Phylogenomic analysis identifies red algal genes of endosymbiotic origin in the chromalveolates

Molecular Biology and Evolution

Volumn 23, Issue 3, 2006, Pages 663-674

  Li, Shenglan ^a   Nosenko, Tetyana ^a   Hackett, Jeremiah D ^a,b   Bhattacharya, Debashish ^a  

^a UNIVERSITY OF IOWA   (United States)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

Chromalveolates; Emiliania huxleyi; Endosymbiosis; Gene transfer; Phylogenomics

Indexed keywords

CHLOROPHYLL;

ALGA; ARTICLE; BACTERIUM; CYANOBACTERIUM; EMILIANIA HUXLEYI; ENDOSYMBIONT; ENDOSYMBIOSIS; EXPRESSED SEQUENCE TAG; FUNGUS; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE TARGETING; HAPLOTYPE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTID; PROTEIN EXPRESSION; RED ALGA;

ALGAE, RED; ALGAL PROTEINS; ANIMALS; GENE TRANSFER, HORIZONTAL; GENES, PLANT; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; PLASTIDS; SYMBIOSIS; THYLAKOIDS;

ALGAE; ANIMALIA; BACTERIA (MICROORGANISMS); CHLOROPHYTA; CYANOBACTERIA; EMBRYOPHYTA; EMILIANIA HUXLEYI; EUKARYOTA; FUNGI; GLAUCOCYSTOPHYCEAE; PLANTAE; PROTISTA; RHODOPHYTA;

EID: 33244468402     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msj075     Document Type: Article

References (63)

1. Archibald, J. M., M. B. Rogers, M. Toop, K. Ishida, and P. J. Keeling. 2003. Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc. Natl. Acad. Sci. USA 100:7678-7683.
2. Armbrust, E. V., J. A. Berges, C. Bowler et al. (45 co-authors). 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79-86.
3. Asamizu, E., M. Nakajima, Y. Kitade, N. Saga, Y. Nakamura, and S. Tabata. 2003. Comparison of RNA expression profiles between the two generations of Porphyra yezoensis (Rhodophyta), based on expressed sequence tag frequency analysis. J. Phycol. 39:923-930.
4. Bachvaroff, T. R., G. T. Concepcion, C. R. Rogers, E. M. Herman, and C. F. Delwiche. 2004. Dinoflagellate expressed sequence tag data indicate massive transfer of chloroplast genes to the nuclear genome. Protist 155:65-78.
5. Bachvaroff, T. R., M. V. Sanchez Puerta, and C. F. Delwiche. 2005. Chlorophyll c-containing plastid relationships based on analyses of a multigene data set with all four chromalveolate lineages. Mol. Biol. Evol. 22:1777-1782.
6. Baldauf, S. L., A. J. Roger, I. Wenk-Siefert, and W. F. Doolittle. 2000. A kingdom-level phytogeny of eukaryotes based on combined protein data. Science 290:972-977.
7. Bhattacharya, D., and L. Medlin. 1995. The phylogeny of plastids: a review based on comparisons of small-subunit ribosomal RNA coding regions. J. Phycol. 31:489-498.
8. Bhattacharya, D., H. S. Yoon, and J. D. Hackett. 2004. Photosynthetic eukaryotes unite: endosymbiosis connects the dots. BioEssays 26:50-60.
9. Bonaldo, M. F., G. Lennon, and M. B. Soares. 1996. Normalization and subtraction: two approaches to facilitate gene discovery. Genome Res. 6:791-806.
10. 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.
11. _. 2004. Only six kingdoms of life. Proc. Biol. Sci. 271:1251-1262.
12. Coppin, A., J. S. Varre, L. Lienard, D. Dauvillee, Y. Guerardel, M. O. Soyer-Gobillard, A. Buleon, S. Ball, and S. Tomavo. 2005. Evolution of plant-like crystalline storage polysaccharide in the protozoan parasite Toxoplasma gondii argues for a red alga ancestry. J. Mol. Evol. 60:257-267.
13. Delwiche, C. F. 1999. Tracing the thread of plastid diversity through the tapestry of life. Am. Nat. 154(S4):S164-S177.
14. Eisen, J. A., and C. M. Fraser. 2003. Phylogenomics: intersection of evolution and genomics. Science 300:1706-1707.
15. Fast, N. M., J. C. Kissinger, D. S. Roos, and 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.
16. Felsenstein, J. 1985. Confidence limits on phytogenies: an approach using the bootstrap. Evolution 39:783-791.
17. Funes, S., E. Davidson, A. Reyes-Prieto, S. Magallon, P. Herion, M. P. King, and D. Gonzalez-Halphen. 2002. A green algal apicoplast ancestor. Science 298:2155.
18. Gibbs, S. P. 1993. The evolution of algal chloroplasts. Pp. 107-121 in R. A Lewin, ed. Origins of plastids. Chapman and Hall, New York.
19. Gibson, L. C. D., R. D. Willows, C. G. Kannangara, D. von Wettstein, and C. N. Hunter. 1995. Magnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: reconstitution of activity by combining the products of the bchH, -I, and -D genes expressed in Escherichia coli. Proc. Natl. Acad. Sci. USA 92:1941-1944.
20. Graciet, E., S. Lebreton, and B. Gontero. 2004. Emergence of new regulatory mechanisms in the Benson-Calvin pathway via protein-protein interactions: a glyceraldehyde-3-phosphate dehydrogenase/CP12/ phosphoribulokinase complex. J. Exp. Bot. 55:1245-1254.
21. Graybeal, A. 1998. Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47:9-17.
22. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
23. Hackett, J. D., H. S. Yoon, M. B. Soares, M. F. Bonaldo, T. L. Casavant, T. E. Scheetz, and D. Bhattacharya. 2005. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics 6:80.
24. Hackett, J. D., H. S. Yoon, M. B. Soares, M. F. Bonaldo, T. L. Casavant, T. E. Scheetz, T. Nosenko, and D. Bhattacharya. 2004. Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr. Biol. 14:213-218.
25. Hagopian, J. C., M. Reis, J. P. Kitajima, D. Bhattacharya, and M. C. Oliveira. 2004. Comparative analysis of the complete plastid genome sequence of the red alga Gracilaria tenuistipitata var. liui: insight on the evolution of rhodoplasts and their relationship to other plastids. J. Mol. Evol. 59:464-477.
26. Harper, J. T., E. Waanders, and P. J. Keeling. 2005. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int. J. Syst. Evol. Microbiol. 55:487-496.
27. He, Z., L. Li, and S. Luan. 2004. Characterization of an Arabidopsis cDNA encoding a thylakoid lumen protein related to a novel 'pentapeptide repeat' family of proteins. Plant Physiol. 134:1248-1267.
28. Hillis, D. M., D. D. Pollock, J. A. McGuire, and D. J. Zwickl. 2003. Is sparse sampling a problem for phylogenetic inference? Syst. Biol. 52:124-126.
29. Huang, J., N. Mullapudi, C. A. Lancto, M. Scott, M. S. Abrahamsen, and J. C. Kissinger. 2004. Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol. 5:R88.
30. Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755.
31. Ishida, K., and B. R. Green. 2002. Second- and third-hand chloroplasts in dinoflagellates: phylogeny of oxygen-evolving enhancer 1 (psbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont. Proc. Natl. Acad. Sci. USA 99:9294-9299.
32. Jensen, P. E., L. C. D. Gibson, K. W. Henningsen, and C. N. Hunter. 1996. Expression of the chlI, chlD, and chlH genes from the cyanobacterium Synechocystis PCC6803 in Escherichia coli and demonstration that the three cognate proteins are required for magnesium-protoporphyrin chelatase activity. J. Biol. Chem. 271:16662-16667.
33. Jensen, P. E., L. C. D. Gibson, F. Shephard, V. Smith, and C. N. Hunter. 1999. Introduction of a new branchpoint in tetrapyrrole biosynthesis in Escherichia coli by co-expression of genes encoding the chlorophyll-specific enzymes magnesium chelatase and magnesium protoporphyrin methyltransferase. FEBS Lett. 455:349-354.
34. Johnson, C. H., V. Kruft, and A. R. Subramanian. 1990. Identification of a plastid-specific ribosomal protein in the 30 S subunit of chloroplast ribosomes and isolation of the cDNA clone encoding its cytoplasmic precursor. J. Biol. Chem. 265:12790-12795.
35. Kieselbach, T., A. Mant, C. Robinson, and W. P. Schröder. 1998. Characterization of an Arabidopsis cDNA encoding a thylakoid lumen protein related to a novel 'pentapeptide repeat' family of proteins. FEES Lett. 428:241-244.
36. Köhler, S., C. F. Delwiche, P. W. Denny, L. G. Tilney, P. Webster, R. J. Wilson, J. D. Palmer, and D. S. Roos. 1997. A plastid of probable green algal origin in apicomplexan parasites. Science 275:1485-1489.
37. Lidie, K. L., J. C. Ryan, M. Barbier, and F. M. Van Dolah. 2005. Gene expression in the Florida red tide dinoflagellate Karenia brevis: analysis of an expressed sequence tag (EST) library and development of a DNA microarray. Mar. Biotechol. 7:481-493.
38. Lopez-Juez, E., and K. A. Pyke. 2005. Plastids unleashed: their development and their integration in plant development. Int. J. Dev. Biol. 49:557-577.
39. Lupas, N. A., and T. Frickey. 2004. PhyloGenie: automated phylome generation and analysis. Nucleic Acids Res. 32:5231-5238.
40. Martin, W., and R. G. Herrmann. 1998. Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol. 118:9-17.
41. Martin, W., T. Rujan, E. Richly, A. Hansen, S. Cornelsen, T. Lins, D. Leister, B. Stoebe, M. Hasegawa, and D. Penny. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99:12246-12251.
42. Matsuzaki, M., O. Misumi, I. T. Shin et al. (40 co-authors). 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653-657.
43. McFadden, G. I. 1999. Plastids and protein targeting. Curr. Opin. Plant. Biol. 2:513-519.
44. McFadden, G. I., and G. G. van Dooren. 2004. Evolution: red algal genome affirms a common origin of all plastids. Curr. Biol. 14:R514-R516.
45. Michels, A. K., N. Wedel, and P. G. Kroth. 2005. Diatom plastids possess a phosphoribulokinase with an altered regulation and no oxidative pentose phosphate pathway. Plant Physiol. 137:911-920.
46. Miyagishima, S. Y., H. Nozaki, K. Nishida, K. Nishida, M. Matsuzaki, and T. Kuroiwa. 2004. Two types of FtsZ proteins in mitochondria and red-lineage chloroplasts: the duplication of FtsZ is implicated in endosymbiosis. J. Mol. Evol. 58:291-303.
47. Moreira, D., H. Le Guyader, and H. Phillippe. 2000. The origin of red algae and the evolution of chloroplasts. Nature 405:69-72.
48. Patron, N. J., M. B. Rogers, and P. J. Keeling. 2004. Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot. Cell 3:1169-1175.
49. Patron, N. J., R. F. Waller, J. M. Archibald, and P. J. Keeling. 2005. Complex protein targeting to dinoflagellate plastids. J. Mol. Biol. 348:1015-1024.
50. Porter, M. A., S. Milanez, C. D. Stringer, and F. C. Hartman. 1986. Purification and characterization of ribulose-5-phosphate kinase from spinach. Arch. Biochem. Biophys. 245:14-23.
51. Rodríguez-Ezpeleta, N., H. Brinkmann, S. C. Burey, B. Roure, G. Burger, W. Loffelhardt, H. J. Bohnert, H. Philippe, and B. F. Lang. 2005. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15:1325-1330.
52. Romano, P., J. Gray, P. Horton, and S. Luan. 2005. Plant immunophilins: functional versatility beyond protein maturation. New Phytol. 166:753-769.
53. Scala, S., N. Carels, A. Falciatore, M. L. Chiusano, and C. Bowler. 2002. Genome properties of the diatom Phaeodactylum tricornutum. Plant Physiol. 129:993-1002.
54. Schmid, H. C., U. Oster, J. Kogel, S. Lenz, and W. Rudiger. 2001. Cloning and characterization of chlorophyll synthase from Avena sativa. Biol. Chem. 382:903-911.
55. Tengs, T., O. J. Dahlberg, K. Shalchian-Tabrizi, D. Klaveness, K. Rudi, C. F. Delwiche, and K. S. Jakobsen. 2000. Phylogenetic analyses indicate that the 19′ hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol. Biol. Evol. 17:718-729.
56. Trivedi, N., J. Bishof, S. Davis et al. (50 co-authors). 2002. Parallel creation of non-redundant gene indices from partial mRNA transcripts. Future Gen. Comp. Sys. 18:863-870.
57. Weber, A. P., C. Oesterhelt, W. Gross et al. (12 co-authors). 2004. EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol. Biol. 55:17-32.
58. Wilson, D. N., and K. H. Nierhaus. The how and Y of cold shock. Nat. Struct. Mol. Biol. 11:1026-1028.
59. Yamaguchi, K., and A. R. Subramanian. 2000. The plastid ribosomal proteins. Identification of all the proteins in the 50 S subunit of an organelle ribosome (chloroplast). J. Biol. Chem. 275:28466-28482.
60. Yoon, H. S., J. D. Hackett, G. Pinto, and D. Bhattacharya. 2002. The single, ancient origin of chromist plastids. Proc. Natl. Acad. Sci. USA 99:15507-15512.
61. Yoon, H. S., J. D. Hackett, C. Ciniglia, G. Pinto, and D. Bhattacharya. 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21:809-818.
62. Yoon, H. S., J. D. Hackett, F. M. Van Dolah, T. Nosenko, K. L. Lidie, and D. Bhattacharya. 2005. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol. Biol. Evol. 22:1299-1308.
63. Zarnt, T., T. Tradler, G. Stoller, C. Scholz, F. X. Schmid, and G. Fischer. 1997. Modular structure of the trigger factor required for high activity in protein folding. J. Mol. Biol. 271:827-837.