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Structure and function of the chloroplast signal recognition particle

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Abstract

The targeting of proteins, including the insertion and translocation of proteins in or across membranes, is a fundamental process within a cell, and a variety of specialized mechanisms for protein transport have been developed during evolution. The signal recognition particle (SRP) is found in the cytoplasm of most, if not all, eukaryotes and prokaryotes where it plays a central role in the co-translational insertion of membrane proteins into the endoplasmic reticulum and plasma membrane, respectively. SRP is a ribonucleoprotein consisting of an RNA and at least one polypeptide of ~54 kDa (SRP54). Interestingly, chloroplasts contain a specialized type of signal recognition particle. Chloroplast SRP (cpSRP) contains a SRP54 homologue but differs strikingly from cytosolic SRP in various aspects of structure and function. In contrast to cytosolic SRP, it contains a novel protein subunit (cpSRP43) and lacks RNA. CpSRP is also distinctive in its ability to interact with its substrate, light-harvesting chlorophyll a/b-binding protein, post-translationally. Furthermore, it is remarkable that the 54 kDa subunit of cpSRP is also involved in the co-translational transport of chloroplast-encoded thylakoid proteins, and is therefore able to switch between the co- and post-translational means of interaction with its respective substrate proteins.

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References

  • Abdallah F, Salamini F, Leister D (2000) A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci 5:141–142

    CAS  PubMed  Google Scholar 

  • Amin P, Sy DA, Pilgrim ML, Parry DH, Nussaume L, Hoffman NE (1999) Arabidopsis mutants lacking the 43- and 54-kilodalton subunits of the chloroplast signal recognition particle have distinct phenotypes. Plant Physiol 121:61–70

    Article  CAS  PubMed  Google Scholar 

  • Beck K, Eisner G, Trescher D, Dalbey RE, Brunner J, Muller M (2001) YidC, an assembly site for polytopic Escherichia coli membrane proteins located in immediate proximity to the SecYE translocon and lipids. EMBO Rep 2:709–714

    CAS  PubMed  Google Scholar 

  • Bernstein HD (2000) The biogenesis and assembly of bacterial membrane proteins. Curr Opin Microbiol 3:203–209

    Article  CAS  PubMed  Google Scholar 

  • Bork P (1993) Hundreds of ankyrin-like repeats in functionally diverse proteins: mobile modules that cross phyla horizontally? Proteins 17:363–374

    CAS  PubMed  Google Scholar 

  • Chen M, Samuelson JC, Jiang F, Muller M, Kuhn A, Dalbey RE (2002) Direct interaction of YidC with the Sec-independent Pf3 coat protein during its membrane protein insertion. J Biol Chem 277:7670–7675

    Article  CAS  PubMed  Google Scholar 

  • Cline K, Mori H (2001) Thylakoid Delta pH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J Cell Biol 154:719–729

    Google Scholar 

  • DeLille J, Peterson EC, Johnson T, Moore M, Kight A, Henry R (2000) A novel precursor recognition element facilitates posttranslational binding to the signal recognition particle in chloroplasts. Proc Natl Acad Sci USA 97:1926–1931

    Article  CAS  PubMed  Google Scholar 

  • Eichacker LA, Henry R (2001) Function of a chloroplast SRP in thylakoid protein export. Biochim Biophys Acta 1541:120–134

    Article  CAS  PubMed  Google Scholar 

  • Eissenberg JC, Elgin SC (2000) The HP1 protein family: getting a grip on chromatin. Curr Opin Genet Dev 10:204–210

    CAS  PubMed  Google Scholar 

  • Franklin AE, Hoffman NE (1993) Characterization of a chloroplast homologue of the 54-kDa subunit of the signal recognition particle. J Biol Chem 268:22175–22180

    CAS  PubMed  Google Scholar 

  • Fröderberg L, Houben E, Samuelson JC, Chen MY, Park SK, Phillips GJ, Dalbey R, Luirink J, de Gier JWL (2003) Versatility of inner membrane protein biogenesis in Escherichia coli. Mol Microbiol 47:1015–1027

    Article  PubMed  Google Scholar 

  • Gier JW de, Luirink J (2001) Biogenesis of inner membrane proteins in Escherichia coli. Mol Microbiol 40:314–322

    PubMed  Google Scholar 

  • Glick BS, Von Heijne G (1996) Saccharomyces cerevisiae mitochondria lack a bacterial-type Sec machinery. Protein Sci 5:2651–2652

    CAS  PubMed  Google Scholar 

  • Groves MR, Mant A, Kuhn A, Koch J, Dubel S, Robinson C, Sinning I (2001) Functional characterization of recombinant chloroplast signal recognition particle. J Biol Chem 276:27778–27786

    Article  CAS  PubMed  Google Scholar 

  • Hell K, Herrmann JM, Pratje E, Neupert W, Stuart RA (1998) Oxa1p, an essential component of the N-tail protein export machinery in mitochondria. Proc Natl Acad Sci USA 95:2250–2255

    CAS  PubMed  Google Scholar 

  • Hell K, Neupert W, Stuart RA (2001) Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J 20:1281–1288

    Article  CAS  PubMed  Google Scholar 

  • High S, Henry R, Mould RM, Valent Q, Meacock S, Cline K, Gray JC, Luirink J (1997) Chloroplast SRP54 interacts with a specific subset of thylakoid precursor proteins. J Biol Chem 272:11622–11628

    Article  CAS  PubMed  Google Scholar 

  • Hoffman NE, Franklin AE (1994) Evidence for a stromal GTP requirement for the integration of a chlorophyll a/b-binding polypeptide into thylakoid membranes. Plant Physiol 105:295–304

    Article  CAS  PubMed  Google Scholar 

  • Hoober JK, Eggink LL (1999) Assembly of light-harvesting complex II and biogenesis of thylakoid membranes in chloroplasts. Photosynth Res 61:197–215

    Article  CAS  Google Scholar 

  • Houben EN, Scotti PA, Valent QA, Brunner J, de Gier JL, Oudega B, Luirink J (2000) Nascent Lep inserts into the Escherichia coli inner membrane in the vicinity of YidC, SecY and SecA. FEBS Lett 476:229–233

    Article  CAS  PubMed  Google Scholar 

  • Hutin C, Havaux M, Carde JP, Kloppstech K, Meiherhoff K, Hoffman N, Nussaume L (2002) Double mutation cpSRP43--/cpSRP54-- is necessary to abolish the cpSRP pathway required for thylakoid targeting of the light-harvesting chlorophyll proteins. Plant J 29:531–543

    Article  CAS  PubMed  Google Scholar 

  • Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240

    Article  PubMed  Google Scholar 

  • Jiang F, Yi L, Moore M, Chen M, Rohl T, van Wijk KJ, de Gier JW, Henry R, Dalbey R (2002) Chloroplast YidC homologue Albino3 can functionally complement the bacterial YidC depletion strain and promote membrane insertion of both bacterial and chloroplast thylakoid proteins. J Biol Chem 277:19281–19288

    Article  CAS  PubMed  Google Scholar 

  • Johnson AE, van Waes MA (1999) The translocon: a dynamic gateway at the ER membrane. Annu Rev Cell Dev Biol 15:799–842

    Article  PubMed  Google Scholar 

  • Jonas-Straube E, Hutin C, Hoffman NE, Schünemann D (2001) Functional analysis of the protein-interacting domains of chloroplast SRP43. J Biol Chem 276:24654–24660

    Article  CAS  PubMed  Google Scholar 

  • Keenan RJ, Freymann DM, Stroud RM, Walter P (2001) The signal recognition particle. Ann Rev Biochem 70:755–775

    Article  CAS  PubMed  Google Scholar 

  • Kermorgant M, Bonnefoy N, Dujardin G (1997) Oxa1p, which is required for cytochrome c oxidase and ATP synthase complex formation, is embedded in the mitochondrial inner membrane. Curr Genet 31:302–307

    Article  CAS  PubMed  Google Scholar 

  • Kim SJ, Jansson S, Hoffman NE, Robinson C, Mant A (1999) Distinct “assisted” and “spontaneous” mechanisms for the insertion of polytopic chlorophyll-binding proteins into the thylakoid membrane. J Biol Chem 274:4715–4721

    Article  CAS  PubMed  Google Scholar 

  • Klimyuk VI, Persello-Cartieaux F, Havaux M, Contard-David P, Schuenemann D, Meiherhoff K, Gouet P, Jones JD, Hoffman NE, Nussaume L (1999) A chromodomain protein encoded by the arabidopsis CAO gene is a plant- specific component of the chloroplast signal recognition particle pathway that is involved in LHCP targeting. Plant Cell 11:87–99

    Article  CAS  PubMed  Google Scholar 

  • Klostermann E, Droste Gen Helling I, Carde JP, Schünemann D (2002) The thylakoid membrane protein ALB3 associates with the cpSecY-translocase in Arabidopsis thaliana. Biochem J 368:777–781

    Article  CAS  PubMed  Google Scholar 

  • Kogata N, Nishio K, Hirohashi T, Kikuchi S, Nakai M (1999) Involvement of a chloroplast homologue of the signal recognition particle receptor protein, FtsY, in protein targeting to thylakoids. FEBS Lett 447:329–333

    Article  CAS  PubMed  Google Scholar 

  • Koonin EV, Zhou S, Lucchesi JC (1995) The chromo superfamily: new members, duplication of the chromo domain and possible role in delivering transcription regulators to chromatin. Nucleic Acids Res 23:4229–33

    CAS  PubMed  Google Scholar 

  • Laan M van der, Houben EN, Nouwen N, Luirink J, Driessen AJ (2001) Reconstitution of Sec-dependent membrane protein insertion: nascent FtsQ interacts with YidC in a SecYEG-dependent manner. EMBO Rep 2:519–523

    PubMed  Google Scholar 

  • Leeuw E de, te Kaat K, Moser C, Menestrina G, Demel R, de Kruijff B, Oudega B, Luirink J, Sinning I (2000) Anionic phospholipids are involved in membrane association of FtsY and stimulate its GTPase activity. EMBO J 19:531–541

    Article  PubMed  Google Scholar 

  • Li X, Henry R, Yuan J, Cline K, Hoffman NE (1995) A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc Natl Acad Sci USA 92:3789–3793

    CAS  PubMed  Google Scholar 

  • Luirink J, ten Hagen-Jongman CM, van der Weijden CC, Oudega B, High S, Dobberstein B, Kusters R (1994) An alternative protein targeting pathway in Escherichia coli: studies on the role of FtsY. EMBO J 13:2289–2296

    CAS  PubMed  Google Scholar 

  • Martoglio B, Dobberstein B (1996) Snapshots of membrane-translocating proteins. Trends in Cell Biol 6:142–147

    Article  CAS  Google Scholar 

  • Moore M, Harrison MS, Peterson EC, Henry R (2000) Chloroplast Oxa1p homolog Albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275:1529–1532

    Article  CAS  PubMed  Google Scholar 

  • Mori H, Cline K (2001) Post-translational protein translocation into thylakoids by the Sec and DeltapH-dependent pathways. Biochim Biophys Acta 1541:80–90

    CAS  PubMed  Google Scholar 

  • Mori H, Summer EJ, Ma X, Cline K (1999) Component specificity for the thylakoidal Sec and Delta pH-dependent protein transport pathways. J Cell Biol 146:45–56

    CAS  PubMed  Google Scholar 

  • Mutka SC, Walter P (2001) Multifaceted physiological response allows yeast to adapt to the loss of the signal recognition particle-dependent protein-targeting pathway. Mol Biol Cell 12:577–588

    PubMed  Google Scholar 

  • Nilsson R, van Wijk KJ (2002) Transient interaction of cpSRP54 with elongating nascent chains of the chloroplast-encoded D1 protein: “cpSRP54 caught in the act.” FEBS Lett 524:127–133

    Google Scholar 

  • Nilsson R, Brunner J, Hoffman NE, van Wijk KJ (1999) Interactions of ribosome nascent chain complexes of the chloroplast- encoded D1 thylakoid membrane protein with cpSRP54. EMBO J 18:733–742

    Article  CAS  PubMed  Google Scholar 

  • Payan LA, Cline K (1991) A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane protein. J Cell Biol 112:603–613

    CAS  PubMed  Google Scholar 

  • Pilgrim ML, van Wijk KJ, Parry DH, Sy DA, Hoffman NE (1998) Expression of a dominant negative form of cpSRP54 inhibits chloroplast biogenesis in Arabidopsis. Plant J 13:177–186

    Article  CAS  PubMed  Google Scholar 

  • Rapoport TA, Jungnickel B, Kutay U (1996) Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu Rev Biochem 65:271–303

    CAS  PubMed  Google Scholar 

  • Robinson C, Thompson SJ, Woolhead C (2001) Multiple pathways used for the targeting of thylakoid proteins in chloroplasts. Traffic 2:245–251

    CAS  PubMed  Google Scholar 

  • Samuelson JC, Chen M, Jiang F, Moller I, Wiedmann M, Kuhn A, Phillips GJ, Dalbey RE (2000) YidC mediates membrane protein insertion in bacteria. Nature 406:637–641

    Article  CAS  PubMed  Google Scholar 

  • Samuelson JC, Jiang F, Yi L, Chen M, de Gier JW, Kuhn A, Dalbey RE (2001) Function of YidC for the insertion of M13 procoat protein in Escherichia coli: translocation of mutants that show differences in their membrane potential dependence and Sec requirement. J Biol Chem 276:34847–34852

    Article  CAS  PubMed  Google Scholar 

  • Schleiff E, Klösgen RB (2001) Without a little help from “my” friends: direct insertion of proteins into chloroplast membranes? Biochim Biophys Acta 1541:22–33

    Article  CAS  PubMed  Google Scholar 

  • Schünemann D, Gupta S, Persello-Cartieaux F, Klimyuk VI, Jones JDG, Nussaume L, Hoffman NE (1998) A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc Natl Acad Sci USA 95:10312–10316

    Article  PubMed  Google Scholar 

  • Schünemann D, Amin P, Hoffman NE (1999) Functional divergence of the plastid and cytosolic forms of the 54-kDa subunit of signal recognition particle. Biochem Biophys Res Commun 254:253–258

    Article  PubMed  Google Scholar 

  • Scotti PA, Urbanus ML, Brunner J, de Gier JW, von Heijne G, van der Does C, Driessen AJ, Oudega B, Luirink J (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J 19:542–549

    Article  CAS  PubMed  Google Scholar 

  • Sedgwick SG, Smerdon SJ (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24:311–316

    PubMed  Google Scholar 

  • Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, Coupland G (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9:717–730

    CAS  PubMed  Google Scholar 

  • Tu CJ, Schünemann D, Hoffman NE (1999) Chloroplast FtsY, chloroplast signal recognition particle, and GTP are required to reconstitute the soluble phase of light-harvesting chlorophyll protein transport into thylakoid membranes. J Biol Chem 274:27219–27224

    Article  CAS  PubMed  Google Scholar 

  • Tu CJ, Peterson EC, Henry R, Hoffman NE (2000) The L18 domain of light-harvesting chlorophyll proteins binds to chloroplast signal recognition particle 43. J Biol Chem 275:13187–13190

    Article  CAS  PubMed  Google Scholar 

  • Urbanus ML, Scotti PA, Froderberg L, Saaf A, de Gier JW, Brunner J, Samuelson JC, Dalbey RE, Oudega B, Luirink J (2001) Sec-dependent membrane protein insertion: sequential interaction of nascent FtsQ with SecY and YidC. EMBO Rep 2:524–529

    CAS  PubMed  Google Scholar 

  • Valent QA (2001) Signal recognition particle-mediated protein targeting in Escherichia coli. Antonie Van Leeuwenhoek 79:17–31

    Article  CAS  PubMed  Google Scholar 

  • Valent QA, Scotti PA, High S, de Gier JW, von Heijne G, Lentzen G, Wintermeyer W, Oudega B, Luirink J (1998) The Escherichia coli SRP and SecB targeting pathways converge at the translocon. EMBO J 17:2504–2512

    Article  CAS  PubMed  Google Scholar 

  • Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541:91–101

    Article  CAS  PubMed  Google Scholar 

  • Woolhead CA, Thompson SJ, Moore M, Tissier C, Mant A, Rodger A, Henry R, Robinson C (2001) Distinct Albino3-dependent and -independent pathways for thylakoid membrane protein insertion. J Biol Chem 276:40841–40846

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto HY, Bassi R (1996) Carotenoids: Localization and function. In: Ort DR, Yocum CF (eds) Oxygenic photosynthesis: the light reactions. Kluwer, The Netherlands, pp 539–563

  • Yuan J, Kight A, Goforth RL, Moore M, Peterson EC, Sakon J, Henry R (2002) ATP stimulates signal recognition particle (SRP)/FtsY-supported protein integration in chloroplasts. JBiol Chem 277:32400–32404

    Article  CAS  Google Scholar 

  • Zelazny A, Seluanov A, Cooper A, Bibi E (1997) The NG domain of the prokaryotic signal recognition particle receptor, FtsY, is fully functional when fused to an unrelated integral membrane polypeptide. Proc Natl Acad Sci USA 94:6025–6029

    Article  CAS  PubMed  Google Scholar 

  • Zhang LX, Paakkarinen V, Suorsa M, Aro EM (2001) A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis. J Biol Chem 276:37809–37814

    CAS  PubMed  Google Scholar 

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This work was supported by the Deutsche Forschungsgemeinschaft.

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Correspondence to Danja Schünemann.

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Communicated by S. Hohmann

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Schünemann, D. Structure and function of the chloroplast signal recognition particle. Curr Genet 44, 295–304 (2004). https://doi.org/10.1007/s00294-003-0450-z

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