Skip to main content
SpringerLink
Log in

Protein Import into Complex Plastids: Current Findings and Perspectives

  • Chapter
  • First Online:
Endosymbiosis

Abstract

Transport of proteins across either two, three, four, or even five membranes is a feature of plastids, which evolved via the engulfment of a phototrophic eukaryote by another eukaryotic cell (secondary/tertiary endosymbiosis). Although emerging data are helpful for a mechanistic explanation of protein transport across the membranes surrounding secondary plastids, several questions still have to be answered. Here, we describe the recent models concerning protein import into secondary plastids and discuss their implications.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agrawal S, van Dooren GG, Beatty WL, Striepen B (2009) Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins. J Biol Chem 284:33683–33691

    Article  PubMed  CAS  Google Scholar 

  • Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:81–88

    Article  Google Scholar 

  • Bionda T, Tillmann B, Simm S, Beilstein K, Ruprecht M, Schleiff E (2010) Chloroplast import signals: the length requirement for translocation in vitro and in vivo. J Mol Biol 402:510–523

    Article  PubMed  CAS  Google Scholar 

  • Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, Maier UG (2009) Protein targeting into secondary plastids. J Eukaryot Microbiol 56:9–15

    Article  PubMed  CAS  Google Scholar 

  • Bolte K, Gruenheit N, Felsner G, Sommer MS, Maier UG, Hempel F (2011) Making new out of old: recycling and modification of an ancient protein translocation system during eukaryotic evolution. Bioessays 33(5):368–376

    Article  PubMed  CAS  Google Scholar 

  • Bonifacino JS (2004) The GGA proteins: adaptors on the move. Nat Rev Mol Cell Biol 5:23–32

    Article  PubMed  CAS  Google Scholar 

  • Bullmann L, Haarmann R, Mirus O, Bredemeier R, Hempel F, Maier UG, Schleiff E (2010) Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J Biol Chem 285:6848–6856

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T (2003) Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci 358:109–133

    Article  PubMed  CAS  Google Scholar 

  • Chaal BK, Green BR (2005) Protein import pathways in ‘complex’ chloroplasts derived from secondary endosymbiosis involving a red algal ancestor. Plant Mol Biol 57:333–342

    Article  PubMed  CAS  Google Scholar 

  • Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama S, Arias MC, Ball SG, Gile GH, Hirakawa Y, Hopkins JF, Kuo A, Rensing SA, Schmutz J, Symeonidi A, Elias M, Eveleigh RJM, Herman EK, Klute MJ, Nakayama T, Obornik M, Reyes-Prieto A, Armbrust EV, Aves SJ, Beiko RG, Coutinho P, Dacks JB, Durnford DG, Fast NM, Green BR, Grisdale CJ, Hempel F, Henrissat B, Hoppner MP, Ishida K-I, Kim E, Koreny L, Kroth PG, Liu Y, Malik S-B, Maier UG, McRose D, Mock T, Neilson JAD, Onodera NT, Poole AM, Pritham EJ, Richards TA, Rocap G, Roy SW, Sarai C, Schaack S, Shirato S, Slamovits CH, Spencer DF, Suzuki S, Worden AZ, Zauner S, Barry K, Bell C, Bharti AK, Crow JA, Grimwood J, Kramer R, Lindquist E, Lucas S, Salamov A, McFadden GI, Lane CE, Keeling PJ, Gray MW, Grigoriev IV, Archibald JM (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65

    Article  PubMed  CAS  Google Scholar 

  • DeRocher A, Hagen CB, Froehlich JE, Feagin JE, Parsons M (2000) Analysis of targeting sequences demonstrates that trafficking to the Toxoplasma gondii plastid branches off the secretory system. J Cell Sci 113:3969–3977

    PubMed  CAS  Google Scholar 

  • DeRocher A, Gilbert B, Feagin JE, Parsons M (2005) Dissection of brefeldin A-sensitive and -insensitive steps in apicoplast protein targeting. J Cell Sci 118:565–574

    Article  PubMed  CAS  Google Scholar 

  • DeRocher AE, Coppens I, Karnataki A, Gilbert LA, Rome ME, Feagin JE, Bradley PJ, Parsons M (2008) Thioredoxin family protein of the apicoplast periphery identifies abundant candidate transport vesicles in Toxoplasma gondii. Eukaryot Cell 7:1518–1529

    Article  PubMed  CAS  Google Scholar 

  • Douglas S, Zauner S, Fraunholz M, Beaton M, Penny S, Deng LT, Wu X, Reith M, Cavalier-Smith T, Maier UG (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410:1091–1096

    Article  PubMed  CAS  Google Scholar 

  • Durnford DG, Gray MW (2006) Analysis of Euglena gracilis plastid- targeted proteins reveals different classes of transit sequences. Eukaryot Cell 5:2079–2091

    Article  PubMed  CAS  Google Scholar 

  • Felsner G, Sommer MS, Maier UG (2010) The physical and functional borders of transit peptide-like sequences in secondary endosymbionts. BMC Plant Biol 10:223

    Article  PubMed  Google Scholar 

  • Felsner G, Sommer MS, Gruenheit N, Hempel F, Moog D, Zauner S, Martin W, Maier UG (2011) ERAD components in organisms with complex red plastids suggest recruitment of a preexisting protein transport pathway for the periplastid membrane. Genome Biol Evol 3:140–150

    Article  PubMed  CAS  Google Scholar 

  • Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299:705–708

    Article  PubMed  CAS  Google Scholar 

  • Gibbs SP (1979) The route of entry of cytoplasmically synthesized proteins into chloroplasts of algae possessing chloroplast ER. J Cell Sci 35:253–266

    PubMed  CAS  Google Scholar 

  • Gilson PR, Su V, Slamovits CH, Reith ME, Keeling PJ, McFadden GI (2006) Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature’s smallest nucleus. Proc Natl Acad Sci U S A 103:9566–9571

    Article  PubMed  CAS  Google Scholar 

  • Gould SB, Sommer MS, Hadfi K, Zauner S, Maier UG (2006a) Protein targeting into the complex plastid of cryptophytes. J Mol Evol 62:674–681

    Article  PubMed  CAS  Google Scholar 

  • Gould SB, Sommer MS, Kroth PG, Gile GH, Keeling PJ, Maier UG (2006b) Nucleus-to-nucleus gene transfer and protein retargeting into a remnant cytoplasm of cryptophytes and diatoms. Mol Biol Evol 23:2413–2422

    Article  PubMed  CAS  Google Scholar 

  • Gould SB, Fan E, Hempel F, Maier UG, Klösgen RB (2007) Translocation of a phycoerythrin alpha subunit across five biological membranes. J Biol Chem 282:30295–30302

    Article  PubMed  CAS  Google Scholar 

  • Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517

    Article  PubMed  CAS  Google Scholar 

  • Gruber A, Vugrinec S, Hempel F, Gould SB, Maier UG, Kroth PG (2007) Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol Biol 64:519–530

    Article  PubMed  CAS  Google Scholar 

  • Hempel F, Bozarth A, Sommer MS, Zauner S, Przyborski JM, Maier UG (2007) Transport of nuclear-encoded proteins into secondarily evolved plastids. Biol Chem 388:899–906

    Article  PubMed  CAS  Google Scholar 

  • Hempel F, Bullmann L, Lau J, Zauner S, Maier UG (2009) ERAD derived preprotein transport across the second outermost plastid membrane of diatoms. Mol Biol Evol 26:1781–1790

    Article  PubMed  CAS  Google Scholar 

  • Hempel F, Felsner G, Maier UG (2010) New mechanistic insights into pre-protein transport across the second outermost plastid membrane of diatoms. Mol Microbiol 76:793–801

    Article  PubMed  CAS  Google Scholar 

  • Hirakawa Y, Ishida K (2010) Internal plastid-targeting signal found in a RuBisCO small subunit protein of a chlorarachniophyte alga. Plant J 64:402–410

    Article  PubMed  CAS  Google Scholar 

  • Hirakawa Y, Nagamune K, Ishida K (2009) Protein targeting into secondary plastids of chlorarachniophytes. Proc Natl Acad Sci U S A 106:12820–12825

    Article  PubMed  CAS  Google Scholar 

  • Hirakawa Y, Gile GH, Ota S, Keeling PJ, Ishida K (2010) Characterization of periplastidal compartment-targeting signals in chlorarachniophytes. Mol Biol Evol 27:1538–1545

    Article  PubMed  CAS  Google Scholar 

  • Hirakawa Y, Burki F, Keeling PJ (2012) Genome-based reconstruction of the protein import maschinery in the secondary plastid of a chlorarachniophyte alga. Eukaryot Cell 11:324–333

    Article  PubMed  CAS  Google Scholar 

  • Inaba T, Schnell DJ (2008) Protein trafficking to plastids: one theme, many variations. Biochem J 413:15–28

    Article  PubMed  CAS  Google Scholar 

  • Janouškovec J, Hórak A, Oborník M, Lukeš J, Keeling PJ (2011) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107:10949–10954

    Article  Google Scholar 

  • Kalanon M, Tonkin CJ, McFadden GI (2009) Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot Cell 8:1146–1154

    Article  PubMed  CAS  Google Scholar 

  • Karnataki A, Derocher A, Coppens I, Nash C, Feagin JE, Parsons M (2007) Cell cycle-regulated vesicular trafficking of Toxoplasma APT1, a protein localized to multiple apicoplast membranes. Mol Microbiol 63:1653–1668

    Article  PubMed  CAS  Google Scholar 

  • Keeling PJ (2009) Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 56:1–8

    Article  PubMed  CAS  Google Scholar 

  • Kessler F, Schnell D (2009) Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr Opin Cell Biol 21:494–500

    Article  PubMed  CAS  Google Scholar 

  • Kilian O, Kroth PG (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41:175–183

    Article  PubMed  CAS  Google Scholar 

  • Kitajima A, Asatsuma S, Okada H, Hamada Y, Kaneko K, Nanjo Y, Kawagoe Y, Toyooka K, Matsuoka K, Takeuchi M, Nakano A, Mitsui T (2009) The rice alpha-amylase glycoprotein is targeted from the Golgi apparatus through the secretory pathway to the plastids. Plant Cell 21:2844–2858

    Article  PubMed  CAS  Google Scholar 

  • Lane CE, van den Heuvel K, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM (2007) Nucleomorph genome of Hemiselmis andersenii reveals complete intron loss and compaction as a driver of protein structure and function. Proc Natl Acad Sci U S A 104:19908–19913

    Article  PubMed  CAS  Google Scholar 

  • Lang M, Kroth PG (2001) Diatom fucoxanthin chlorophyll a/c-binding protein (FCP) and land plant light-harvesting proteins use a similar pathway for thylakoid membrane insertion. J Biol Chem 276:7985–7991

    Article  PubMed  CAS  Google Scholar 

  • Lim L, McFadden GI (2010) The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond B Biol Sci 365:749–763

    Article  PubMed  CAS  Google Scholar 

  • Lim L, Kalanon M, McFadden GI (2009) New proteins in the apicoplast membranes: time to rethink apicoplast protein targeting. Trends Parasitol 25:197–200

    Article  PubMed  CAS  Google Scholar 

  • Lukeš J, Leander BS, Keeling PJ (2009) Cascades of convergent evolution: the corresponding evolutionary histories of euglenozoans and dinoflagellates. Proc Natl Acad Sci USA 106:9963–9970

    Article  PubMed  Google Scholar 

  • Maier UG, Douglas SE, Cavalier-Smith T (2000) The nucleomorph genomes of cryptophytes and chlorarachniophytes. Protist 151:103–109

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 99:12246–12251

    Article  PubMed  CAS  Google Scholar 

  • Moog M, Stork S, Zauner S, Maier UG (2011) In silico and in vivo investigations of the proteins of a minimized eukaryotic cytoplasm. Genome Biol Evol 3:375–382

    Article  PubMed  CAS  Google Scholar 

  • Moore CE, Curtis B, Mills T, Tanifuji G, Archibald JM (2012) Nucleomorph genome sequence of the cryptophyte alga Chroomonas mesostigmatica CCMP1168 reveals lineage-specific gene loss and genome complexity. Genome Biol Evol 4:1162–1175

    Article  PubMed  Google Scholar 

  • Nassoury N, Cappadocia M, Morse D (2003) Plastid ultrastructure defines the protein import pathway in dinoflagellates. J Cell Sci 116:2867–2874

    Article  PubMed  CAS  Google Scholar 

  • Nanjo Y, Oka H, Ikarashi N, Kaneko K, Kitajima A, Mitsui T, Muñoz FJ, Rodríguez-López M, Baroja-Fernández E, Pozueta-Romero J (2006) Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 18:2582–2592

    Article  PubMed  CAS  Google Scholar 

  • Osafune T, Schiff JA, Hase E (1991) Stage-dependent localization of LHCP II apoprotein in the Golgi of synchronized cells of Euglena gracilis by immunogold electron microscopy. Exp Cell Res 193:320–330

    Article  PubMed  CAS  Google Scholar 

  • Patron NJ, Waller RF (2007) Transit peptide diversity and divergence: a global analysis of plastid targeting signals. Bioessays 29:1048–1058

    Article  PubMed  CAS  Google Scholar 

  • Patron NJ, Waller RF, Archibald JM, Keeling PJ (2005) Complex protein targeting to dinoflagellate plastids. J Mol Biol 348:1015–1024

    Article  PubMed  CAS  Google Scholar 

  • Reichert AS, Neupert W (2002) Contact sites between the outer and inner membrane of mitochondria-role in protein transport. Biochim Biophys Acta 1592:41–49

    Article  PubMed  CAS  Google Scholar 

  • Rogers MB, Archibald JM, Field MA, Striepen B, Keeling PJ (2004) Plastid-targeting peptides from the chlorarachniophyte Bigelowiella natans. J Eukaryot Microbiol 51:529–535

    Article  PubMed  CAS  Google Scholar 

  • Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ (2007) The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol Biol Evol 24:54–62

    Article  PubMed  CAS  Google Scholar 

  • Schnepf E, Deichgräber G (1984) “Myzocytosis” a kind of endocytosis with implications to compartmentalization in endosymbiosis. Naturwissenschaften 71:218–219

    Article  Google Scholar 

  • Sláviková S, Vacula R, Fang Z, Ehara T, Osafune T, Schwartzbach SD (2005) Homologous and heterologous reconstitution of Golgi to chloroplast transport and protein import into the complex chloroplasts of Euglena. J Cell Sci 118:1651–1661

    Article  PubMed  Google Scholar 

  • Soll J, Schleiff E (2004) Protein import into chloroplasts. Nat Rev Mol Cell Biol 5:198–208

    Article  PubMed  CAS  Google Scholar 

  • Sommer MS, Gould SB, Lehmann P, Gruber A, Przyborski JM, Maier UG (2007) Der1-mediated pre-protein import into the periplastid compartment of chromalveolates? Mol Biol Evol 24:918–928

    Article  PubMed  CAS  Google Scholar 

  • Spork S, Hiss JA, Mandel M, Sommer M, Kooij TWA, Chu T, Schneider G, Maier UG, Przyborski JM (2009) An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Eukaryot Cell 8:1134–1145

    Article  PubMed  CAS  Google Scholar 

  • Stork S, Moog D, Przyborski JM, Wilhelmi I, Zauner S, Maier UG (2012) Distribution of the SELMA translocon in secondary plastids of red algal origin and predicted uncoupling of ubiquitin-dependent translocation from degradation. Eukaryot Cell. doi:10.1128/EC.00183-12

    PubMed  Google Scholar 

  • Sulli C, Fang ZH, Muchhal U, Schwartzbach SD (1999) Topology of Euglena chloroplast protein precursors within endoplasmic reticulum to golgi to chloroplast transport vesicles. J Biol Chem 274:457–463

    Article  PubMed  CAS  Google Scholar 

  • Tonkin CJ, Struck NS, Mullin KA, Stimmler LM, McFadden GI (2006) Evidence for Golgi-independent transport from the early secretory pathway to the plastid in malaria parasites. Mol Microbiol 61:614–630

    Article  PubMed  CAS  Google Scholar 

  • Tonkin CJ, Kalanon M, McFadden GI (2008a) Protein targeting to the malaria parasite plastid. Traffic 9:166–175

    PubMed  CAS  Google Scholar 

  • Tonkin CJ, Roos DS, McFadden GI (2008b) N-terminal positively charged amino acids, but not their exact position, are important for apicoplast transit peptide fidelity in Toxoplasma gondii. Mol Biochem Parasitol 150:192–200

    Article  Google Scholar 

  • van Dooren GG, Schwartzbach SD, Osafune T, McFadden GI (2001) Translocation of proteins across the multiple membranes of complex plastids. Biochim Biophys Acta 1541:34–53

    Article  PubMed  Google Scholar 

  • van Dooren GG, Tomova C, Agrawal S, Humbel BM, Striepen B (2008) Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc Natl Acad Sci U S A 105:13574–13579

    Article  PubMed  Google Scholar 

  • Villarejo A, Burén S, Larsson S, Déjardin A, Monné M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rolland N, von Heijne G, Grebe M, Bako L, Samuelsson G (2005) Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat Cell Biol 7:1224–1231

    Article  PubMed  Google Scholar 

  • Waller RF, Reed MB, Cowman AF, McFadden GI (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 19:1794–1802

    Article  PubMed  CAS  Google Scholar 

  • Wunder T, Martin R, Löffelhardt W, Schleiff E, Steiner JM (2007) The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles. BMC Evol Biol 7:236

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are supported by the Deutsche Forschungsgemeinschaft within SFB 593, SFB-TR1, and GRK 1216, and the LOEWE program of the State of Hessen.

Author information

Authors and Affiliations

  1. Laboratorium für Zellbiologie, Philipps-Universität Marburg, Karl-von-Frisch Strasse 8, 35032, Marburg, Germany

    Christopher Grosche, Franziska Hempel, Kathrin Bolte, Lars Abram, Uwe G. Maier & Stefan Zauner

  2. LOEWE-Zentrum für Synthetische Mikrobiologie (SynMikro), Hans-Meerwein-Strasse, 35032, Marburg, Germany

    Christopher Grosche, Franziska Hempel & Uwe G. Maier

  3. Institut für Zell- und Entwicklungsbiologie der Pflanzen, Universität Bielefeld, Universitätsstrasse 25, 33615, Bielefeld, Germany

    Lars Abram

Authors
  1. Christopher Grosche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Franziska Hempel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathrin Bolte
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lars Abram
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Uwe G. Maier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stefan Zauner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Uwe G. Maier .

Editor information

Editors and Affiliations

  1. Department of Biochemistry, University of Vienna, Vienna, Austria

    Wolfgang Löffelhardt

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Grosche, C., Hempel, F., Bolte, K., Abram, L., Maier, U.G., Zauner, S. (2014). Protein Import into Complex Plastids: Current Findings and Perspectives. In: Löffelhardt, W. (eds) Endosymbiosis. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1303-5_12

Download citation

Publish with us

Policies and ethics

Search

Navigation