Evolution of Protein Targeting into “Complex” Plastids: The “Secretory Transport Hypothesis”

O. Kilian; P. G. Kroth

doi:10.1055/s-2003-42710

Plant Biology, Table of Contents

Plant Biol (Stuttg) 2003; 5(4): 350-358
DOI: 10.1055/s-2003-42710

Acute View

Georg Thieme Verlag Stuttgart · New York

Evolution of Protein Targeting into “Complex” Plastids: The “Secretory Transport Hypothesis”

O. Kilian¹ , P. G. Kroth¹

¹Fachbereich Biologie, Universität Konstanz, Konstanz, Germany

Abstract

In algae different types of plastids are known, which vary in pigment content and ultrastructure, providing an opportunity to study their evolutionary origin. One interesting feature is the number of envelope membranes surrounding the plastids. Red algae, green algae and glaucophytes have plastids with two membranes. They are thought to originate from a primary endocytobiosis event, a process in which a prokaryotic cyanobacterium was engulfed by a eukaryotic host cell and transformed into a plastid. Several other algal groups, like euglenophytes and heterokont algae (diatoms, brown algae, etc.), have plastids with three or four surrounding membranes, respectively, probably reflecting the evolution of these organisms by so-called secondary endocytobiosis, which is the uptake of a eukaryotic alga by a eukaryotic host cell. A prerequisite for the successful establishment of primary or secondary endocytobiosis must be the development of suitable protein targeting machineries to allow the transport of nucleus-encoded plastid proteins across the various plastid envelope membranes. Here, we discuss the possible evolution of such protein transport systems. We propose that the secretory system of the respective host cell might have been the essential tool to establish protein transport into primary as well as into secondary plastids.

Key words

Protein transport - chloroplast - secondary endocytobiosis.

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References

1 Apt K. E., Hoffman N. E., Grossman A. R.. The gamma subunit of R-phycoerythrin and its possible mode of transport into the plastid of red algae. J. Biol. Chem.. (1993); 268 16208-16215
2 Apt K. E., Zaslavkaia L., Lippmeier J. C., Lang M., Kilian O., Wetherbee R., Grossman A. R., Kroth P. G.. In vivo characterization of diatom multipartite plastid targeting signals. J. Cell Sci.. (2002); 115 4061-4069
3 Bhaya D., Grossman A. R.. Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol. Gen. Genet.. (1991); 229 400-404
4 Blanchard J. L., Lynch M.. Organellar genes - why do they end up in the nucleus?. Trends Genet.. (2000); 16 315-320
5 Bodył A.. How are plastid proteins of the apicomplexan parasites imported? A hypothesis. Acta Protozool.. (1997); 38 31-37
6 Bodył A.. Is protein import into plastids with four-membrane envelopes dependent on two Toc systems in tandem?. Plant Biology. (2002); 4 423-431
7 Bouck G. B.. Fine structure and organelle associations in brown algae. J. Cell Biol.. (1965); 26 523-537
8 Bruce B. D.. Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol.. (2000); 10 440-447
9 Cavalier-Smith T.. The origins of plastids. Biol. J. Linn. Soc.. (1982); 17 289-306
10 Cavalier-Smith T.. The kingdom Chromista: origin and systematics. Round, F. E. and Chapman, D. J., eds. Progress in Phycological Research. Bristol; Biopress Ltd. (1986): 309-347
11 Cavalier-Smith T.. Membrane heredity, symbiogenesis, and the multiple origins of algae. Arai, R., Kato, M., and Doi, Y., eds. Biodiversity and Evolution. Tokyo; National Science Museum Foundation (1995): 75-114
12 Cavalier-Smith T.. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Euk. Microbiol.. (1999); 46 347-366
13 Cavalier-Smith T.. Membrane heredity and early chloroplast evolution. Trends Plant Sci.. (2000); 5 174-182
14 Cavalier-Smith T.. Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Phil. Trans. R. Soc. Lond. B.. (2002); 358 109-134
15 Chen X. J., Schnell D. J.. Protein import into chloroplasts. Trends Cell Biol.. (1999); 9 222-227
16 Delwiche C. F.. Tracing the thread of plastid diversity through the tapestry of life. Amer. Natural.. (1999); 154 S164-S177
17 Delwiche C. F., Palmer J. D.. The origin of plastids and their spread via secondary symbiosis. Plant Syst. Evol.. (1997); 11 53-86
18 DeRocher A., Hagen C. B., Froehlich J. E., Feagin J. E., Parsons M.. Analysis of targeting sequences demonstrates that trafficking to the Toxoplasma gondii plastid branches off the secretory system. J. Cell Sci.. (2000); 113 3969-3977
19 Doolittle W. F.. A paradigm gets shifty. Nature. (1998); 392 15-16
20 Douglas S. E.. Plastid evolution: origins, diversity, trends. Curr. Op. Genet. Develop.. (1998); 8 655-661
21 Douglas S., Zauner S., Fraunholz M., Beaton M., Penny S., Deng L.-T., Wu X., Reith M., Cavalier-Smith T., Maier U.-G.. The highly reduced genome of an enslaved algal nucleus. Nature. (2001); 410 1091-1096
22 Durnford D. G., Deane J. A., Tan S., McFadden G. I., Gantt E., Green B. R.. A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J. Mol. Evol.. (1999); 48 59-68
23 Gibbs S. P.. The chloroplasts of Euglena may have evolved from symbiotic green algae. Can. J. Bot.. (1978); 56 2883-2889
24 Gibbs S. P.. The route of entry of cytoplasmically synthesized proteins into chloroplasts of algae possessing chloroplast ER. J. Cell Sci.. (1979); 35 253-266
25 Gibbs S. P.. The chloroplast endoplasmic reticulum: structure, function, and evolutionary significance. Int. Rev. Cytol.. (1981); 72 49-99
26 Gillot M. A., Gibbs S. P.. The cryptomonad nucleomorph: its ultrastructure and evolutionary significance. J. Phycol.. (1980); 16 558-568
27 Gilson P. R., Maier U. G., McFadden G. I.. Size isn't everything: lessons in gentic miniturization from nucleomorphs. Curr. Op. Gen. Dev.. (1997); 7 800-806
28 Häuber M. M., Müller S. B., Speth V., Maier U. G.. How to evolve a complex plastid? - A hypothesis. Bot. Acta. (1994); 107 383-386
29 Heins L., Collinson I., Soll J.. The protein translocation apparatus of chloroplast envelopes. Trends Plant Sci.. (1998); 3 56-61
30 Heins L., Soll J.. Chloroplast biogenesis: Mixing the prokaryotic and the eukaryotic?. Curr. Biol.. (1998); 8 R215-R217
31 Heins L., Mehrle A., Hemmler R., Wagner R., Kuchler M., Hormann F., Sveshnikov D., Soll J.. The preprotein conducting channel at the inner envelope membrane of plastids. EMBO J.. (2002); 21 2616-2625
32 Hopkins J., Fowler R., Krishna S., Wilson I., Mitchell G., Bannister L.. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist. (1999); 150 283-292
33 Inagaki J., Fujita Y., Hase T., Yamamoto Y.. Protein translocation within chloroplast is similar in Euglena and higher plants. Biochem. Biophys. Res. Commun.. (2000); 277 436-442
34 Ishida K., Cavalier-Smith T., Green B. R.. Endomembrane structure and the chloroplast protein targeting pathway in Heterosigma akashiwo (Raphidophyceae, Chromista). J. Phycol.. (2000); 36 1135-1144
35 Jakowitsch J., Neumann-Spallart C., Ma Y., Schenk H. E. A., Bohnert H. J., Löffelhardt W.. In vitro import of pre-ferredoxin-NADP-oxidoreductase from Cyanophora paradoxa into cyanelles and into pea chloroplasts. FEBS Lett.. (1996); 381 153-155
36 Joyard J., Teyssier E., Miege C., Berny-Seigneurin D., Marechal E., Block M. A., Dorne A. J., Rolland N., Ajlani G., Douce R.. The biochemical machinery of plastid envelope membranes. Plant Physiol.. (1998); 118 715-723
37 Jürgens U. J., Weckesser J.. Carotenoid-containing outer membrane of Synechocystis sp. strain PCC6714. J. Bacteriol.. (1985); 164 384-389
38 Kadowaki K. I., Kubo N., Ozawa K., Hirai A.. Targeting presequence acquisition after mitochondrial gene transfer to the nucleus occurs by duplication of existing targeting signals. EMBO J.. (1996); 15 6652-6661
39 Keegstra K., Cline K.. Protein import and routing systems of chloroplasts. Plant Cell. (1999); 11 557-570
40 Kindle K. L., Lawrence S. D.. Transit peptide mutations that impair in vitro and in vivo chloroplast protein import do not affect accumulation of the gamma-subunit of chloroplast ATPase. Plant Physiol.. (1998); 116 1179-1190
41 Köhler R. A., Cao J., Zipfel W. R., Webb W. W., Hanson M. R.. Exchange of protein molecules through connections between higher plant plastids. Science. (1997 a); 276 2039-2042
42 Köhler S., Delwiche C. F., Denny P. W., Tilney L. G., Webster P., Wilson R. J. M., Palmer J. D., Roos D. S.. A plastid of probable green algal origin in apicomplexan parasites. Science. (1997 b); 275 1485-1489
43 Kroth P., Strotmann H.. Diatom plastids: secondary endocytobiosis, plastid genome and protein import. Physiol. Plant.. (1999); 107 136-141
44 Lang M., Apt K. E., Kroth P. G.. Protein transport in “complex” diatom plastids utilizes two different targeting domains. J. Biol. Chem.. (1998); 273 30973-30978
45 Long M., de Souza S. J., Rosenberg C., Gilbert W.. Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome c₁ precursor. Proc. Natl. Acad. Sci. USA. (1996); 93 7727-7731
46 Martin W., Herrmann R. G.. Gene transfer from organelles to the nucleus: How much, what happens, and why?. Plant Physiol.. (1998); 118 9-17
47 Martin W., Müller M.. The hydrogen hypothesis for the first eukaryote. Nature. (1998); 392 37-41
48 Martin W., Stoebe B., Goremykin V., Hansmann S., Hasegawa M., Kowallik K. V.. Gene transfer to the nucleus and the evolution of chloroplasts. Nature. (1998); 393 162-165
49 McFadden G. I.. Plastids and protein targeting. J. Euk. Microbiol.. (1999); 46 339-346
50 McFadden G. I.. Primary and secondary endosymbiosis and the origin of plastids. J. Phycol.. (2001); 37 951-959
51 McFadden G. I., Gilson P. R., Hofmann C. J. B., Adcock G. J., Maier U.-G.. Evidence that an amoeba aquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc. Natl. Acad. Sci. USA. (1994); 91 3690-3694
52 McFadden G. I., Roos D. S.. Apicomplexan plastids as drug targets. Trends Microbiol.. (1999); 7 328-333
53 Melkonian M.. Systematics and evolution of algae. I. Genomics meets phylogeny. Progr. Botany. (2001); 62 340-382
54 Muchhal U. S., Schwartzbach S. D.. Characterization of a Euglena gene encoding a polyprotein precursor to the light-harvesting chlorophyll a/b-binding protein of photosystem II. Plant Mol. Biol.. (1992); 18 287-299
55 Palmer J. D.. Organelle genomes: going, going, gone!. Science. (1997); 275 790-791
56 Park H., Eggink L. L., Roberson R. W., Hoober J. K.. Transfer of proteins from the chloroplast to vacuoles in Chlamydomonas reinhardtii (Chlorophyta): A pathway for degradation. J. Phycol.. (1999); 35 528-538
57 Rassow J., Pfanner N.. The protein import machinery of the mitochondrial membranes. Traffic. (2000); 1 457-464
58 Reumann S., Davila-Aponte J., Keegstra K.. The evolutionary origin of the protein-translocating channel of chloroplastidic envelope membranes: identification of a cyanobacterial homolog. Proc. Natl. Acad. Sci.. (1999); 96 784-789
59 Reumann S., Keegstra K.. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci.. (1999); 4 302-307
60 Robinson C., Hynds P. J., Robinson D., Mant A.. Multiple pathways for the targeting of thylakoid proteins in chloroplasts. Plant Mol. Biol.. (1998); 38 209-221
61 Schnepf E.. From prey via endosymbiont to plastid: comparative studies in dinoflagellates. Lewin, R. A., ed. Origins of Plastids. New York; Chapman & Hall (1993): 53-76
62 Schwartzbach S. D., Osafune T., Löffelhardt W.. Protein import into cyanelles and complex chloroplasts. Plant Mol. Biol.. (1998); 38 247-263
63 Smith-Johannsen H., Gibbs S. P.. Effects of chloramphenicol on chloroplast and mitochondrial ultrastructure in Ochromonas danica. . J. Cell Biol.. (1972); 52 598-614
64 Steiner J. M., Löffelhardt W.. Protein import into cyanelles. Trends Plant Sci.. (2002); 7 72-77
65 Su Q., Schumann P., Schild C., Boschetti A.. A processing intermediate of a stromal chloroplast import protein in Chlamydomonas. . Biochem. J.. (1999); 344 391-395
66 Sulli C., Fang Z. W., Muchhal U. S., Schwartzbach S. D.. Topology of Euglena chloroplast protein precursors within endoplasmic reticulum to golgi to chloroplast transport vesicles. J. Biol. Chem.. (1999); 274 457-463
67 Vothknecht U. C., Soll J.. Protein import: The hitchhikers guide into chloroplasts. Biol. Chem.. (2000); 381 887-897
68 Waller R. F., Reed M. B., Cowman A. F., and McFadden G. I.. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J.. (2000); 19 1794-1802
69 Walter P., Johnson A. E.. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol.. (1994); 10 87-119
70 Wastl J., Maier U. G.. Transport of proteins into cryptomonads complex plastids. J. Biol. Chem.. (2000); 275 23194-23198

P. G. Kroth

Universität Konstanz
Fachbereich Biologie

Postfach M611

78457 Konstanz

Germany

Email: peter.kroth@uni-konstanz.de

Section Editor: G. Thiel