Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina

Molecular Biology and Evolution

Volumn 25, Issue 7, 2008, Pages 1297-1306

  Slamovits, Claudio H ^a   Keeling, Patrick J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Apicoplast; Chromalveolates; Dinoflagellates; Oxyrrhis; Plastid evolution

Indexed keywords

AMINO ACID METABOLISM; APICOPLAST; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; CYTOSOL; EUKARYOTE; GENE IDENTIFICATION; GENETIC ANALYSIS; GENOME; NONHUMAN; OXYRRHIS MARINA; PHOTOSYNTHESIS; PHYLOGENY; PLASTID; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; DINOFLAGELLIDA; EVOLUTION, MOLECULAR; LIKELIHOOD FUNCTIONS; PHYLOGENY; PLASTIDS; PROTOZOAN PROTEINS;

ALGAE; CHROMALVEOLATA; DINOPHYCEAE; OXYRRHIS; OXYRRHIS MARINA; PROTISTA;

EID: 45849090251     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn075     Document Type: Article

References (61)

1. Abrahamsen MS, Templeton TJ, Enomoto S, et al. (20 coauthors). 2004. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 304:441-445.
2. Archibald JM, Keeling PJ. 2002. Recycled plastids: a green movement in eukaryotic evolution. Trends Genet. 18:577-584.
3. Archibald JM, Rogers MB, Toop M, Ishida K, Keeling PJ. 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.
4. Bachvaroff TR, Concepcion GT, Rogers CR, Herman EM, Delwiche CF. 2004. Dinoflagellate expressed sequence tags data indicate massive transfer of chloroplast genes to the nuclear genome. Protist. 155:65-78.
5. Bodyl A. 2005. Do plastid-related characters support the chromalveolate hypothesis? J Phycol. 41:712-719.
6. Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Nikolaev SI, Jakobsen KS, Pawlowski J. 2007. Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE. 2:e790.
7. 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.
8. Eisenreich W, Bacher A, Arigoni D, Rohdich F. 2004. Biosynthesis of isoprenoids via the non-mevalonate pathway. Cell Mol Life Sci. 61:1401-1426.
9. Fast NM, Xue L, Bingham S, Keeling PJ. 2002. Re-examining alveolate evolution using multiple protein molecular phylogenies. J Eukaryot Microbiol. 49:30-37.
10. Foth BJ, McFadden GI. 2003. The apicoplast: a plastid in Plasmodium falciparum and other apicomplexan parasites. Int Rev Cytol. 224:57-110.
11. Givan CV. 1975. Light-dependent synthesis of glutamine in pea chloroplast preparations. Planta. 122:281-291.
12. Guindon S, Lethiec F, Duroux P, Gascuel O. 2005. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33:W557-W559.
13. Hackett JD, Yoon HS, Li S, Reyes-Prieto A, Rummele SE, Bhattacharya D. 2007. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol. 24:1702-1713.
14. Hackett JD, Yoon HS, Soares MB, Bonaldo MF, Casavant TL, Scheetz TE, Nosenko T, Bhattacharya D. 2004. Migration of the plastid genome to the nucleus in a peridinin dinoflagellate. Curr Biol. 14:213-218.
15. Harb OS, Chatterjee B, Fraunholz MJ, Crawford MJ, Nishi M, Roos DS. 2004. Multiple functionally redundant signals mediate targeting to the apicoplast in the apicomplexan parasite Toxoplasma gondii. Eukaryot Cell. 3:663-674.
16. Harper JT, Keeling PJ. 2003. Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol. 20:1730-1735.
17. Harper JT, Waanders E, Keeling PJ. 2005. On the monophyly of the chromalveolates using a six-protein phylogeny of eukaryotes. Int J Sys Evol Microbiol. 55:487-496.
18. Huang J, Mullapudi N, Lancto CA, Scott M, Abrahamsen MS, Kissinger JC. 2004. Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol. 5:R88.
19. Keeling PJ. 2004. The diversity and evolutionary history of plastids and their hosts. Am J Bot. 91:1481-1493.
20. Keeling PJ, Palmer JD, Donald RG, Roos DS, Waller RF, McFadden GI. 1999. Shikimate pathway in apicomplexan parasites. Nature. 397:219-220.
21. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S. 2004. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr Biol. 14:354-362.
22. Leander BS, Keeling PJ. 2004. Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from HSP90 and actin phylogenies. J Phycol. 40:341-350.
23. Lichtenthaler HK. 2000. Non-mevalonate isoprenoid biosynthesis: enzymes, genes and inhibitors. BiochemSoc Trans. 28:785-789.
24. Moore RB, Obornik M, Janouskovec J, et al. (14 co-authors). 2008. A photosynthetic alveolate closely related to apicomplexan parasites. Nature. 451:959-963.
25. Morse D, Salois P, Markovic P, Hastings JW. 1995. A nuclear-encoded form II RuBisCO in dinoflagellates. Science. 268:1622-1624.
26. Nassoury N, Cappadocia M, Morse D. 2003. Plastid ultrastructure defines the protein import pathway in dinoflagellates. J Cell Sci. 116:2867-2874.
27. Nimer NA, Brownlee C, Merrett MJ. 1999. Extracellular carbonic anhydrase facilitates carbon dioxide availability for photosynthesis in the marine dinoflagellate Prorocentrum micans. Plant Physiol. 120:105-112.
28. Obornik M, Green BR. 2005. Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol Biol Evol. 22:2343-2353.
29. O'Brien EA, Koski LB, Zhang Y, Yang L, Wang E, Gray MW, Burger G, Lang BF. 2007. TBestDB: a taxonomically broad database of expressed sequence tags (ESTs). Nucleic Acids Res. 35:D445-D451.
30. Palmer JD. 2003. The symbiotic birth and spread of plastids: how many times and whodunit? J Phycol. 39:1-9.
31. Patron NJ, Rogers MB, Keeling PJ. 2004. Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell. 3:1169-1175.
32. Patron NJ, Waller RF, Archibald JM, Keeling PJ. 2005. Complex protein targeting to dinoflagellate plastids. J Mol Biol. 348:1015-1024.
33. Patron NJ, Waller RF, Keeling PJ. 2006. A tertiary plastid uses genes from two endosymbionts. J Mol Biol. 357:1373-1382.
34. Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG, McLeod R, Roberts CW. 2006. Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot Cell. 5:1517-1531.
35. Roberts F, Roberts CW, Johnson JJ, et al. 1998. Evidence for the shikimate pathway in apicomplexan parasites. Nature. 393:801-805.
36. Robertson DL, Tartar A. 2006. Evolution of glutamine synthetase in heterokonts: evidence for endosymbiotic gene transfer and the early evolution of photosynthesis. Mol Biol Evol. 23:1048-1055.
37. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 19:1572-1574.
38. Roos DS, Crawford MJ, Donald RG, Fraunholz M, Harb OS, He CY, Kissinger JC, Shaw MK, Striepen B. 2002. Mining the Plasmodium genome database to define organellar function: what does the apicoplast do? Philos Trans R Soc Lond B Biol Sci. 357:35-46.
39. Rost B, Richter KU, Riebesell U, Hansen PJ. 2006. Inorganic carbon acquisition in red tide dinoflagellates. Plant Cell Environ. 29:810-822.
40. Saldarriaga JF, McEwan ML, Fast NM, Taylor FJR, Keeling PJ. 2003. Multiple protein phylogenies show that Oxyhrris marina and Perkinsus marinus are early branches of the dinoflagellate lineage. Int J Sys Evol Microbiol. 53:355-365.
41. Saldarriaga JF, Taylor FJR, Keeling PJ, Cavalier-Smith T. 2001. Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol. 53:204-213.
42. Sanchez-Puerta MV, Lippmeier JC, Apt KE, Delwiche CF. 2007. Plastid genes in a non-photosynthetic dinoflagellate. Protist. 158:105-117.
43. Sato S, Clough B, Coates L, Wilson RJ. 2004. Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist. 155:117-125.
44. Schott EJ, Pecher WT, Okafor F, Vasta GR. 2003. The protistan parasite Perkinsus marinus is resistant to selected reactive oxygen species. Exp Parasitol. 105:232-240.
45. Singh BK, Matthews BF. 1994. Molecular regulation of amino acid biosynthesis in plants. Amino Acids. 7:165-174.
46. Slamovits CH, Saldarriaga JF, Larocque A, Keeling PJ. 2007. The highly reduced and fragmented mitochondrial genome of the early-branching dinoflagellate Oxyrrhis marina shares characteristics with both apicomplexan and dinoflagellate mitochondrial genomes. J Mol Biol. 372:356-368.
47. Smith KS, Jakubzick C, Whittam TS, Ferry JG. 1999. Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci USA. 96:15184-15189.
48. Stelter K, El-Sayed NM, Seeber F. 2007. The expression of a plant-type ferredoxin redox system provides molecular evidence for a plastid in the early dinoflagellate Perkinsus marinus. Protist. 158:119-130.
49. Swofford DL. 2002. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, Sunderland (MA).
50. Teles-Grilo ML, Tato-Costa J, Duarte SM, Maia A, Casal G, Azevedo C. 2007. Is there a plastid in Perkinsus atlanticus (Phylum Perkinsozoa)? Eur J Protistol. 43:163-167.
51. Tonkin CJ, Roos DS, McFadden GI. 2006. N-terminal positively charged amino acids, but not their exact position, are important for apicoplast transit peptide fidelity in Toxoplasma gondii. Mol Biochem Parasitol. 150:192-200.
52. Tyler BM, Tripathy S, Zhang X, et al. (52 co-authors). 2006. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science. 313:1261-1266.
53. van Dooren GG, Schwartzbach SD, Osafune T, McFadden GI. 2001. Translocation of proteins across the multiple membranes of complex plastids. Biochim Biophys Acta. 1541:34-53.
54. van Dooren GG, Stimmler LM, McFadden GI. 2006. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol Rev. 30:596-630.
55. Varadharajan S, Sagar BK, Rangarajan PN, Padmanaban G. 2004. Localization of ferrochelatase in Plasmodium falciparum. Biochem J. 384:429-436.
56. Waller RF, Keeling PJ, Donald RG, Striepen B, Handman E, Lang-Unnasch N, Cowman AF, Besra GS, Roos DS, McFadden GI. 1998. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci USA. 95:12352-12357.
57. Waller RF, Patron NJ, Keeling PJ. 2006. Phylogenetic history of plastid-targeted proteins in the peridinin-containing dinoflagellate Heterocapsa triquetra. Int J Syst Evol Microbiol. 56:1439-1447.
58. Williams BA, Hirt RP. 2004. RACE and RAGE cloning in parasitic microbial eukaryotes. Methods Mol Biol. 270:151-172.
59. Williamson DH, Gardner MJ, Preiser P, Moore DJ, Rangachari K, Wilson RJ. 1994. The evolutionary origin of the 35 kb circular DNA of Plasmodium falciparum: new evidence supports a possible rhodophyte ancestry. Mol Gen Genet. 243:249-252.
60. Wilson RJMI, Denny PW, Preiser DJ, et al. (11 co-authors). 1996. Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol. 261:155-172.
61. Zhang H, Hou Y, Miranda L, Campbell DA, Sturm NR, Gaasterland T, Lin S. 2007. Spliced leader RNA trans-splicing in dinoflagellates. Proc Natl Acad Sci USA. 104:4618-4623.