and fungal mitochondria. Therefore the maturation of bacterial and plastid c-type cytochromes involves the transport of heme and apocytochrome from the n-side to the p-side of the respective biological membranes and the formation of the covalent bond at the p-side. It should be underlined that the site of the c-type apocytochrome synthesis is also distinct from the site of its functioning. The aim of this review is to present the current state of knowledge concerning the structure and function of two systems - system I and system II - in the maturation of plant mitochondrial and plastid c-type cytochromes, respectively.
Publisher

Year
Volume
55
Issue
3
Pages
417-433
Physical description
Dates
published
2008
received
2007-08-14
revised
2008-07-11
accepted
2008-07-31
(unknown)
2008-09-04
Contributors
author
  • Department of Molecular and Cellular Biology, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University, Poznań, Poland
References
  • Ahuja U, Thöny-Meyer L (2003) Dynamic features of a heme delivery system for cytochrome c maturation. J Biol Chem 278: 52061-52070.
  • Ahuja U, Thöny-Meyer L (2005) CcmD is involved in complex formation between CcmC and the heme chaperone CcmE during cytochrome c maturation. J Biol Chem 280: 236-243.
  • Allen JWA, Ferguson SJ (2006) What is the substrate specificity of the System I cytochrome c biogenesis apparatus? Biochem Soc Trans 34: 150-151.
  • Allen JWA, Daltrop O, Stevens JM, Ferguson SJ (2003) c-type cytochromes: diverse structures and biogenesis systems pose evolutionary problems. Philos Trans R Soc Lond B Biol Sci 358: 255-266.
  • Allen JWA, Ginger ML, Ferguson SJ (2004a) Complexity and diversity in c-type cytochrome biogenesis systems. Biochem Soc Trans 33: 145-146.
  • Allen JWA, Ginger ML, Ferguson SJ (2004b) Maturation of the unusual single-cysteine (XXXCH) mitochondrial c-type cytochromes found in trypanosomatids must occur through a novel biogenesis pathway. Biochem J 383: 537-542.
  • Allen JWA, Harvat EM, Stevens JM, Ferguson SJ (2006) A variant system I for cytochrome c biogenesis in archaea and some bacteria has a novel CcmE and no CcmH. FEBS Lett 580: 4827-4834.
  • Allen JWA, Jackson AP, Rigden DJ, Willis AC, Ferguson SJ, Ginger ML (2008) Order within a mosaic distribution of mitochondrial c-type cytochrome biogenesis systems? FEBS J 275: 2385-2402.
  • Baker HM, Anderson BF, Baker EN (2003) Dealing with iron: common structural principles in proteins that transport iron and heme. Proc Natl Acad Sci USA 100: 3579-3583.
  • Balmer Y, Koller A, del Val G, Manieri W, Schürmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci 100: 370-375.
  • Balmer Y, Vensel WH, Hurkman WJ, Buchanan BB (2006) Thioredoxin target proteins in chloroplast thylakoid membranes. Antioxid Redox Signal 8: 1829-1834.
  • Beckman DL, Trawick DR, Kranz RG (1992) Bacterial cytochromes c biogenesis. Genes Dev 6: 268-283.
  • Bernard DG, Gabilly ST, Dujardin G, Merchant S, Hamel PP (2003) Overlapping specificities of the mitochondrial cytochrome c and c1 heme lyases. J Biol Chem 278: 49732-49742.
  • Bernard DG, Quevillon-Cheruel S, Merchant S, Guiard B, Hamel PP (2005) Cyc2p, a membrane-bound flavoprotein involved in the maturation of mitochondrial c-type cytochromes. J Biol Chem 280: 39852-39859.
  • Bonnard G, Grienenberger JM (1995) A gene proposed to encode a transmembrane domain of an ABC transporter is expressed in wheat mitochondria. Mol Gen Genet 246: 91-99.
  • Choquet Y, Stern DB, Wostrikoff K, Kuras R, Girard-Bascou J, Wollman F-A (1998) Translation of cytochrome f is autoregulated through the 5' untranslated region of petA mRNA in Chlamydomonas chloroplasts. Proc Natl Acad Sci USA 95: 4380-4385.
  • Christensen O, Harvat EM, Thöny-Meyer L, Ferguson SJ, Stevens JM (2007) Loss of ATP hydrolysis activity by CcmAB results in loss of c-type cytochrome synthesis and incomplete processing of CcmE. FEBS J 274: 2322-2332.
  • Cianciotto NP, Cornelis P, Baysse C (2005) Impact of the bacterial type I cytochrome c maturation system on different biological processes. Mol Microbiol 56: 1408-1415.
  • Clifton SW, Minx P, Fauron CMR, Gibson M, Allen JO, Sun H, Thompson M, Barbazuk WB, Kanuganti S, Tayloe C, Meyer L, Wilson RK, Newton KJ (2004) Sequence and comparative analysis of the maize NB mitochondrial genome. Plant Physiol 136: 3486-3503.
  • Cook GM, Poole RK (2000) Oxidase and periplasmic cytochrome assembly in Escherichia coli K-12: CydDC and CcmAB are not required for haem-membrane association. Microbiology 146: 527-536.
  • Cornah JE, Roper JM, Pal Singh D, Smith AG (2002) Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and nonphotosynthetic cells of pea (Pisum sativum L.). Biochem J 362: 423-432.
  • Diekert K, de Kroon AIPM, Ahting U, Niggemeyer B, Neupert W, de Kruijff B, Lill R (2001) Apocytochrome c requires the TOM complex for translocation across the mitochondrial outer membrane. EMBO J 20: 5626-5635.
  • Dreyfuss BW, Hamel PP, Nakamoto SS, Merchant S (2003) Functional analysis of a divergent system II protein, Ccs1, involved in c-type cytochrome biogenesis. J Biol Chem 278: 2604-2613.
  • Enggist E, Thöny-Meyer L (2003) The C-terminal flexible domain of the heme chaperone CcmE is important but not essential for its function. J Bacteriol 185: 3821-3827.
  • Enggist E, Schneider MJ, Schulz H, Thöny-Meyer L (2003) Biochemical and mutational characterization of the heme chaperone CcmE reveals a heme binding site. J Bacteriol 185: 175-183.
  • Faivre-Nitschke SE, Nazoa P, Gualberto JM, Grienenberger JM, Bonnard G (2001) Wheat mitochondria ccmB encodes the membrane domain of a putative ABC transporter involved in cytochrome c biogenesis. Biochim Biophys Acta 1519: 199-208.
  • Feissner RE, Richard-Fogal CL, Frawley ER, Kranz RG (2006a) ABC transporter-mediated release of a haem chaperone allows cytochrome c biogenesis. Mol Microbiol 61: 219-231.
  • Feissner RE, Richard-Fogal CL, Frawley ER, Loughman JA, Earley KW, Kranz RG (2006b) Recombinant cytochromes c biogenesis systems I and II and analysis of haem delivery pathways in Escherichia coli. Mol Microbiol 60: 563-577.
  • Ferguson SJ (2001) Keilin's cytochromes: how bacteria use them, vary them and make them. Biochem Soc Trans 29: 629-640.
  • Giegé P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96: 15324-15329.
  • Giegé P, Rayapuram N, Meyer EH, Grienenberger J-M, Bonnard G (2004) CcmFC involved in cytochrome c maturation is present in a large sized complex in wheat mitochondria. FEBS Lett 563: 165-169.
  • Giegé P, Grienenberger JM, Bonnard G (2008) Cytochrome c biogenesis in mitochondria. Mitochondrion 8: 61-73.
  • Goldman BS, Kranz RG (2001) ABC transporters associated with cytochrome c biogenesis. Res Microbiol 152: 323-329.
  • Goldman BS, Beck DL, Monika EM, Kranz RG (1998) Transmembrane heme delivery systems. Proc Natl Acad Sci USA 95: 5003-5008.
  • Gonzalez DH, Bonnard G, Grienenberger J-M (1993) A gene involved in the biogenesis of cytochromes is cotranscribed with a ribosomal protein gene in wheat mitochondria. Curr Genet 24: 248-255.
  • Hamel PP, Dreyfuss BW, Xie Z, Gabilly ST, Merchant S (2003) Essential histidine and tryptophan residues in CcsA, a system II polytopic cytochrome c biogenesis protein. J Biol Chem 278: 2593-2603.
  • Handa H (2003) The complete nucleotide sequence and RNA editing content of the mitochondrial genome of rapeseed (Brassica napus L.): comparative analysis of the mitochondrial genomes of rapeseed and Arabidopsis thaliana. Nucleic Acids Res 31: 5907-5916.
  • Handa H, Bonnard G, Grienenberger J-M (1996) The rapeseed mitochondrial gene encoding a homologue of the bacterial protein Ccl1 is divided into two independently transcribed reading frames. Mol Gen Genet 252: 292-302.
  • Hazle T, Bonen L (2007) Comparative analysis of sequences preceding protein-coding mitochondrial genes in flowering plants. Mol Biol Evol 24: 1101-1112.
  • Hell K (2008) The Erv1-Mia40 disulfide relay system in the IMS of mitochondria. Biochim Biophys Acta 1783: 601-609.
  • Howe CJ, Schlarb-Ridley BG, Wastl J, Purton S, Bendall DS (2006) The novel cytochrome c6 of chloroplasts: a case of evolutionary bricolage ? J Exp Bot 57: 13-22.
  • Inoue K, Dreyfuss BW, Kindle KL, Stern DB, Merchant S, Sodeinde OA (1997) Ccs1, a nuclear gene required for the post-translational assembly of chloroplast c-type cytochromes. J Biol Chem 272: 31747-31754.
  • Jekabsons W, Schuster W (1995) orf250 encodes a second subunit of an ABC-type heme transporter in Oenothera mitochondria. Mol Gen Genet 246: 166-173.
  • Katzen F, Deshmukh M, Daldal F, Beckwith J (2002) Evolutionary domain fusion expanded the substrate specificity of the transmembrane electron transporter DsbD. EMBO J 21: 3960-3969.
  • Kranz R, Lill R, Goldman B, Bonnard G, Merchant S (1998) Molecular mechanisms of cytochrome c biogenesis: three distinct systems. Mol Microbiol 29: 383-396.
  • Kubo T, Nishizawa S, Sugawara A, Itchoda N, Estiati A, Mikami T (2000) The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNACys(GCA). Nucleic Acids Res 28: 2571-2576.
  • Lang BF, Burger G, O'Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997) An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387: 493-497.
  • Lee J-H, Harvat EM, Stevens JM, Ferguson SJ, Saier Jr MH (2007) Evolutionary origins of members of a superfamily of integral membrane cytochrome c biogenesis proteins. Biochim Biophys Acta 1768: 2164-2181.
  • Lennartz K, Plücken H, Seidler A, Westhoff P, Bechtold N, Meierhoff K (2001) HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b6f complex in Arabidopsis. Plant Cell 13: 2539-2551.
  • Lennartz K, Bossmann S, Westhoff P, Bechtold N, Meierhoff K (2006) HCF153, a novel nuclear-encoded factor necessary during a post-translational step in biogenesis of the cytochrome b6f complex. Plant J 45: 101-112.
  • Levitan A, Danon A, Lisowsky T (2004) Unique features of plant mitochondrial sulfhydryl oxidase. J Biol Chem 279: 20002-20008.
  • Lister R, Chew O, Rudhe C, Lee M-N, Whelan J (2001) Arabidopsis thaliana ferrochelatase-I and -II are not imported into Arabidopsis mitochondria. FEBS Lett 506: 291-295.
  • Masuda T, Suzuki T, Shimada H, Ohta H, Takamiya K (2003) Subcellular localization of two types of ferrochelatase in cucumber. Planta 217: 602-609.
  • Meima R, Eschevins C, Fillinger S, Bolhuis A, Hamoen LW, Dorenbos R, Quax WJ, van Dijl JM, Provvedi R, Chen I, Dubnau D, Bron S (2002) The bdbDC operon of Bacillus subtilis encodes thiol-disulfide oxidoreductases required for competence development. J Biol Chem 277: 6994-7001.
  • Menassa R, El-Rouby N, Brown GG (1997) An open reading frame for a protein involved in cytochrome c biogenesis is split into two parts in Brassica mitochondria. Curr Genet 31: 70-79.
  • Meyer EH, Giegé P, Gelhaye E, Rayapuram N, Ahuja U, Thöny-Meyer L, Grienenberger J-M, Bonnard G (2005) AtCCMH, an essential component of the c-type cytochrome maturation pathway in Arabidopsis mitochondria, interacts with apocytochrome c. Proc Natl Acad Sci 102: 16113-16118.
  • Motohashi K, Hisabori T (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem 281: 35039-35047.
  • Nakamoto SS, Hamel P, Merchant S (2000) Assembly of chloroplast cytochromes b and c. Biochimie 82: 603-614.
  • Nicholson DW, Stuart RA, Neupert W (1989) Biogenesis of cytochrome c1. Role of cytochrome c1 heme lyase and of the two proteolytic processing steps during import into mitochondria. J Biol Chem 264: 10156-10168.
  • Notsu Y, Masood S, Nishikawa T, Kubo N, Akiduki G, Nakazono M, Hirai A, Kadowaki K (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268: 434-445.
  • Oda K, Yamato K, Ohta E, Nakamura Y, Takemura M, Nozato N, Akashi K, Kanegae T, Ogura Y, Kohchi T, Ohyama K (1992) Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol 223: 1-7.
  • Ogihara Y, Yamazaki Y, Murai K, Kanno A, Terachi T, Shiina T, Miyashita N, Nasuda S, Nakamura C, Mori N, Takumi S, Murata M, Futo S, Tsunewaki K (2005) Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res 33: 6235-6250.
  • Ohta N, Sato N, Kuroiwa T (1998) Structure and organization of the mitochondrial genome of the unicellular red alga Cyanidioschyzon merolae deduced from the complete nucleotide sequence. Nucleic Acids Res 26: 5190-5198.
  • Page MLD, Hamel PP, Gabilly ST, Zegzouti H, Perea JV, Alonso JM, Ecker JR, Theg SM, Christensen SK, Merchant S (2004) A homolog of prokaryotic thiol disulfide transporter CcdA is required for the assembly of the cytochrome b6f complex in Arabidopsis chloroplasts. J Biol Chem 279: 32474-32482.
  • Quinn JM, Barraco P, Eriksson M, Merchant S (2000) Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. J Biol Chem 275: 6080-6089.
  • Raczynska KD, Le Ret M, Rurek M, Bonnard G, Augustyniak H, Gualberto JM (2006) Plant mitochondrial genes can be expressed from mRNAs lacking stop codons. FEBS Lett 580: 5641-5646.
  • Ramseier TM, Winteler HV, Hennecke H (1991) Discovery and sequence analysis of bacterial genes involved in the biogenesis of c-type cytochromes. J Biol Chem 266: 7793-7803.
  • Rayapuram N, Hagenmuller J, Grienenberger J-M, Giegé P, Bonnard G (2007) AtCCMA interacts with AtCCMB to form a novel mitochondrial ABC transporter involved in cytochrome c maturation in Arabidopsis. J Biol Chem 282: 21015-21023.
  • Reid E, Cole J, Eaves DJ (2001) The Escherichia coli CcmG protein fulfils a specific role in cytochrome c assembly. Biochem J 355: 51-58.
  • Ren Q, Thöny-Meyer L (2001) Physical interaction of CcmC with heme and the heme chaperone CcmE during cytochrome c maturation. J Biol Chem 276: 32591-32596.
  • Ren Q, Ahuja U, Thöny-Meyer L (2002) A bacterial cytochrome c heme lyase. CcmF forms a complex with the heme chaperone CcmE and CcmH but not with apocytochrome c. J Biol Chem 277: 7657-7663.
  • Richard-Fogal CL, Frawley ER, Feissner RE, Kranz RG (2007) Heme concentration dependence and metalloporphyrin inhibition of the system I and II cytochrome c assembly pathways. J Bacteriol 189: 455-463.
  • Richard-Fogal CL, Frawley ER, Kranz RG (2008) Topology and function of CcmD in cytochrome c maturation. J Bacteriol 190: 3489-3493.
  • Rothstein SJ, Gatenby AA, Willey DL, Gray JC (1985) Binding of pea cytochrome f to the inner membrane of Escherichia coli requires the bacterial secA gene product. Proc Natl Acad Sci USA 82: 7955-7959.
  • Sanders C, Deshmukh M, Astor D, Kranz RG, Daldal F (2005) Overproduction of CcmG and CcmFHRc fully supress the c-type cytochrome biogenesis defect of Rhodobacter capsulatus CcmI-null mutants. J Bacteriol 187: 4245-4256.
  • Sanders C, Boulay C, Daldal F (2007) Membrane-spanning and periplasmic segments of CcmI have distinct functions during cytochrome c biogenesis in Rhodobacter capsulatus. J Bacteriol 189: 789-800.
  • Santana MA, Tan FC, Smith AG (2002) Molecular characterization of coproporphyrinogen oxidase from Glycine max and Arabidopsis thaliana. Plant Physiol Biochem 40: 289-298.
  • Schulz H, Hennecke H, Thöny-Meyer L (1998) Prototype of a heme chaperone essential for cytochrome c maturation. Science 281: 1197-1200.
  • Schuster W (1994) The highly edited orf206 in Oenothera mitochondria may encode a component of a heme transporter involved in cytochrome c biogenesis. Plant Mol Biol 25: 33-42.
  • Schuster W, Combettes B, Flieger K, Brennicke A (1993) A plant mitochondrial gene encodes a protein involved in cytochrome c biogenesis. Mol Gen Genet 239: 49-57.
  • Spielewoy N, Schulz H, Grienenberger J-M, Thöny-Meyer L, Bonnard G (2001) CCME, a nuclear-encoded heme-binding protein involved in cytochrome c maturation in plant mitochondria. J Biol Chem 276: 5491-5497.
  • Steiner H, Kispal G, Zollner A, Haid A, Neupert W, Lill R (1996) Heme binding to a conserved Cys-Pro-Val motif is crucial for the catalytic function of mitochondrial heme lyases. J Biol Chem 271: 32605-32611.
  • Stevens JM, Daltrop O, Higham CW, Ferguson SJ (2003) Interaction of heme with variants of the heme chaperone CcmE carrying active site mutations and a cleavable N-terminal His tag. J Biol Chem 278: 20500-20506.
  • Stevens JM, Daltrop O, Allen JWA, Ferguson SJ (2004) c-type cytochrome formation: chemical and biological enigmas. Acc Chem Res 37: 999-1007.
  • Sugiyama Y, Watase Y, Nagase M, Makita N, Yagura S, Hirai A, Sugiura M (2005) The complete nucleotide sequence and multipatite organization of the tobacco mitochondrial genome: comparative analysis of mitocondrial genomes in higher plants. Mol genet Genomics 272: 603-615.
  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58: 321-346.
  • Thöny-Meyer L, Fischer F, Künzler P, Ritz D, Hennecke H (1995) Escherichia coli genes required for cytochrome c maturation. J Bacteriol 177: 4321-4326.
  • Turkarslan S, Sanders C, Daldal F (2006) Extracytoplasmic prosthetic group ligation to apoproteins: maturation of c-type cytochromes. Mol Microbiol 60: 537-541.
  • Walker JE, Saraste M, Runswick MJ, Gay NJ (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945-951.
  • Weigel M, Pesaresi P, Leister D (2003) Tracking the function of the cytochrome c6-like protein in higher plants. Trends Plant Sci 8: 513-517.
  • Uchida T, Stevens JM, Daltrop O, Harvat EM, Hong L, Ferguson SJ, Kitagawa T (2004) The interaction of covalently bound heme with the cytochrome c maturation protein CcmE. J Biol Chem 279: 51981-51988.
  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,926 nucleotides. Nat Genet 15: 57-61.
  • Xie Z, Merchant S (1996) The plastid-encoded ccsA gene is required for heme attachment to chloroplast c-type cytochrome cytochromes. J Biol Chem 271: 4632-4639. Xie Z, Culler D, Dreyfuss BW, Kuras R, Wollman F-A, Girard-Bascou J, Merchant S (1998) 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. Genetics 148: 681-692.
Document Type
Publication order reference
Identifiers
YADDA identifier
bwmeta1.element.bwnjournal-article-abpv55p417kz
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.