Sculpting the endomembrane system in deep time: High resolution phylogenetics of Rab GTPases

Journal of Cell Science

Volumn 125, Issue 10, 2012, Pages 2500-2508

  Elias, Marek ^a,b   Brighouse, Andrew ^c   Gabernet Castello, Carme ^c   Field, Mark C ^c   Dacks, Joel B ^d  

^a UNIVERSITY OF OSTRAVA   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Evolution; Membrane traffic; Phylogenetics

Indexed keywords

RAB PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL ORGANELLE; CLADISTICS; CONTROLLED STUDY; DATA BASE; EUKARYOTE; INTERMETHOD COMPARISON; MEMBRANE; MEMBRANE TRANSPORT; MOLECULAR EVOLUTION; PHYLOGENETIC TREE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN STRUCTURE; TAXONOMY;

ANIMALS; CLASSIFICATION; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; HUMANS; INTRACELLULAR MEMBRANES; MOLECULAR SEQUENCE DATA; PHYLOGENY; RAB GTP-BINDING PROTEINS;

EUKARYOTA; METAZOA;

EID: 84864805551     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.101378     Document Type: Article

References (54)

1. Abascal, F., Zardoya, R. and Posada, D. (2005). ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104-2105.
2. 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.
3. Agop-Nersesian, C., Naissant, B., Ben Rached, F., Rauch, M., Kretzschmar, A., Thiberge, S., Menard, R., Ferguson, D. J., Meissner, M. and Langsley, G. (2009). Rab11A-controlled assembly of the inner membrane complex is required for completion of apicomplexan cytokinesis. PLoS Pathog. 5, e1000270.
4. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
5. Ayong, L., Pagnotti, G., Tobon, A. B. and Chakrabarti, D. (2007). Identification of Plasmodium falciparum family of SNAREs. Mol. Biochem. Parasitol. 152, 113-122.
6. Brighouse, A., Dacks, J. B. and Field, M. C. (2010). Rab protein evolution and the history of the eukaryotic endomembrane system. Cell. Mol. Life Sci. 67, 3449-3465.
7. Bright, L. J., Kambesis, N., Nelson, S. B., Jeong, B. and Turkewitz, A. P. (2010). Comprehensive analysis reveals dynamic and evolutionary plasticity of Rab GTPases and membrane traffic in Tetrahymena thermophila. PLoS Genet. 6, e1001155.
8. Burki, F., Inagaki, Y., Bråte, J., Archibald, J. M., Keeling, P. J., Cavalier-Smith, T., Sakaguchi, M., Hashimoto, T., Horak, A., Kumar, S. et al. (2009). Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, Telonemia and Centroheliozoa, are related to photosynthetic chromalveolates. Genome Biol. Evol. 1, 231-238.
9. Cai, H., Reinisch, K. and Ferro-Novick, S. (2007). Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev. Cell 12, 671-682.
10. Carlton, J. M., Hirt, R. P., Silva, J. C., Delcher, A. L., Schatz, M., Zhao, Q., Wortman, J. R., Bidwell, S. L., Alsmark, U. C., Besteiro, S. et al. (2007). Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315, 207-212.
11. Cavalier-Smith, T. (2002). The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297-354.
12. Colicelli, J. (2004). Human RAS superfamily proteins and related GTPases. Sci. STKE 2004, re13.
13. Dacks, J. B. and Doolittle, W. F. (2002). Novel syntaxin gene sequences from Giardia, Trypanosoma and algae: implications for the ancient evolution of the eukaryotic endomembrane system. J. Cell Sci. 115, 1635-1642.
14. Dacks, J. B. and Field, M. C. (2007). Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J. Cell Sci. 120, 2977-2985.
15. Dacks, J. B., Poon, P. P. and Field, M. C. (2008). Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution. Proc. Natl. Acad. Sci. USA 105, 588-593.
16. Dacks, J. B., Peden, A. A. and Field, M. C. (2009). Evolution of specificity in the eukaryotic endomembrane system. Int. J. Biochem. Cell Biol. 41, 330-340.
17. Diekmann, Y., Seixas, E., Gouw, M., Tavares-Cadete, F., Seabra, M. C. and Pereira-Leal, J. B. (2011). Thousands of rab GTPases for the cell biologist. PLOS Comput. Biol. 7, e1002217.
18. Elias, M. (2010). Patterns and processes in the evolution of the eukaryotic endomembrane system. Mol. Membr. Biol. 27, 469-489.
19. Elias, E. V., Quiroga, R., Gottig, N., Nakanishi, H., Nash, T. E., Neiman, A. and Lujan, H. D. (2008). Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J. Biol. Chem. 283, 35996-36010.
20. Elias, M., Patron, N. J. and Keeling, P. J. (2009). The RAB family GTPase Rab1A from Plasmodium falciparum defines a unique paralog shared by chromalveolates and Rhizaria. J. Eukaryot. Microbiol. 56, 348-356.
21. Embley, T. M. and Martin, W. (2006). Eukaryotic evolution, changes and challenges. Nature 440, 623-630.
22. Field, M. C. and Carrington, M. (2004). Intracellular membrane transport systems in Trypanosoma brucei. Traffic 5, 905-913.
23. Fritz-Laylin, L. K., Prochnik, S. E., Ginger, M. L., Dacks, J. B., Carpenter, M. L., Field, M. C., Kuo, A., Paredez, A., Chapman, J., Pham, J. et al. (2010). The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631-642.
24. Fukuda, R., McNew, J. A., Weber, T., Parlati, F., Engel, T., Nickel, W., Rothman, J. E. and Söllner, T. H. (2000). Functional architecture of an intracellular membrane t-SNARE. Nature 407, 198-202.
25. Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.
26. Gurkan, C., Koulov, A. V. and Balch, W. E. (2007). An evolutionary perspective on eukaryotic membrane trafficking. Adv. Exp. Med. Biol. 607, 73-83.
27. Hirst, J., Barlow, L. D., Francisco, G. C., Sahlender, D. A., Seaman, M. N., Dacks, J. B. and Robinson, M. S. (2011). The fifth adaptor protein complex. PLoS Biol. 9, e1001170.
28. Huizing, M., Helip-Wooley, A., Westbroek, W., Gunay-Aygun, M. and Gahl, W. A. (2008). Disorders of lysosome-related organelle biogenesis: clinical and molecular genetics. Annu. Rev. Genomics Hum. Genet. 9, 359-386.
29. Keeling, P. J. (2010). The endosymbiotic origin, diversification and fate of plastids. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 729-748.
30. Kissmehl, R., Schilde, C., Wassmer, T., Danzer, C., Nuehse, K., Lutter, K. and Plattner, H. (2007). Molecular identification of 26 syntaxin genes and their assignment to the different trafficking pathways in Paramecium. Traffic 8, 523-542.
31. Kloepper, T. H., Kienle, C. N. and Fasshauer, D. (2007). An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell 18, 3463-3471.
32. Koonin, E. V. (2010). Preview. The incredible expanding ancestor of eukaryotes. Cell 140, 606-608.
33. Lal, K., Field, M. C., Carlton, J. M., Warwicker, J. and Hirt, R. P. (2005). Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis. Mol. Biochem. Parasitol. 143, 226-235.
34. Letunic, I., Doerks, T. and Bork, P. (2009). SMART 6: recent updates and new developments. Nucleic Acids Res. 37, D229-D232.
35. Lumb, J. H., Leung, K. F., Dubois, K. N. and Field, M. C. (2011). Rab28 function in trypanosomes: interactions with retromer and ESCRT pathways. J. Cell Sci. 124, 3771-3783.
36. Mackiewicz, P. and Wyroba, E. (2009). Phylogeny and evolution of Rab7 and Rab9 proteins. BMC Evol. Biol. 9, 101.
37. Nakada-Tsukui, K., Saito-Nakano, Y., Husain, A. and Nozaki, T. (2010). Conservation and function of Rab small GTPases in Entamoeba: annotation of E. invadens Rab and its use for the understanding of Entamoeba biology. Exp. Parasitol. 126, 337-347.
38. Olkkonen, V. M. and Ikonen, E. (2006). When intracellular logistics fails - genetic defects in membrane trafficking. J. Cell Sci. 119, 5031-5045.
39. Pereira-Leal, J. B. (2008). The Ypt/Rab family and the evolution of trafficking in fungi. Traffic 9, 27-38.
40. Pereira-Leal, J. B. and Seabra, M. C. (2001). Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313, 889-901.
41. Roger, A. J. and Simpson, A. G. (2009). Evolution: revisiting the root of the eukaryote tree. Curr. Biol. 19, R165-R167.
42. Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
43. Rutherford, S. and Moore, I. (2002). The Arabidopsis Rab GTPase family: another enigma variation. Curr. Opin. Plant Biol. 5, 518-528.
44. Saito-Nakano, Y., Loftus, B. J., Hall, N. and Nozaki, T. (2005). The diversity of rab GTPases in Entamoeba histolytica. Exp. Parasitol. 110, 244-252.
45. Saito-Nakano, Y., Nakahara, T., Nakano, K., Nozaki, T. and Numata, O. (2010). Marked amplification and diversification of products of ras genes from rat brain, Rab GTPases, in the ciliates Tetrahymena thermophila and Paramecium tetraurelia. J. Eukaryot. Microbiol. 57, 389-399.
46. Sanderfoot, A. (2007). Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol. 144, 6-17.
47. Schmidt, H. A., Strimmer, K., Vingron, M. and von Haeseler, A. (2002). TREEPUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18, 502-504.
48. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
49. Stanier, R. (1970). Some aspects of the biology of cells and their possible evolutionary significance. In Organization and Control in Prokaryotic and Eukaryotic Cells (ed. H. Charles and B. Knight), pp. 1-38. Cambridge, UK: Cambridge University Press.
50. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525.
51. Südhof, T. C. and Rothman, J. E. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474-477.
52. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
53. Walker, G., Dorrell, R. G., Schlacht, A. and Dacks, J. B. (2011). Eukaryotic systematics: a user's guide for cell biologists and parasitologists. Parasitology 138, 1638-1663.
54. Woollard, A. A. and Moore, I. (2008). The functions of Rab GTPases in plant membrane traffic. Curr. Opin. Plant Biol. 11, 610-619.