CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii

Cline, Sara G.; Laughbaum, Isaac A.; Hamel, Patrice P.

doi:10.3389/fpls.2017.01306

Title: CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii

Journal Article · Thu Aug 03 00:00:00 EDT 2017 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2017.01306· OSTI ID:1463691

Cline, Sara G. ^[1]; Laughbaum, Isaac A. ^[2]; Hamel, Patrice P. ^[3]

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

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.

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Research Organization:: The Ohio State Univ., Columbus, OH (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0014562

OSTI ID:: 1463691

Journal Information:: Frontiers in Plant Science, Vol. 8; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 5 works

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References (72)

Maturation of Plastid c-type Cytochromes Gabilly, Stéphane T.; Hamel, Patrice P. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01313	journal	July 2017
Identification of an OPR protein involved in the translation initiation of the PsaB subunit of photosystem I Rahire, Michèle; Laroche, Fabrice; Cerutti, Lorenzo The Plant Journal, Vol. 72, Issue 4 https://doi.org/10.1111/j.1365-313X.2012.05111.x	journal	September 2012
Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii Auchincloss, Andrea H.; Zerges, William; Perron, Karl The Journal of Cell Biology, Vol. 157, Issue 6 https://doi.org/10.1083/jcb.200201060	journal	June 2002
ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites Emanuelsson, Olof; Nielsen, Henrik; Heijne, Gunnar Von Protein Science, Vol. 8, Issue 5 https://doi.org/10.1110/ps.8.5.978	journal	January 1999
Two Chlamydomonas OPR proteins stabilize chloroplast mRNAs encoding small subunits of photosystem II and cytochrome b ₆ f Wang, Fei; Johnson, Xenie; Cavaiuolo, Marina The Plant Journal, Vol. 82, Issue 5 https://doi.org/10.1111/tpj.12858	journal	May 2015
The biosynthesis of membrane and soluble plastidic c-type cytochromes of Chlamydomonas reinhardtii is dependent on multiple common gene products. Howe, G.; Merchant, S. The EMBO Journal, Vol. 11, Issue 8 https://doi.org/10.1002/j.1460-2075.1992.tb05346.x	journal	August 1992
High-Efficiency Transformation of Chlamydomonas reinhardtii by Electroporation Shimogawara, Kosuke; Fujiwara, Shoko; Grossman, Arthur Genetics, Vol. 148, Issue 4 https://doi.org/10.1093/genetics/148.4.1821	journal	April 1998
Cytochrome c maturation system on the negative side of bioenergetic membranes: CCB or System IV: Cytochrome c maturation System IV de Vitry, Catherine FEBS Journal, Vol. 278, Issue 22 https://doi.org/10.1111/j.1742-4658.2011.08373.x	journal	October 2011
Biogenesis of respiratory cytochromes in bacteria. Thöny-Meyer, L. Microbiology and molecular biology reviews : MMBR, Vol. 61, Issue 3 https://doi.org/10.1128/.61.3.337-376.1997	journal	January 1997
Structural and Functional Discussion of the Tetra-Trico-Peptide Repeat, a Protein Interaction Module Zeytuni, Natalie; Zarivach, Raz Structure, Vol. 20, Issue 3 https://doi.org/10.1016/j.str.2012.01.006	journal	March 2012
A Novel Component of the Disulfide-Reducing Pathway Required for Cytochrome c Assembly in Plastids Gabilly, Stéphane T.; Kropat, Janette; Karamoko, Mohamed Genetics, Vol. 187, Issue 3 https://doi.org/10.1534/genetics.110.125369	journal	January 2011
Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum Levitan, A.; Trebitsh, T.; Kiss, V. Proceedings of the National Academy of Sciences, Vol. 102, Issue 17 https://doi.org/10.1073/pnas.0500676102	journal	April 2005
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
Biochemical requirements for the maturation of mitochondrial c-type cytochromes Hamel, Patrice; Corvest, Vincent; Giegé, Philippe Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1793, Issue 1 https://doi.org/10.1016/j.bbamcr.2008.06.017	journal	January 2009
Cytochrome c biogenesis System I: An intricate process catalyzed by a maturase supercomplex? Verissimo, Andreia F.; Daldal, Fevzi Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 7 https://doi.org/10.1016/j.bbabio.2014.03.003	journal	July 2014
Cytochrome c biogenesis: the Ccm system Sanders, Carsten; Turkarslan, Serdar; Lee, Dong-Woo Trends in Microbiology, Vol. 18, Issue 6 https://doi.org/10.1016/j.tim.2010.03.006	journal	June 2010
Genes required for cytochrome c synthesis inBacillus subtilis: B. subtilis cytochrome c synthesis Le Brun, Nick E.; Bengtsson, Jenny; Hederstedt, Lars Molecular Microbiology, Vol. 36, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.01883.x	journal	May 2000
Cytochrome c assembly Mavridou, Despoina A. I.; Ferguson, Stuart J.; Stevens, Julie M. IUBMB Life, Vol. 65, Issue 3 https://doi.org/10.1002/iub.1123	journal	January 2013
New Insights into the Unique Structure of the F ₀ F ₁ -ATP Synthase from the Chlamydomonad Algae Polytomella sp. and Chlamydomonas reinhardtii van Lis, Robert; Mendoza-Hernández, Guillermo; Groth, Georg Plant Physiology, Vol. 144, Issue 2 https://doi.org/10.1104/pp.106.094060	journal	April 2007
I-TASSER server for protein 3D structure prediction Zhang, Yang BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-40	journal	January 2008
Evolution of an atypical de-epoxidase for photoprotection in the green lineage Li, Zhirong; Peers, Graham; Dent, Rachel M. Nature Plants, Vol. 2, Issue 10 https://doi.org/10.1038/nplants.2016.140	journal	September 2016
Structural basis for specific single-stranded RNA recognition by designer pentatricopeptide repeat proteins Shen, Cuicui; Zhang, Delin; Guan, Zeyuan Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11285	journal	April 2016
Cytochrome c Biogenesis: Mechanisms for Covalent Modifications and Trafficking of Heme and for Heme-Iron Redox Control Kranz, R. G.; Richard-Fogal, C.; Taylor, J. -S. Microbiology and Molecular Biology Reviews, Vol. 73, Issue 3 https://doi.org/10.1128/mmbr.00001-09	journal	August 2009
Pentatricopeptide Repeat Proteins in Plants Barkan, Alice; Small, Ian Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040159	journal	April 2014
Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast Raynaud, C.; Loiselay, C.; Wostrikoff, K. Proceedings of the National Academy of Sciences, Vol. 104, Issue 21 https://doi.org/10.1073/pnas.0703162104	journal	May 2007
Identification of a Chlamydomonas plastidial 2-lysophosphatidic acid acyltransferase and its use to engineer microalgae with increased oil content Yamaoka, Yasuyo; Achard, Dorine; Jang, Sunghoon Plant Biotechnology Journal, Vol. 14, Issue 11 https://doi.org/10.1111/pbi.12572	journal	May 2016
The Octatricopeptide Repeat Protein Raa8 Is Required for Chloroplast trans Splicing Marx, Christina; Wünsch, Christiane; Kück, Ulrich Eukaryotic Cell, Vol. 14, Issue 10 https://doi.org/10.1128/ec.00096-15	journal	July 2015
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 Pollock, Steve V.; Prout, Davey L.; Godfrey, Ashley C. Plant Molecular Biology, Vol. 56, Issue 1 https://doi.org/10.1007/s11103-004-2650-4	journal	September 2004
Structure of human mitochondrial RNA polymerase Ringel, Rieke; Sologub, Marina; Morozov, Yaroslav I. Nature, Vol. 478, Issue 7368 https://doi.org/10.1038/nature10435	journal	September 2011
Subunit–subunit interactions and overall topology of the dimeric mitochondrial ATP synthase of Polytomella sp. Cano-Estrada, Araceli; Vázquez-Acevedo, Miriam; Villavicencio-Queijeiro, Alexa Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 8 https://doi.org/10.1016/j.bbabio.2010.02.024	journal	August 2010
Incorporation of glutamine repeats makes protein oligomerize: implications for neurodegenerative diseases. Stott, K.; Blackburn, J. M.; Butler, P. J. Proceedings of the National Academy of Sciences, Vol. 92, Issue 14 https://doi.org/10.1073/pnas.92.14.6509	journal	July 1995
A Homolog of Prokaryotic Thiol Disulfide Transporter CcdA Is Required for the Assembly of the Cytochrome b ₆ f Complex in Arabidopsis Chloroplasts Page, M. L. Dudley; Hamel, Patrice P.; Gabilly, Stéphane T. Journal of Biological Chemistry, Vol. 279, Issue 31 https://doi.org/10.1074/jbc.M404285200	journal	May 2004
The FLP proteins act as regulators of chlorophyll synthesis in response to light and plastid signals in Chlamydomonas Falciatore, A. Genes & Development, Vol. 19, Issue 1 https://doi.org/10.1101/gad.321305	journal	January 2005
The flanking regions of PsaD drive efficient gene expression in the nucleus of the green alga Chlamydomonas reinhardtii Fischer, N.; Rochaix, J. -D. Molecular Genetics and Genomics, Vol. 265, Issue 5 https://doi.org/10.1007/s004380100485	journal	April 2001
Analysis of Sp1 in vivo reveals mutiple transcriptional domains, including a novel glutamine-rich activation motif Courey, Albert J.; Tjian, Robert Cell, Vol. 55, Issue 5 https://doi.org/10.1016/0092-8674(88)90144-4	journal	December 1988
TPR proteins: the versatile helix D'Andrea, L. Trends in Biochemical Sciences, Vol. 28, Issue 12 https://doi.org/10.1016/j.tibs.2003.10.007	journal	December 2003
Complementation of a Chlamydomonas reinhardtii mutant using a genomic cosmid library Purton, Saul; Rochaix, Jean-David Plant Molecular Biology, Vol. 24, Issue 3 https://doi.org/10.1007/bf00024121	journal	February 1994
Identification and Expression Analysis of cDNA Encoding a Chloroplast Recombination Protein REC1, the Chloroplast RecA Homologue in Chlamydomonas reinhardtii Nakazato, Emi; Fukuzawa, Hideya; Tabata, Satoshi Bioscience, Biotechnology, and Biochemistry, Vol. 67, Issue 12 https://doi.org/10.1271/bbb.67.2608	journal	January 2003
The chemistry and biochemistry of heme c: functional bases for covalent attachment Bowman, Sarah E. J.; Bren, Kara L. Natural Product Reports, Vol. 25, Issue 6 https://doi.org/10.1039/b717196j	journal	January 2008
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 Eberhard, Stephan; Loiselay, Christelle; Drapier, Dominique The Plant Journal, Vol. 67, Issue 6 https://doi.org/10.1111/j.1365-313X.2011.04657.x	journal	July 2011
Maturation of thylakoid lumen proteins proceeds post-translationally through an intermediate in vivo. Howe, G.; Merchant, S. Proceedings of the National Academy of Sciences, Vol. 90, Issue 5 https://doi.org/10.1073/pnas.90.5.1862	journal	March 1993
Spontaneous Dominant Mutations in Chlamydomonas Highlight Ongoing Evolution by Gene Diversification Boulouis, Alix; Drapier, Dominique; Razafimanantsoa, Hélène The Plant Cell, Vol. 27, Issue 4 https://doi.org/10.1105/tpc.15.00010	journal	March 2015
The Nucleus-Encoded trans -Acting Factor MCA1 Plays a Critical Role in the Regulation of Cytochrome f Synthesis in Chlamydomonas Chloroplasts Boulouis, Alix; Raynaud, Cécile; Bujaldon, Sandrine The Plant Cell, Vol. 23, Issue 1 https://doi.org/10.1105/tpc.110.078170	journal	January 2011
WoLF PSORT: protein localization predictor Horton, P.; Park, K. -J.; Obayashi, T. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm259	journal	May 2007
The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions Das, A. K. The EMBO Journal, Vol. 17, Issue 5 https://doi.org/10.1093/emboj/17.5.1192	journal	March 1998
A novel multifunctional factor involved in trans-splicing of chloroplast introns in Chlamydomonas Merendino, L. Nucleic Acids Research, Vol. 34, Issue 1 https://doi.org/10.1093/nar/gkj429	journal	January 2006
Two adjacent nuclear genes are required for functional complementation of a chloroplast trans-splicing mutant from Chlamydomonas reinhardtii: C. reinhardtii chloroplast trans-splicing Balczun, Carsten; Bunse, Astrid; Hahn, Daniela The Plant Journal, Vol. 43, Issue 5 https://doi.org/10.1111/j.1365-313X.2005.02478.x	journal	July 2005
An overview of pentatricopeptide repeat proteins and their applications Manna, Sam figshare https://doi.org/10.6084/m9.figshare.1401873	text	January 2015
Functional Analysis of a Divergent System II Protein, Ccs1, Involved in c -Type Cytochrome Biogenesis Dreyfuss, Beth Welty; Hamel, Patrice P.; Nakamoto, Stacie S. Journal of Biological Chemistry, Vol. 278, Issue 4 https://doi.org/10.1074/jbc.m208652200	journal	November 2002
Continuous evolution of base editors with expanded target compatibility and improved activity Thuronyi, Benjamin W.; Koblan, Luke W.; Levy, Jonathan M. Nature Biotechnology, Vol. 37, Issue 9 https://doi.org/10.1038/s41587-019-0193-0	journal	July 2019
Cytochrome c biogenesis in mitochondria - Systems III and V: Cytochrome c biogenesis in mitochondria Allen, James W. A. FEBS Journal, Vol. 278, Issue 22 https://doi.org/10.1111/j.1742-4658.2011.08231.x	journal	August 2011
Variant c-type cytochromes as probes of the substrate specificity of the E. coli cytochrome c maturation (Ccm) apparatus Allen, James W. A.; Sawyer, Elizabeth B.; Ginger, Michael L. Biochemical Journal, Vol. 419, Issue 1 https://doi.org/10.1042/bj20081999	journal	March 2009
Mutations in Cytochrome Assembly and Periplasmic Redox Pathways in Bordetella pertussis Feissner, R. E.; Beckett, C. S.; Loughman, J. A. Journal of Bacteriology, Vol. 187, Issue 12 https://doi.org/10.1128/jb.187.12.3941-3949.2005	journal	June 2005
GATEWAY™ vectors for Agrobacterium-mediated plant transformation Karimi, Mansour; Inzé, Dirk; Depicker, Ann Trends in Plant Science, Vol. 7, Issue 5, p. 193-195 https://doi.org/10.1016/S1360-1385(02)02251-3	journal	May 2002
An overview of pentatricopeptide repeat proteins and their applications Manna, Sam Biochimie, Vol. 113 https://doi.org/10.1016/j.biochi.2015.04.004	journal	June 2015
CcsBA is a cytochrome c synthetase that also functions in heme transport Frawley, E. R.; Kranz, R. G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 25 https://doi.org/10.1073/pnas.0903132106	journal	June 2009
Redox Processes Controlling the Biogenesis of c -Type Cytochromes Bonnard, Géraldine; Corvest, Vincent; Meyer, Etienne H. Antioxidants & Redox Signaling, Vol. 13, Issue 9 https://doi.org/10.1089/ars.2010.3161	journal	November 2010
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation Nakagawa, Tsuyoshi; Kurose, Takayuki; Hino, Takeshi Journal of Bioscience and Bioengineering, Vol. 104, Issue 1 https://doi.org/10.1263/jbb.104.34	journal	July 2007
The Plastid-encoded ccsA Gene Is Required for Heme Attachment to Chloroplast c-type Cytochromes Merchant, S. Journal of Biological Chemistry, Vol. 271, Issue 9 https://doi.org/10.1074/jbc.271.9.4632	journal	March 1996
WebLogo: A Sequence Logo Generator Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc Genome Research, Vol. 14, Issue 6, p. 1188-1190 https://doi.org/10.1101/gr.849004	journal	May 2004
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 Xie, Zhiyi; Culler, Duane; Dreyfuss, Beth Welty Genetics, Vol. 148, Issue 2 https://doi.org/10.1093/genetics/148.2.681	journal	February 1998
Gene isolation through genomic complementation using an indexed library of Chlamydomonas reinhardtii DNA Zhang, Hongtao; Herman, Patricia L.; Weeks, Donald P. Plant Molecular Biology, Vol. 24, Issue 4 https://doi.org/10.1007/BF00023562	journal	February 1994
A Gamete-specific, Sex-limited Homeodomain Protein in Chlamydomonas Kurvari, Venkatesh; Grishin, Nick V.; Snell, William J. The Journal of Cell Biology, Vol. 143, Issue 7 https://doi.org/10.1083/jcb.143.7.1971	journal	December 1998
Ccs1 , a Nuclear Gene Required for the Post-translational Assembly of Chloroplast c -Type Cytochromes Inoue, Kaori; Dreyfuss, Beth Welty; Kindle, Karen L. Journal of Biological Chemistry, Vol. 272, Issue 50 https://doi.org/10.1074/jbc.272.50.31747	journal	December 1997
Increased Efficiency of Cloning Large DNA Fragments Using a Lower Copy Number Plasmid Feng, T.; Li, Z.; Jiang, W. BioTechniques, Vol. 32, Issue 5 https://doi.org/10.2144/02325bm03	journal	May 2002
Operation of trans-thylakoid thiol-metabolizing pathways in photosynthesis Karamoko, Mohamed; Gabilly, Stéphane T.; Hamel, Patrice P. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00476	journal	January 2013
RAP, the Sole Octotricopeptide Repeat Protein in Arabidopsis , Is Required for Chloroplast 16S rRNA Maturation Kleinknecht, Laura; Wang, Fei; Stübe, Roland The Plant Cell, Vol. 26, Issue 2 https://doi.org/10.1105/tpc.114.122853	journal	February 2014
Composition and function of cytochrome c biogenesis System II: Cytochrome c biogenesis System II Simon, Jörg; Hederstedt, Lars FEBS Journal, Vol. 278, Issue 22 https://doi.org/10.1111/j.1742-4658.2011.08374.x	journal	October 2011
CCS5, a Thioredoxin-like Protein Involved in the Assembly of Plastid c -Type Cytochromes Gabilly, Stéphane T.; Dreyfuss, Beth Welty; Karamoko, Mohamed Journal of Biological Chemistry, Vol. 285, Issue 39 https://doi.org/10.1074/jbc.m109.099069	journal	July 2010
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 Beckett, Caroline S.; Loughman, Jennifer A.; Karberg, Katherine A. Molecular Microbiology, Vol. 38, Issue 3 https://doi.org/10.1046/j.1365-2958.2000.02174.x	journal	November 2000
Mechanistic Insight into Pentatricopeptide Repeat Proteins as Sequence-Specific RNA-Binding Proteins for Organellar RNAs in Plants Nakamura, T.; Yagi, Y.; Kobayashi, K. Plant and Cell Physiology, Vol. 53, Issue 7 https://doi.org/10.1093/pcp/pcs069	journal	May 2012
Role of heme in the biosynthesis of cytochrome c6. Howe, G.; Merchant, S. Journal of Biological Chemistry, Vol. 269, Issue 8 https://doi.org/10.1016/S0021-9258(17)37536-1	journal	February 1994

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plastid
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cytochrome c
heme
assembly factor
OPR

Title: CCS2, an Octatricopeptide-Repeat Protein, Is Required for Plastid Cytochrome c Assembly in the Green Alga Chlamydomonas reinhardtii

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