Evolutionary pressures on apicoplast transit peptides

Molecular Biology and Evolution

Volumn 21, Issue 12, 2004, Pages 2183-2194

  Ralph, Stuart A ^a,c   Foth, Bernardo J ^a,d   Hall, Neil ^b,e   McFadden, Geoffrey I ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e J CRAIG VENTER INSTITUTE   (United States)

Author keywords

Apicoplast; Nucleotide bias; Plasmodium falciparum; Plastid; Targeting; Transit peptide

Indexed keywords

DNA; NUCLEAR PROTEIN; SIGNAL PEPTIDE;

AMINO ACID METABOLISM; AMINO ACID SEQUENCE; ANGIOSPERM; APICOPLAST; ARTICLE; CONTROLLED STUDY; EVOLUTIONARY ADAPTATION; GENE; MOLECULAR EVOLUTION; NONHUMAN; NUTRIENT AVAILABILITY; PLASMODIUM FALCIPARUM; PLASTID; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN SECONDARY STRUCTURE; PROTEIN SECRETION; PROTEIN TARGETING; PROTEIN TRANSPORT;

AMINO ACIDS; ANIMALS; BASE COMPOSITION; BASE PAIRING; CHLOROPLASTS; COMPUTATIONAL BIOLOGY; DATABASES, NUCLEIC ACID; EVOLUTION, MOLECULAR; PLASMODIUM; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

MAGNOLIOPHYTA; PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 8444244485     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh233     Document Type: Article

References (68)

1. Akashi, H. 2001. Gene expression and molecular evolution. Curr. Opin. Genet. Dev. 11:660-666.
2. Akashi, H., T. Gojobori. 2002. Metabolic efficiency and amino acid composition in the proteomes of Escherichia coli and Bacillus subtilis. Proc. Natl. Acad. Sci. USA 99:3695-3700.
3. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, D. L. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nuc. Acid. Res. 25:3389-3402.
4. Apt, K. E., N. Hoffman, A. R. Grossman. 1993. The γ subunit of R-phycoerythrin and its possible mode of transport into the plastid of red algae. J. Biol. Chem. 268:16208-16215.
5. Apt, K. E., L. Zaslavkaia, J. C. Lippmeier, M. Lang, O. Kilian, R. Wetherbee, A. R. Grossman, P. G. Kroth. 2002. In vivo characterization of diatom multipartite plastid targeting signals. J. Cell. Sci. 115:4061-4069.
6. The Arabidopsis Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815.
7. Baudouin-Cornu, P., Y. Surdin-Kerjan, P. Marliere, D. Thomas. 2001. Molecular evolution of protein atomic composition. Science 293:297-300.
8. Bhaya, D., A. Grossman. 1991. Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol. Gen. Genet. 229:400-404.
9. Blond-Elguindi, S., S. E. Cwirla, W. J. Dower, R. J. Lipshutz, S. R. Sprang, J. F. Sambrook, M. J. Gething. 1993. Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75:717-728.
10. Bruce, B. D. 1998. The role of lipids in plastid protein transport. Plant Mol. Biol. 38:223-246.
11. _. 2000. Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol. 10:440-447.
12. _. 2001. The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochim. Biophys. Acta 1541:2-21.
13. Carels, N., G. Bernardi. 2000. Two classes of genes in plants. Genetics 154:1819-1825.
14. Carlton, J. M., S. V. Angiuoli, B. B. Suh et al. (44 co-authors) 2002. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 419:512-519.
15. 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.
16. Cawley, S. E., A. I. Wirth, T. P. Speed. 2001. Phat - a gene finding program for Plasmodium falciparum. Mol. Biochem. Parasitol. 118:167-174.
17. Chow, K. S., D. P. Singh, J. M. Roper, A. G. Smith. 1997. A single precursor protein for ferrochelatase-I from Arabidopsis is imported in vitro into both chloroplasts and mitochondria. J. Biol. Chem. 272:27565-27571.
18. Deane, J. A., M. Fraunholz, V. Su, U. G. Maier, W. Martin, D. G. Durnford, G. I. McFadden. 2000. Evidence for nucleomorph to host nucleus gene transfer: light-harvesting complex proteins from cryptomonads and chlorarachniophytes. Protist 151:239-252.
19. DeRocher, A., C. B. Hagen, J. E. Froehlich, J. E. Feagin, M. Parsons. 2000. Analysis of targeting sequences demonstrates that trafficking to the Toxoplasma gondii plastid branches off the secretory system. J. Cell Sci. 113:3969-3977.
20. Dorin, D., K. Le Roch, P. Sallicandro, P. Alano, D. Parzy, P. Poullet, L. Meijer, C. Doerig. 2001. Pfnek-1, a NIMA-related kinase from the human malaria parasite Plasmodium falciparum Biochemical properties and possible involvement in MAPK regulation. Eur. J. Biochem. 268:2600-2608.
21. Douglas, S., S. Zauner, M. Fraunholz, M. Beaton, S. Penny, L. T. Deng, X. Wu, M. Reith, T. Cavalier-Smith, U. G. Maier. 2001. The highly reduced genome of an enslaved algal nucleus. Nature 410:1091-1096.
22. Douglas, S. E., C. A. Murphy, D. F. Spencer, M. W. Gray. 1991. Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350: 148-151.
23. Emanuelsson, O., H. Nielsen, S. Brunak, G. von Heijne. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300:1005-1016.
24. Fast, N. M., J. C. Kissinger, D. S. Roos, P. J. Keeling. 2001. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18:418-426.
25. Foth, B. J., S. A. Ralph, C. J. Tonkin, N. S. Struck, M. Fraunholz, D. S. Roos, A. F. Cowman, G. I. McFadden. 2003. Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299:705-708.
26. Gardner, M. J., N. Hall, E. Fung et al. (45 co-authors). 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
27. Gilson, P. R., G. I. McFadden. 2002. Jam packed genomes - a preliminary, comparative analysis of nucleomorphs. Genetica 115:13-28.
28. Harb, O. S., B. Chatterjee, M. J. Fraunholz, M. J. Crawford, M. Nishi, D. S. Roos. 2004. Multiple functionally redundant signals mediate targeting to the apicoplast in the apicomplexan parasite Toxoplasma gondii. Eurkaryotic Cell 3:663-674.
29. Harper, J. T., P. J. Keeling. 2003. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol. Biol. Evol 20:1730-1735.
30. Ishida, K., T. Cavalier-Smith, B. R. Green. 2000. Endomembrane structure and the chloroplast protein targeting pathway in Heterosigma akashiwo (Raphidophyceae, Chromista). J. Phycol. 36:1135-1144.
31. Knarr, G., S. Modrow, A. Todd, M. J. Gething, J. Buchner. 1999. BiP-binding sequences in HIV gp160. Implications for the binding specificity of Bip. J. Biol. Chem. 274:29850-29857.
32. Knight, R. D., S. J. Freeland, L. F. Landweber. 2001. A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol. 2: RESEARCH0010.
33. Krimm, I., P. Gans, J. F. Hernandez, G. J. Arlaud, J. M. Lancelin. 1999. A coil-helix instead of a helix-coil motif can be induced in a chloroplast transit peptide from Chlamydomonas reinhardtii. Eur. J. Biochem. 265:171-180.
34. Lancelin, J. M., I. Bally, G. J. Arlaud, M. Blackledge, P. Gans, M. Stein, J. P. Jacquot. 1994. NMR structures of ferredoxin chloroplastic transit peptide from Chlamydomonas reinhardtii promoted by trifluoroethanol in aqueous solution. FEBS Lett. 343:261-266.
35. Lang, M., K. E. Apt, P. G. Kroth. 1998. Protein transport into complex diatom plastids utilizes two different targeting signals. J. Biol. Chem. 273:30973-30978.
36. Marechal, E., N. Azzouz, C. Santos de Macedo, M. A. Block, J. E. Feagin, R. T. Schwarz, J. Joyard. 2002. Synthesis of chloroplast galactolipids in apicomplexan parasites. Eukaryotic Cell 1:653-656.
37. May, T., J. Soll. 2000. 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 12:53-64.
38. McFadden, G. I., P. R. Gilson, C. J. Hofmann, G. J. Adcock, U.-G. Maier. 1994. Evidence that an amoeba acquired a chloroplast by retaining part of an engulfed eukaryotic alga. Proc. Natl. Acad. Sci. USA 91:3690-3694.
39. Moriyama, E. N., J. R. Powell. 1997. Codon usage bias and tRNA abundance in Drosophila. J. Mol. Evol. 45:514-523.
40. Musto, H., S. Caccio, H. Rodriguez-Maseda, G. Bernardi. 1997. Compositional constraints in the extremely GC-poor genome of Plasmodium falciparum. Mem. Inst. Oswaldo Cruz 92: 835-841.
41. Musto, H., H. Rodriguez-Maseda, G. Bernardi. 1995. Compositional properties of nuclear genes from Plasmodium falciparum. Gene 152:127-132.
42. Musto, H., H. Romero, A. Zavala, K. Jabbari, G. Bernardi. 1999. Synonymous codon choices in the extremely GC-poor genome of Plasmodium falciparum: compositional constraints and translational selection. J. Mol. Evol. 49:27-35.
43. Nakai, K., M. Kaneshia. 1992. A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 14:897-911.
44. Nielsen, H., J. Engelbrecht, S. Brunak, G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
45. Pancic, P. G., H. Strotmann. 1993. Structure of the nuclear encoded γ subunit of CF0Fi of the diatom Odontella sinensis including its presequence. FEBS Lett. 320:61-66.
46. Peeters, N., I. Small. 2001. Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta 1541:54-63.
47. Perkins, S. L., J. J. Schall. 2002. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J. Parasitol. 88:972-978.
48. Pinnaduwage, P., B. D. Bruce. 1996. In vitro interaction between a chloroplast transit peptide and chloroplast outer envelope lipids is sequence-specific and lipid class- dependent. J. Biol. Chem. 271:32907-32915.
49. Rathore, D., A. M. Wahl, M. Sullivan, T. F. McCutchan. 2001. A phylogenetic comparison of gene trees constructed from plastid, mitochondrial and genomic DNA of Plasmodium species. Mol. Biochem. Parasitol. 114:89-94.
50. Saul, A., D. Battistutta. 1988. Codon usage in Plasmodium falciparum. Mol. Biochem. Parasitol. 27:35-42.
51. Salzberg, S. L., M. Pertea, A. L. Delcher, M. J. Gardner, H. Tettelin. 1999. Interpolated Markov models for eukaryotic gene finding. Genomics 59:24-31.
52. Singer, G. A., D. A. Hickey. 2000. Nucleotide bias causes a genomewide bias in the amino acid composition of proteins. Mol. Biol. Evol. 17:1581-1588.
53. Su, Q., K. Schmid, C. Schild, A. Boschetti. 2001. Effect of precursor protein phosphorylation on import into isolated chloroplasts from Chlamydomonas. FEBS Lett. 508:165-169.
54. Surolia, N., A. Surolia. 2001. Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat. Med. 7:167-173.
55. Theg, S. M., F. J. Geske. 1992. Biophysical characterization of a transit peptide directing chloroplast protein import. Biochemistry 31:5053-5060.
56. van Dooren, G. G., S. D. Schwartzbach, T. Osafune, G. I. McFadden. 2001. Translocation of proteins across the multiple membranes of complex plastids. Biochim. Biophys. Acta 1541:34-53.
57. van Dooren, G. G., V. Su, M. C. D'Ombrain, G. I. McFadden. 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.
58. Verra, F., A. L. Hughes. 1999. Biased amino acid composition in repeat regions of Plasmodium antigens. Mol. Biol. Evol. 16: 627-633.
59. von Heijne, G., K. Nishikawa. 1991. Chloroplast transit peptides: the perfect random coil? FEBS Lett. 278:1-3.
60. Waegemann, K., J. Soll. 1996. Phosphorylation of the transit sequence of chloroplast precursor proteins. J. Biol. Chem. 271: 6545-6554.
61. Waller, R. F., M. B. Reed, A. F. Cowman, G. I. McFadden. 2000. Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J. 19:1794-1802.
62. Wastl, J., U. G. Maier. 2000. Transport of proteins into cryptomonads complex plastids. J. Biol. Chem. 275:23194-23198.
63. Weber, J. L. 1987. Analysis of sequences from the extremely A + T-rich genome of Plasmodium falciparum. Gene 52:103-109.
64. Wienk, H. L., R. W. Wechselberger, M. Czisch B. de Kruijff. 2000. Structure, dynamics, and insertion of a chloroplast targeting peptide in mixed micelles. Biochemistry 39:8219-8227.
65. Wienk, H. L. J., M. Czisch B. de Kruijff 1999. The structural flexibility of the preferredoxin transit peptide. FEBS Lett 453:318-326.
66. Yu, J., S. Hu, J. Wang et al. (86 co-authors). 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296:79-92.
67. Yung, S., N. Lang-Unnasch. 1999. Targeting of a nuclear encoded protein to the apicoplast of Toxoplasma gondii. J. Eukaryot. Microbiol. 46:79S-80S.
68. Yung, S. C., T. R. Unnasch, N. Lang-Unnasch. 2003. Cis and trans factors involved in apicoplast targeting in Toxoplasma gondii. J. Parasitol. 89:767-776.