Transport of nuclear-encoded proteins into secondarily evolved plastids

Biological Chemistry

Volumn 388, Issue 9, 2007, Pages 899-906

  Hempel, Franziska ^a   Bozarth, Andrew ^a   Sommer, Maik S ^a   Zauner, Stefan ^a   Przyborski, Jude M ^a   Maier, Uwe G ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Protein targeting; Secondary endosymbiosis; Secondary plastids

Indexed keywords

NUCLEAR PROTEIN;

ALGA; APICOMPLEXA; CELL NUCLEUS; CRYPTOPHYTA; ENDOSYMBIOSIS; GREEN ALGA; NONHUMAN; PHOTOTROPH; PLASTID; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RED ALGA; REVIEW; THYLAKOID MEMBRANE;

ALGAE; ALGAL PROTEINS; BIOSYNTHETIC PATHWAYS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR MEMBRANES; MODELS, BIOLOGICAL; PLANT PROTEINS; PLANTS; PLASTIDS; PROTEIN TRANSPORT; THYLAKOIDS;

ALGAE; EUKARYOTA;

EID: 34547925627     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2007.119     Document Type: Review

References (66)

1. Adl, S.M., Simpson, A.G., Farmer, M.A., Andersen, R.A., Anderson, O.R., Barta, J.R., Bowser, S.S., Brugerolle, G., Fensome, R.A., Fredericq, S., et al. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399-451.
2. Apt, K.E., Zaslavkaia, L., Lippmeier, J.C., Lang, M., Kilian, O., Wetherbee, R., Grossman, A.R., and Kroth, P.G. (2002). In vivo characterization of diatom multipartite plastid targeting signals. J. Cell Sci. 115, 4061-4069.
3. Archibald, J.M. and Keeling, P.J. (2002). Recycled plastids: a 'green movement' in eukaryotic evolution. Trends Genet. 18, 577-584.
4. Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H., Zhou, S., Allen, A.E., Apt, K.E., Bechner, M., et al. (2004). The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306, 79-86.
5. Bachvaroff, T.R., Sanchez Puerta, M.V., and Delwiche, C.F. (2005). Chlorophyll c-containing plastid relationships based on analyses of a multigene data set with all four chromalveolate lineages. Mol. Biol. Evol. 22, 1772-1782.
6. Becker, T., Jelic, M., Vojta, A., Radunz, A., Soll, J., and Schleiff, E. (2004). Preprotein recognition by the Toc complex. EMBO J. 23, 520-530.
7. Bhaya, D. and Grossman, A. (1991). Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol. Gen. Genet. 229, 400-404.
8. Bodyl, A. (2004). Evolutionary origin of a preprotein translocase in the periplastid membrane of complex plastids: a hypothesis. Plant Biol. 6, 513-518.
9. 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.
10. Cavalier-Smith, T. (2000). Membrane heredity and early chloroplast evolution. Trends Plant Sci. 5, 174-182.
11. Cavalier-Smith, T. (2002). Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr. Biol. 12, R62-R64.
12. Chaal, B.K. and Green, B.R. (2005). Protein import pathways in 'complex' chloroplasts derived from secondary endosymbiosis involving a red algal ancestor. Plant Mol. Biol. 57, 333-342.
13. Chaal, B.K., Ishida, K., and Green, B.R. (2003). A thylakoidal processing peptidase from the heterokont alga Heterosigma akashiwo. Plant Mol. Biol. 52, 463-472.
14. Cheresh, P., Harrison, T., Fujioka, H., and Haldar, K. (2002). Targeting the malarial plastid via the parasitophorous vacuole. J. Biol. Chem. 277, 16265-16277.
15. Delwiche, C.F. and Palmer, J. (1997). The origin of plastids and their spread via secondary symbiosis. In: Origins of the Algae and their Plastids, D. Bhattacharya, ed. (Vienna, Austria: Springer), pp. 53-86.
16. DeRocher, A., Hagen, C.B., Froehlich, J.E., Feagin, J.E., and 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.
17. Deschamps, P., Haferkamp, I., Dauvillee, D., Haebel, S., Steup, M., Buleon, A., Putaux, J.L., Colleoni, C., d'Hulst, C., Plancke, C., et al. (2006). Nature of the periplastidial pathway of starch synthesis in the cryptophyte Guillardia theta. Eukaryot. Cell 5, 954-963.
18. Douglas, S., Zauner, S., Fraunholz, M., Beaton, M., Penny, S., Deng, L.T., Wu, X., Reith, M., Cavalier-Smith, T., and Maier, U.G. (2001). The highly reduced genome of an enslaved algal nucleus. Nature 410, 1091-1096.
19. Durnford, D.G. and Gray, M.W. (2006). Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryot. Cell 5, 13084-13090.
20. Foth, B.J., Ralph, S.A., Tonkin, C.J., Struck, N.S., Fraunholz, M., Roos, D.S., Cowman, A.F., and McFadden, G.I. (2003). Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299, 705-708.
21. Gibbs, S.P. (1979). The route of entry of cytoplasmically synthesized proteins into chloroplasts of algae possessing chloroplast ER. J. Cell Sci. 35, 253-266.
22. Gibbs, S.P. (1981). The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann. NY Acad. Sci. 361, 193-208.
23. Gilson, P.R., Su, V., Slamovits, C.H., Reith, M.E., Keeling, P.J., and McFadden, G.I. (2006). Complete nucleotide sequence of the chlorarachniophyte nucleomorph: nature's smallest nucleus. Proc. Natl. Acad. Sci. USA 103, 9566-9571.
24. Gould, S.B., Sommer, M.S., Hadfi, K., Zauner, S., Kroth, P.G., and Maier, U.G. (2006a). Protein targeting into the complex plastid of cryptophytes. J. Mol. Evol. 62, 674-681.
25. Gould, S.B., Sommer, M.S., Kroth, P.G., Gile, G.H., Keeling, P.J., and Maier, U.G. (2006b). Nucleus-to-nucleus gene transfer and protein retargeting into a remnant cytoplasm of cryptophytes and diatoms. Mol. Biol. Evol. 23, 2413-2422.
26. Greenwood, A.D., Griffiths, H.B., and Santore, U.J. (1977). Chloroplasts and cell compartments in Cryptophyceae. Br. Phycol. J. 12, 119.
27. Haldar, K., Mohandas, N., Samuel, B.U., Harrison, T., Hiller, N.L., Akompong, T., and Cheresh, P. (2002). Protein and lipid trafficking induced in erythrocytes infected by malaria parasites. Cell Microbiol. 4, 383-395.
28. Harper, J.T., Waanders, E., and Keeling, P.J. (2005). On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int. J. Syst. Evol. Microbiol. 55, 487-496.
29. Hibberd, D.J. and Norris, R.E. (1984). Cytology and ultrastructure of Chlorarachnion reptans (Chlorarachniophyta divisio nova, Chlorarachniophyceae classis nova). J. Phycol. 20, 310-330.
30. Inagaki, J., Fujita, Y., Hase, T., and Yamamoto, Y. (2000). Protein translocation within chloroplast is similar in Euglena and higher plants. Biochem. Biophys. Res. Commun. 277, 436-442.
31. Ismail, N. and Ng, D.T. (2006). Have you HRD? Understanding ERAD is DOAble! Cell 126, 237-239.
32. Jarvis, P. and Robinson, C. (2004). Mechanisms of protein import and routing in chloroplasts. Curr. Biol. 14, R1064-R1077.
33. Kessler, F. and Schnell, D.J. (2004). Chloroplast protein import: solve the GTPase riddle for entry. Trends Cell Biol. 14, 334-338.
34. Kessler, F. and Schnell, D.J. (2006). The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic 7, 248-257.
35. Kilian, O. and Kroth, P.G. (2005). Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J. 41, 175-183.
36. Kroth, P.G. and Strotmann, H. (1999). Diatom plastids: secondary endocytobiosis, plastid genome and protein import. Physiol. Plant. 107, 136-141.
37. Lang, M. and Kroth, P.G. (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.
38. Lang, M., Apt, K.E., and Kroth, P.G. (1998). Protein transport into 'complex' diatom plastids utilizes two different targeting signals. J. Biol. Chem. 273, 30973-30978.
39. May, T. and Soll, J. (2000). 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12, 53-64.
40. McFadden, G.I. (2001). Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 37, 951-959.
41. McFadden, G.I. and van Dooren, G.G. (2004). Evolution: red algal genome affirms a common origin of all plastids. Curr. Biol. 14, R514-R516.
42. McFadden, G.I., Reith, M.E., Munholland, J., and Lang-Unnasch, N. (1996). Plastid in human parasites. Nature 381, 482.
43. Melkonian, M. (2001). Systematics and evolution of algae. In: Progress in Botany, Vol. 62, W. Beyschlag, ed. (Berlin/Heidelberg, Germany: Springer-Verlag), pp. 340-382.
44. Meusser, B., Hirsch, C., Jarosch, E., and Sommer, T. (2005). ERAD: the long road to destruction. Nat. Cell Biol. 7, 766-772.
45. Nassoury, N., Cappadocia, M., and Morse, D. (2003). Plastid ultrastructure defines the protein import pathway in dinoflagellates. J. Cell Sci. 116, 2867-2874.
46. Patron, N.J., Waller, R.F., Archibald, J.M., and Keeling, P.J. (2005). Complex protein targeting to dinoflagellate plastids. J. Mol. Biol. 348, 1015-1024.
47. Ponpuak, M., Klemba, M., Park, M., Gluzman, I.Y., Lamppa, G.K., and Goldberg, D.E. (2007). A role for falcilysin in transit peptide degradation in the Plasmodium falciparum apicoplast. Mol. Microbiol. 63, 314-334.
48. Rogers, M.B., Archibald, J.M., Field, M.A., Li, C., Striepen, B., and Keeling, P.J. (2004). Plastid-targeting peptides from the chlorarachniophyte Bigelowiella natans. J. Eukaryot. Microbiol. 51, 529-535.
49. Rogers, M.B., Gilson, P.R., Su, V., McFadden, G.I., and Keeling, P.J. (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.
50. Slavikova, S., Vacula, R., Fang, Z., Ehara, T., Osafune, T., and Schwartzbach, S.D. (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.
51. Soll, J. and Schleiff, E. (2004). Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5, 198-208.
52. Sommer, M.S., Gould, S.B., Lehmann, P., Gruber, A., Przyborski, J.M., and Maier, U.-G. (2007). Der1-mediated pre-protein import into the periplastid compartment of chromalveolates? Mol. Biol. Evol. 24, 1-11.
53. Steiner, J.M., Yusa, F., Pompe, J.A., and Loffelhardt, W. (2005). Homologous protein import machineries in chloroplasts and cyanelles. Plant J. 44, 646-652.
54. Stoebe, B. and Maier, U.-G. (2002). One, two, three: nature's tool box for building plastids. Protoplasma 219, 123-130.
55. Sulli, C., Fang, Z., Muchhal, U., and Schwartzbach, S.D. (1999). Topology of Euglena chloroplast protein precursors within endoplasmic reticulum to Golgi to chloroplast transport vesicles. J. Biol. Chem. 274, 457-463.
56. Szafranski, K., Lehmann, R., Parra, G., Guigo, R., and Glockner, G. (2005). Gene organization features in A/T-rich organisms. J. Mol. Evol. 60, 90-98.
57. Tonkin, C.J., Roos, D.S., and McFadden, G.I. (2006a). 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.
58. Tonkin, C.J., Struck, N.S., Mullin, K.A., Stimmler, L.M., and McFadden, G.I. (2006b). Evidence for Golgi-independent transport from the early secretory pathway to the plastid in malaria parasites. Mol. Microbiol. 61, 614-630.
59. Tyler, B.M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R.H., Aerts, A., Arredondo, F.D., Baxter, L., Bensasson, D., Beynon, J.L., et al. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313, 1261-1266.
60. van Dooren, G.G., Schwartzbach, S.D., Osafune, T., and Mc-Fadden, G.I. (2001). Translocation of proteins across the multiple membranes of complex plastids. Biochim. Biophys. Acta 1541, 34-53.
61. van Dooren, G.G., Su, V., D'Ombrain, M.C., and McFadden, G.I. (2002). Processing of an apicoplast leader sequence in Plasmodium falciparum and the identification of a putative leader cleavage enzyme. J. Biol. Chem. 277, 23612-23619.
62. Villarejo, A., Buren, S., Larsson, S., Dejardin, A., Monne, M., Rudhe, C., Karlsson, J., Jansson, S., Lerouge, P., Rolland, N., et al. (2005). Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat. Cell Biol. 7, 1224-1231.
63. Waller, R.F., Keeling, P.J., Donald, R.G.K., Striepen, B., Handmann, E., Lang-Unnasch, N., Cowman, A.F., Besra, G.S., Roos, D.S., and McFadden, G.I. (1998). Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 95, 12352-12357.
64. Waller, R.F., Reed, M.B., Cowman, A.F., and McFadden, G.I. (2000). Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19, 1794-1802.
65. Wastl, J. and Maier, U.G. (2000). Transport of proteins into cryptomonads complex plastids. J. Biol. Chem. 275, 23194-23198.
66. Yoon, H.S., Hackett, J.D., and Bhattacharya, D. (2002). A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. USA 99, 11724-11729.