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Translation initiation factor 3 families: what are their roles in regulating cyanobacterial and chloroplast gene expression?

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Abstract

Initiation is a key control point for the regulation of translation in prokaryotes and prokaryotic-like translation systems such as those in plant chloroplasts. Genome sequencing and biochemical studies are increasingly demonstrating differences in many aspects of translation between well-studied microbes such as Escherichia coli and lesser studied groups such as cyanobacteria. Analyses of chloroplast translation have revealed its prokaryotic origin but also uncovered many unique aspects that do not exist in E. coli. Recently, a novel form of posttranscriptional regulation by light color was discovered in the filamentous cyanobacterium Fremyella diplosiphon that requires a putative stem-loop and involves the use of two different prokaryotic translation initiation factor 3s (IF3s). Multiple (up to five) putative IF3s have now been found to be encoded in 22 % of sequenced cyanobacterial genomes and 26 % of plant nuclear genomes. The lack of similar light-color regulation of gene expression in most of these species suggests that IF3s play roles in regulating gene expression in response to other environmental and developmental cues. In the plant Arabidopsis, two nuclear-encoded IF3s have been shown to localize to the chloroplasts, and the mRNA levels encoding these vary significantly in certain organ and tissue types and during several phases of development. Collectively, the accumulated data suggest that in about one quarter of photosynthetic prokaryotes and eukaryotes, IF3 gene families are used to regulate gene expression in addition to their traditional roles in translation initiation. Models for how this might be accomplished in prokaryotes versus eukaryotic plastids are presented.

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References

  • Agrawal GK, Kato H, Asayama M, Shirai M (2001) An AU-box motif upstream of the SD sequence of light-dependent psbA transcripts confers mRNA instability in darkness in cyanobacteria. Nucleic Acids Res 29:1835–1843

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aizawa K, Fujita Y (1997) Regulation of synthesis of PSI in the cyanophytes Synechocystis PCC6714 and Plectonema boryanum during the acclimation of the photosystem stoichiometry to the light quality. Plant Cell Physiol 38:319–326

    Article  CAS  Google Scholar 

  • Babic S, Hunter CN, Rakhlin NJ, Simons RW, PhillipsJones MK (1997) Molecular characterization of the pifC gene encoding translation initiation factor 3, which is required for normal photosynthetic complex formation in Rhodobacter sphaeroides NCIB 8253. Eur J Biochem 249:564–575

    Article  CAS  PubMed  Google Scholar 

  • Barkan A (2011) Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol 155:1520–1532

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Beligni MV, Yamaguchi K, Mayfield SP (2004) The translational apparatus of Chlamydomonas reinhardtii chloroplast. Photosynth Res 82:315–325

    Article  CAS  PubMed  Google Scholar 

  • Bezy RP, Wiltbank L, Kehoe DM (2011) Light-dependent attenuation of phycoerythrin gene expression reveals convergent evolution of green light sensing in cyanobacteria. Proc Natl Acad Sci USA 108:18542–18547

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bovy A, de Vrieze G, Lugones L, van Horssen P, van den Berg C, Borrias M, Weisbeek P (1993) Iron-dependent stability of the ferredoxin I transcripts from the cyanobacterial strains Synechococcus species PCC 7942 and Anabaena species PCC 7937. Mol Microbiol 7:429–439

    Article  CAS  PubMed  Google Scholar 

  • Castenholz RW, Waterbury JB (1989) Oxygenic photosynthetic bacteria. Group I. Cyanobacteria. In: Bryant MP, Pfenning N, Holt JG (eds) JT Staley. Bergey’s manual of systematic bacteriology Williams and Wilkins, Baltimore, pp 1710–1789

    Google Scholar 

  • Cheng Y, Kaiser D (1989) dsg, a gene required for Myxococcus development, is necessary for cell viability. J Bacteriol 171:3727–3731

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng YL, Kalman LV, Kaiser D (1994) The dsg gene of Myxococcus xanthus encodes a protein similar to translation initiation factor IF3. J Bacteriol 176:1427–1433

    PubMed Central  CAS  PubMed  Google Scholar 

  • Davydov II, Wohlgemuth I, Artamonova II, Urlaub H, Tonevitsky AG, Rodnina MV (2013) Evolution of the protein stoichiometry in the L12 stalk of bacterial and organellar ribosomes. Nat Commun 4:1387

    Article  PubMed  Google Scholar 

  • de Smit MH (1998) Translational control by mRNA structure in eubacteria: Molecular biology and physical chemistry. In RNA Structure and Function, Cold Spring Harbor Press, Cold Spring Harbor, p 495–540

  • Deng XW, Gruissem W (1987) Control of plastid gene expression during development: the limited role of transcriptional regulation. Cell 49:379–387

    Article  CAS  PubMed  Google Scholar 

  • Duhring U, Axmann IM, Hess WR, Wilde A (2006) An internal antisense RNA regulates expression of the photosynthesis gene isiA. Proc Natl Acad Sci USA 103:7054–7058

    Article  PubMed Central  PubMed  Google Scholar 

  • Duval M, Korepanov A, Fuchsbauer O, Fechter P, Haller A, Fabbretti A, Choulier L, Micura R, Klaholz BP, Romby P et al (2013) Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation. Plos Biol 11:e1001731

    Article  PubMed Central  PubMed  Google Scholar 

  • Ehira S, Hamano T, Hayashida T, Kojima K, Nakamoto H, Hiyama T, Ohmori M, Shivaji S, Sato N (2003) Conserved temperature-dependent expression of RNA-binding proteins in cyanobacteria with different temperature optima. FEMS Microbiol Lett 225:137–142

    Article  CAS  PubMed  Google Scholar 

  • Ehira S, Ohmori M, Sato N (2005) Role of the 5′-UTR in accumulation of the rbpA1 transcript at low temperature in the cyanobacterium Anabaena variabilis M3. FEMS Microbiol Lett 251:91–98

    Article  CAS  PubMed  Google Scholar 

  • Elvekrog MM, Gonzalez RL (2013) Conformational selection of translation initiation factor 3 signals proper substrate selection. Nat Struct Mol Biol 20:628–635

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Filipovska A, Rackham O (2013) Specialization from synthesis: how ribosome diversity can customize protein function. FEBS Lett 587:1189–1197

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y (1997) A study on the dynamic features of photosystem stoichiometry: accomplishments and problems for future studies. Photosynth Res 53:83–93

    Article  CAS  Google Scholar 

  • Georg J, Hess WR (2011) Cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75:286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gilbert WV (2011) Functional specialization of ribosomes? Trends Biochem Sci 36:127–132

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Giuliodori AM, Branki A, Gualerzi CO, Pon CL (2004) Preferential translation of cold-shock mRNAs during cold adaptation. RNA 10:265–276

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Giuliodori AM, Brandi A, Giangrossi M, Gualerzi CO, Pon CL (2007) Cold-stress-induced de novo expression of infC and role of IF3 in cold-shock translational bias. RNA 13:1355–1365

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gollnick P, Babitzke P (2002) Transcription attenuation. Bba-Gene Struct Expr 1577:240–250

    Article  CAS  Google Scholar 

  • Goujon M, McWilliam H, Li WZ, Valentin F, Squizzato S, Paern J, Lopez R (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38 (Suppl):W695–W699

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gualerzi CO, Fabbretti A, Brandi L, Milon P, Pon CL (2010) Role of the initiation factors in mRNA start site selection and fMet-tRNA recruitment by bacterial ribosomes. Isr J Chem 50:80–94

    Article  CAS  Google Scholar 

  • Gutu A, Nesbit AD, Alverson AJ, Palmer JD, Kehoe DM (2013) Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression. Proc Natl Acad Sci USA 110:16253–16258

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hajnsdorf E, Boni IV (2012) Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie 94:1544–1553

    Article  CAS  PubMed  Google Scholar 

  • Hamano T, Murakami S, Takayama K, Ehira S, Maruyama K, Kawakami H, Morita EH, Hayashi H, Sato N (2004) Characterization of RNA-binding properties of three types of RNA-binding proteins in Anabaena sp PCC 7120. Cell Mol Biol 50:613–624

    CAS  PubMed  Google Scholar 

  • Henkin TM, Yanofsky C (2002) Regulation by transcription attenuation in bacteria: how RNA provides instructions for transcription termination/antitermination decisions. BioEssays 24:700–707

    Article  CAS  PubMed  Google Scholar 

  • Herranen M, Tyystjarvi T, Aro EM (2005) Regulation of photosystem I reaction center genes in Synechocystis sp strain PCC 6803 during light acclimation. Plant Cell Physiol 46:1484–1493

    Article  CAS  PubMed  Google Scholar 

  • Hirose T, Sugiura M (1996) Cis-Acting elements and trans-acting factors for accurate translation of chloroplast psbA mRNAs: development of an in vitro translation system from tobacco chloroplasts. EMBO J 15:1687–1695

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hirose T, Sugiura M (2004) Multiple elements required for translation of plastid atpB mRNA lacking the Shine-Dalgarno sequence. Nucleic Acids Res 32:3503–3510

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Horie Y, Ito Y, Ono M, Moriwaki N, Kato H, Hamakubo Y, Amano T, Wachi M, Shirai M, Asayama M (2007) Dark-induced mRNA instability involves RNase E/G-type endoribonuclease cleavage at the AU-box and SD sequences in cyanobacteria. Mol Genet Genomics 278:331–346

    Article  CAS  PubMed  Google Scholar 

  • Julian P, Milon P, Agirrezabala X, Lasso G, Gil D, Rodnina MV, Valle M (2011) The cryo-EM structure of a complete 30S translation initiation complex from Escherichia coli. PLoS Biol 9:e1001095

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kalman LV, Cheng YL, Kaiser D (1994) The Myxococcus xanthus Dsg gene product performs functions of Translation Initiation Factor If3 in vivo. J Bacteriol 176:1434–1442

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    Article  CAS  PubMed  Google Scholar 

  • Kehoe DM, Gutu A (2006) Responding to color: the regulation of complementary chromatic adaptation. Annu Rev Plant Biol 57:127–150

    Article  CAS  PubMed  Google Scholar 

  • Komili S, Farny NG, Roth FP, Silver PA (2007) Functional specificity among ribosomal proteins regulates gene expression. Cell 131:557–571

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kulkarni RD, Golden SS (1997) mRNA stability is regulated by a coding-region element and the unique 5′ untranslated leader sequences of the three Synechococcus psbA transcripts. Mol Microbiol 24:1131–1142

    Article  CAS  PubMed  Google Scholar 

  • Kulkarni RD, Schaefer MR, Golden SS (1992) Transcriptional and posttranscriptional components of psbA response to high light intensity in Synechococcus sp. Strain PCC 7942. J Bacteriol 174:3775–3781

    PubMed Central  CAS  PubMed  Google Scholar 

  • Laursen BS, Sorensen HP, Mortensen KK, Sperling-Petersen HU (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69:101–123

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li R, Golden SS (1993) Enhancer activity of light-responsive regulatory elements in the untranslated leader regions of cyanobacterial psbA genes. Proc Natl Acad Sci USA 90:11678–11682

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Malys N, McCarthy JEG (2011) Translation initiation: variations in the mechanism can be anticipated. Cell Mol Life Sci 68:991–1003

    Article  CAS  PubMed  Google Scholar 

  • Manuell AL, Quispe J, Mayfield SP (2007) Structure of the chloroplast ribosome: novel domains for translation regulation. PLoS Biol 5:1785–1797

    Article  CAS  Google Scholar 

  • Marin-Navarro J, Manuell AL, Wu J, Mayfield SP (2007) Chloroplast translation regulation. Photosynth Res 94:359–374

    Article  CAS  PubMed  Google Scholar 

  • Mayfield SP, Cohen A, Danon A, Yohn CB (1994) Translation of the psbA mRNA of Chlamydomonas reinhardtii requires a structured RNA element contained within the 5′ untranslated region. J Cell Biol 127:1537–1545

    Article  CAS  PubMed  Google Scholar 

  • Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. BBA-Bioenergetics 1817:247–257

    Article  CAS  PubMed  Google Scholar 

  • Mutsuda M, Sugiura M (2006) Translation initiation of cyanobacterial rbcS mRNAs requires the 38-kDa ribosomal protein S1 but not the Shine-Dalgarno sequence - Development of a cyanobacterial in vitro translation system. J Biol Chem 281:38314–38321

    Article  CAS  PubMed  Google Scholar 

  • Mutsuda M, Sugiura M, Sugita M (1999) Physiological characterization of RNA-binding protein-deficient cells from Synechococcus sp strain PCC7942. Plant Cell Physiol 40:1203–1209

    Article  CAS  Google Scholar 

  • Nakagawa S, Niimura Y, Miura K, Gojobori T (2010) Dynamic evolution of translation initiation mechanisms in prokaryotes. Proc Natl Acad Sci USA 107:6382–6387

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Omairi-Nasser A, de Gracia AG, Ajlani G (2011) A larger transcript is required for the synthesis of the smaller isoform of ferredoxin: NADP oxidoreductase. Mol Microbiol 81:1178–1189

    Article  CAS  PubMed  Google Scholar 

  • Peled-Zehavi H, Danon A (2007) Translation and translational regulation in chloroplasts, vol: Topics in Current Genetics. Springer, Berlin

  • Plader W, Sugiura M (2003) The Shine-Dalgarno-like sequence is a negative regulatory element for translation of tobacco chloroplast rps2 mRNA: an additional mechanism for translational control in chloroplasts. Plant J 34:377–382

    Article  CAS  PubMed  Google Scholar 

  • Rochaix J-D (1996) Post-transcriptional regulation of chloroplast gene expression in Chlamydomonas. Plant Mol Bio 32:327–341

    Article  CAS  Google Scholar 

  • Ruppel NJ, Logsdon CA, Whippo CW, Inoue K, Hangarter RP (2011) A mutation in Arabidopsis SEEDLING PLASTID DEVELOPMENT1 affects plastid differentiation in embryo-derived tissues during seedling growth. Plant Physiol 155:342–353

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sakamoto T, Bryant DA (1997) Temperature-regulated mRNA accumulation and stabilization for fatty acid desaturase genes in the cyanobacterium Synechococcus sp. strain PCC 7002. Mol Microbiol 23:1281–1292

    Article  CAS  PubMed  Google Scholar 

  • Salem K, van Waasbergen LG (2004) Light control of hliA transcription and transcript stability in the cyanobacterium Synechococcus elongatus Strain PCC 7942. J Bacteriol 186:1729–1736

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sato N, Nakamura A (1998) Involvement of the 5′-untranslated region in cold-regulated expression of the rbpA1 gene in the cyanobacterium Anabaena variabilis M3. Nucleic Acids Res 26:2192–2199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schippers JHM, Mueller-Roeber B (2010) Ribosomal composition and control of leaf development. Plant Sci 179:307–315

    Article  CAS  Google Scholar 

  • Schmeing TM, Ramakrishnan V (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature 461:1234–1242

    Article  CAS  PubMed  Google Scholar 

  • Shaner NC, Campbell RE, Steinbach PA, Giepmans BNG, Palmer AE, Tsien RY (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp red fluorescent protein. Nat Biotechnol 22:1567–1572

    Article  CAS  PubMed  Google Scholar 

  • Sharma MR, Wilson DN, Datta PP, Barat C, Schluenzen F, Fucini P, Agrawal RK (2007) Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc Natl Acad Sci USA 104:19315–19320

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shine J, Dalgarno L (1974) The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA 71:1342–1346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shine J, Dalgarno L (1975) Determinant of cistron specificity in bacterial ribosomes. Nature 254:34–38

    Article  CAS  PubMed  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li WZ, Lopez R, McWilliam H, Remmert M, Soding J et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    Article  PubMed Central  PubMed  Google Scholar 

  • Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590

    Article  CAS  PubMed  Google Scholar 

  • Springer M, Graffe M, Grunbergmanago M (1977) Characterization of an Escherichia coli mutant with a thermolabile Initiation Factor-If3 activity. Mol Gen Genet 151:17–26

    Article  CAS  PubMed  Google Scholar 

  • Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61:125–155

    Article  CAS  PubMed  Google Scholar 

  • Subramanian AR (1993) Molecular genetics of chloroplast ribosomal proteins. Trends Biochem Sci 18:177–181

    Article  CAS  PubMed  Google Scholar 

  • Sugiura M, Hirose T, Sugita M (1998) Evolution and mechanism of translation in chloroplasts. Annu Rev Genet 32:437–459

    Article  CAS  PubMed  Google Scholar 

  • Tandeau de Marsac N (1977) Occurrence and nature of chromatic adaptation in cyanobacteria. J Bacteriol 130:82–91

    PubMed Central  CAS  PubMed  Google Scholar 

  • Thomas JC, Ughy B, Lagoutte B, Ajlani G (2006) A second isoform of the ferredoxin : NADP oxidoreductase generated by an in-frame initiation of translation. Proc Natl Acad Sci USA 103:18368–18373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tiller N, Weingartner M, Thiele W, Maximova E, Schottler MA, Bock R (2012) The plastid-specific ribosomal proteins of Arabidopsis thaliana can be divided into non-essential proteins and genuine ribosomal proteins. Plant J 69:302–316

    Article  CAS  PubMed  Google Scholar 

  • Tyystjarvi T, Herranen M, Aro EM (2001) Regulation of translation elongation in cyanobacteria: membrane targeting of the ribosome nascent-chain complexes controls the synthesis of D1 protein. Mol Microbiol 40:476–484

    Article  CAS  PubMed  Google Scholar 

  • Tyystjarvi T, Sirpio S, Aro EM (2004) Post-transcriptional regulation of the psbA gene family in the cyanobacterium Synechococcus sp PCC 7942. FEBS Lett 576:211–215

    Article  CAS  PubMed  Google Scholar 

  • Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2:e718

    Article  PubMed Central  PubMed  Google Scholar 

  • Yamaguchi K, Subramanian AR (2003) Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit - PSRP-2 (U1A-type domains), PSRP-3 alpha/beta (ycf65 homologue) and PSRP-4 (Thx homologue). Eur J Biochem 270:190–205

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Prieto S, Beligni MV, Haynes PA, McDonald WH, Yates JR, Mayfield SP (2002) Proteomic characterization of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: identification of a novel S1 domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. Plant Cell 14:2957–2974

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamaguchi K, Beligni MV, Prieto S, Haynes PA, McDonald WH, Yates JR, Mayfield SP (2003) Proteomic characterization of the Chlamydomonas reinhardtii chloroplast ribosome—identification of proteins unique to the 70 S ribosome. J Biol Chem 278:33774–33785

    Article  CAS  PubMed  Google Scholar 

  • Zerges W, Rochaix JD (1994) The 5′ leader of a chloroplast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii. Mol Cel Biol 14:5268–5277

    CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Indiana University, Bloomington, IN, 47405, USA

    April D. Nesbit, Craig Whippo, Roger P. Hangarter & David M. Kehoe

  2. Department of Biology/Chemistry, Purdue University North Central, 1401 S. US 421, Westville, IN, 46391, USA

    April D. Nesbit

  3. Department of Natural Science, Dickinson State University, Dickinson, ND, 58601, USA

    Craig Whippo

  4. Indiana Molecular Biology Institute, Indiana University, Bloomington, IN, 47405, USA

    David M. Kehoe

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  1. April D. Nesbit
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Correspondence to David M. Kehoe.

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Nesbit, A.D., Whippo, C., Hangarter, R.P. et al. Translation initiation factor 3 families: what are their roles in regulating cyanobacterial and chloroplast gene expression?. Photosynth Res 126, 147–159 (2015). https://doi.org/10.1007/s11120-015-0074-4

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