Abstract
Fifty-six nuclear protein coding genes from Taxonomically Broad EST Database and other databases were selected for phylogenomic-based examination of alternative phylogenetic hypotheses concerning intergroup relationship between multicellular animals (Metazoa) and other representatives of Opisthokonta. The results of this work support sister group relationship between Metazoa and Choanoflagellata. Both of these groups form the taxon Holozoa along with the monophyletic Ichthyosporea or Mesomycetozoea (a group that includes Amoebidium parasiticum, Sphaeroforma arctica, and Capsaspora owczarzaki). These phylogenetic hypotheses receive high statistical support both when utilizing whole alignment and when only 5000 randomly selected alignment positions are used. The presented results suggest subdivision of Fungi into Eumycota and lower fungi, Chytridiomycota. The latter form a monophyletic group that comprises Chytridiales + Spizellomycetales + Blastocladiales (Batrachochytrium, Spizellomyces, Allomyces, Blastocladiella), contrary to the earlier reports based on the analysis of 18S rRNA and a limited set of protein coding genes. The phylogenetic distribution of genes coding for a ubiquitin-fused ribosomal protein S30 implies at least three independent cases of gene fusion: in the ancestors of Holozoa, in heterotrophic Heterokonta (Oomycetes and Blastocystis), and in the ancestors of Cryptophyta and Glaucophyta. Ubiquitin-like sequences fused with ribosomal protein S30 outside of Holozoa are not FUBI orthologs. Two independent events of FUBI replacement by the ubiquitin sequence were detected in the lineage of C. owczarzaki and in the monophyletic group of nematode worms Tylenchomorpha + Cephalobidae. Bursaphelenchus xylophilus (Aphelenchoidoidea) retains a state typical of the rest of the Metazoa. The data emphasize the fact that the reliability of phylogenetic reconstructions depends on the number of analyzed genes to a lesser extent than on our ability to recognize reconstruction artifacts.
Similar content being viewed by others
Abbreviations
- eEF1A:
-
eukaryotic elongation factor 1A
- EFL:
-
elongation factor-like (a paralog of elongation factor 1A)
- FUBI:
-
ubiquitin-like peptide fused with S30 ribosomal protein of animals and other Holozoa
- Hsp:
-
heat shock protein, chaperon
- RpL:
-
ribosomal protein of large ribosomal subunit
- RpS:
-
ribosomal protein of small ribosomal subunit
- tef:
-
gene of elongation factor 1A
References
Spirin, A. S., Belozersky, A. N., Shugaeva, N. V., and Vanyushin, B. F. (1957) Biokhimiya, 22, 744–754.
Beklemishev, V. N. (1994) Methodology of Systematics [in Russian], KMK Publishing House, Moscow.
Hennig, W. (1966) Phylogenetic Systematics, Illinois University Press, Urbana.
Shatalkin, A. I. (1988) Biological Systematics [in Russian], Moscow State University Publishing House, Moscow.
Pavlinov, I. Ya. (2005) Introduction into Modern Phylogenetics (Cladogenetic Analysis) [in Russian], KMK Publishing House, Moscow.
Baldauf, S. L., and Palmer, J. D. (1991) Proc. Natl. Acad. Sci. USA, 90, 11558–11562.
Petrov, N. B., and Aleshin, V. V. (2002) Genetika, 38, 1043–1062.
Moreira, D., von der Heyden, S., Bass, D., Lopez-Garcia, P., Chao, E., and Cavalier-Smith, T. (2007) Mol. Phylogenet. Evol., 44, 255–266.
Cavalier-Smith, T., and Chao, E. E.-Y. (2003) Protist, 154, 341–358.
Shatalkin, A. I. (2005) Zh. Obshch. Biol., 66, 389–415.
Steenkamp, E. T., Wright, J., and Baldauf, S. L. (2006) Mol. Biol. Evol., 23, 93–106.
Philip, G. K., Creevey, C. J., and McInerney, J. O. (2005) Mol. Biol. Evol., 22, 1175–1184.
Seravin, L. N., and Gudkov, A. V. (2005) Zh. Obshch. Biol., 66, 212–223.
Stechmann, A., and Cavalier-Smith, T. (2002) Science, 297, 89–91.
Keeling, P. J., and Inagaki, Y. (2004) Proc. Natl. Acad. Sci. USA, 101, 15380–15385.
King, N., and Carroll, S. B. (2001) Proc. Natl. Acad. Sci. USA, 98, 15032–15037.
Jeffroy, O., Brinkmann, H., Delsuc, F., and Philippe, H. (2006) Trends Genet., 22, 225–231.
Felsenstein, J. (1978) Syst. Zool., 27, 401–410.
Lang, B. F., O’Kelly, C., Nerad, T., Gray, M. W., and Burger, G. (2002) Curr. Biol., 12, 1773–1778.
Medina, M., Collins, A. G., Taylor, J. W., Valentine, J. W., Lipps, J. H., Amaral-Zettler, L., and Sogin, M. L. (2003) Int. J. Astrobiol., 2, 203–211.
Ruiz-Trillo, I., Inagaki, Y., Davis, L. A., Sperstad, S., Landfald, B., and Roger, A. J. (2004) Curr. Biol., 14, R946–R947.
Ruiz-Trillo, I., Lane, C. E., Archibald, J. M., and Roger A. J. (2006) J. Eukaryot. Microbiol., 53, 379–384.
Hertel, L. A., Bayne, C. J., and Loker, E. S. (2003) Int. J. Parasitol., 32, 1183–1191.
Jimenez-Guri, E., Philippe, H., Okamura, B., and Holland, P. W. (2007) Science, 317, 116–118.
Ruiz-Trillo, I., Burger, G., Holland, P. W., King, N., Lang, B. F., Roger, A. J., and Gray, M. W. (2007) Trends Genet., 23, 113–118.
Lutzoni, F., Kauff, F., Cox, C. J., McLaughlin, D., et al. (2004) Am. J. Bot., 91, 1446–1480.
James, T. Y., Kauff, F., Schoch, C., Matheny, P. B., et al. (2006) Nature, 443, 818–822.
Kishino, H., and Hasegawa, M. (1989) J. Mol. Evol., 29, 170–179.
Shimodaira, H., and Hasegawa, M. (1999) Mol. Biol. Evol., 16, 1114–1116.
Shimodaira, H., and Hasegawa, M. (2001) Bioinformatics, 17, 1246–1247.
Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package) version 3.5c, Department of Genetics, University of Washington, Seattle.
Philippe, H. (1993) Nucleic Acids Res., 21, 5264–5272.
Logacheva, M. D., Penin, A. A., Samigullin, T. Y., Vallejo-Roman, C. M., and Antonov, A. S. (2007) Biochemistry (Moscow), 72, 1324–1330.
Kas, K., Michiels, L., and Merregaert, J. (1992) Biochem. Biophys. Res. Commun., 187, 927–933.
Perina, D., Cetkovic, H., Harcet, M., Premzl, M., Lukic-Bilela, L., Muller, W. E., and Gamulin, V. (2006) Gene, 366, 275–284.
Baker, R. T., Williamson, N. A., and Wettenhall, R. E. (1996) J. Biol. Chem., 271, 13549–13555.
Jones, D., and Candido, E. P. (1993) J. Biol. Chem., 268, 19545–19551.
Meldal, B. H., Debenham, N. J., De Ley, P., De Ley, I. T., Vanfleteren, J. R., Vierstraete, A. R., Bert, W., Borgonie, G., Moens, T., Tyler, P. A., Austen, M. C., Blaxter, M. L., Rogers, A. D., and Lambshead, P. J. (2007) Mol. Phylogenet. Evol., 42, 622–636.
Drozdovskii, E. M. (1968) Dokl. AN SSSR, 180, 750–753.
Finley, D., Bartel, B., and Varshavsky, A. (1989) Nature, 338, 394–401.
Rossman, T. G., Visalli, M. A., and Komissarova, E. V. (2003) Oncogene, 22, 1817–1821.
Burki, F., Shalchian-Tabrizi, K., Minge, M., Skjaeveland, A., Nikolaev, S. I., Jakobsen, K. S., and Pawlowski, J. (2007) PLoS ONE, 2, e790.
Rodriguez-Ezpeleta, N., Brinkmann, H., Burger, G., Roger, A. J., Gray, M. W., Philippe, H., and Lang, B. F. (2007) Curr Biol., 17, 1420–1425.
Cavalier-Smith, T., and Chao, E. E-Y. (2006) J. Mol. Evol., 62, 388–420.
Bhattacharya, D., Helmchen, T., Bibeau, C., and Melkonian, M. (1995) Mol. Biol. Evol., 12, 415–420.
Hoef-Emden, K., Marin, B., and Melkonian, M. (2002) J. Mol. Evol., 55, 161–179.
Deane, J. A., Strachan, I. M., Saunders, G. W., Hill, D. R. A., and McFadden, G. I. (2002) J. Phycol., 38, 1529–8817.
Bourlat, S. J., Juliusdottir, T., Lowe, C. J., Freeman, R., Aronowicz, J., Kirschner, M., Lander, E. S., Thorndyke, M., Nakano, H., Kohn, A. B., Heyland, A., Moroz, L. L., Copley, R. R., and Telford, M. J. (2006) Nature, 444, 85–88.
Baurain, D., Brinkmann, H., and Philippe, H. (2006) Mol. Biol. Evol., 24, 6–9.
Samigullin, T. K., Yacentyuk, S. P., Degtyaryeva, G. V., Valiehoroman, K. M., Bobrova, V. K., Capesius, I., Martin, W. F., Troitsky, A. V., Filin, V. R., and Antonov, A. S. (2002) Arctoa, 11, 31–43.
Qiu, Y. L., Li, L., Wang, B., Chen, Z., Knoop, V., Groth-Malonek, M., Dombrovska, O., Lee, J., Kent, L., Rest, J., Estabrook, G. F., Hendry, T. A., Taylor, D. W., Testa, C. M., Ambros, M., Crandall-Stotler, B., Duff, R. J., Stech, M., Frey, W., Quandt, D., and Davis, C. C. (2006) Proc. Natl. Acad. Sci. USA, 103, 15511–15516.
Rokas, A., Williams, B. L., King, N., and Carroll, S. B. (2003) Nature, 425, 798–804.
Philippe, H., Lartillot, N., and Brinkmann, H. (2005) Mol. Biol. Evol., 22, 1246–1253.
Dopazo, H., Santoyo, J., and Dopazo, J. (2004) Bioinformatics, 20(Suppl. 1), i116–i121.
Degtjareva, G. V., Samigullin, T. Y., Sokoloff, D. D., and Vallejo-Roman, C. M. (2004) Botan. J., 89, 896–907.
Rokas, A., and Holland, P. W. H. (2000) Trends Ecol. Evol., 15, 454–459.
Schmidt, H. A., Strimmer, K., Vingron, M., and von Haeseler, A. (2002) Bioinformatics, 18, 502–504.
Huelsenbeck, J. P., and Ronquist, F. (2001) Bioinformatics, 17, 754–755.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © V. V. Aleshin, A. V. Konstantinova, K. V. Mikhailov, M. A. Nikitin, N. B. Petrov, 2007, published in Biokhimiya, 2007, Vol. 72, No. 12, pp. 1610–1623.
Rights and permissions
About this article
Cite this article
Aleshin, V.V., Konstantinova, A.V., Mikhailov, K.V. et al. Do we need many genes for phylogenetic inference?. Biochemistry Moscow 72, 1313–1323 (2007). https://doi.org/10.1134/S000629790712005X
Received:
Issue Date:
DOI: https://doi.org/10.1134/S000629790712005X