An Assessment of Vertical Inheritance versus Endosymbiont Transfer of Nucleus-encoded Genes for Mitochondrial Proteins Following Tertiary Endosymbiosis in Karlodinium micrum

Protist

Volumn 163, Issue 1, 2012, Pages 76-90

  Danne, Jillian C ^a   Gornik, Sebastian G ^a   Waller, Ross F ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Dinoflagellate; Endosymbiotic gene transfer; Haptophyte; Karlodinium; Mitochondrion; Plastid replacement.

Indexed keywords

MITOCHONDRIAL PROTEIN; PROTOZOAL PROTEIN;

ARTICLE; CELL NUCLEUS; CLASSIFICATION; DINOFLAGELLATE; GENETICS; HORIZONTAL GENE TRANSFER; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; PLASTID; RED ALGA; SYMBIOSIS;

CELL NUCLEUS; DINOFLAGELLIDA; GENE TRANSFER, HORIZONTAL; MITOCHONDRIAL PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASTIDS; PROTOZOAN PROTEINS; RHODOPHYTA; SYMBIOSIS;

DINOPHYCEAE; HAPTOPHYCEAE; KARLODINIUM; KARLODINIUM MICRUM; RHODOPHYTA;

EID: 82555194056     PISSN: 14344610     EISSN: 16180941     Source Type: Journal    
DOI: 10.1016/j.protis.2011.03.002     Document Type: Article

References (63)

1. Abdallah F., Salamini F., Leister D. A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci 2000, 5:141-142.
2. Adams K.L., Daley D.O., Qiu Y.L., Whelan J., Palmer J.D. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 2000, 408:354-357.
3. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
4. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
5. Andersson S.G., Zomorodipour A., Andersson J.O., Sicheritz-Ponten T., Alsmark U.C., Podowski R.M., Naslund A.K., Eriksson A.S., Winkler H.H., Kurland C.G. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 1998, 396:133-140.
6. Appleby C.A., Morton R.K. Crystalline cytochrome b2 and lactic dehydrogenase of yeast. Nature 1954, 173:749-752.
7. Bachvaroff T.R., Place A.R. From stop to start: tandem gene arrangement, copy number and trans-splicing sites in the dinoflagellate Amphidinium carterae. PLoS One 2008, 3:e2929.
8. Bannai H., Tamada Y., Maruyama O., Nakai K., Miyano S. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 2002, 18:298-305.
9. Bergholtz T., Daugbjerg N., Moestrup O., Fernández-Tejedor M. On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron micropscopy, nuclear encoded LSU rDNA and pigment composition. J Phycol 2006, 42:170-193.
10. Brennicke A., Grohmann L., Hiesel R., Knoop V., Schuster W. The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants. FEBS Lett 1993, 325:140-145.
11. Brooks G.A., Dubouchaud H., Brown M., Sicurello J.P., Butz C.E. Role of mitochondrial lactate dehydrogenase and lactate oxidation in the intracellular lactate shuttle. Proc Natl Acad Sci USA 1999, 96:1129-1134.
12. Bruno W.J., Socci N.D., Halpern A.L. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol Biol Evol 2000, 17:189-197.
13. Danne J.C., Waller R.F. Analysis of dinoflagellate mitochondrial protein sorting signals indicates a highly stable protein targeting system across eukaryotic diversity. J Mol Biol 2011, 408:643-653.
14. Daum G., Bohni P.C., Schatz G. Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 1982, 257:13028-13033.
15. Deusch O., Landan G., Roettger M., Gruenheit N., Kowallik K.V., Allen J.F., Martin W., Dagan T. Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. Mol Biol Evol 2008, 25:748-761.
16. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300:1005-1016.
17. Emelyanov V.V. Evolutionary relationship of Rickettsiae and mitochondria. FEBS Lett 2001, 501:11-18.
18. Eschbach S., Speth V., Hansmann P., Sitte P. Freeze-fracture study of the single membrane between host cell and endocytobiont in the dinoflagellates Glenodinium foliaceum and Peridinium balticum. J Phycol 1990, 26:324-328.
19. Gabaldon T., Huynen M.A. Reconstruction of the proto-mitochondrial metabolism. Science 2003, 301:609.
20. Gabaldon T., Huynen M.A. Shaping the mitochondrial proteome. Biochim Biophys Acta 2004, 1659:212-220.
21. Gabaldon T., Huynen M.A. From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLoS Comput Biol 2007, 3:e219.
22. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
23. Hackett J.D., Anderson D.M., Erdner D.L., Bhattacharya D. Dinoflagellates: A remarkable evolutionary experiment. Am J Bot 2004, 91:15523-15534.
24. Henze K., Martin W. How do mitochondrial genes get into the nucleus?. Trends Genet 2001, 17:383-387.
25. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
26. Imanian B., Keeling P.J. The dinoflagellates Durinskia baltica and Kryptoperidinium foliaceum retain functionally overlapping mitochondria from two evolutionarily distinct lineages. BMC Evol Biol 2007, 7:172.
27. Imanian B., Carpenter K.J., Keeling P.J. Mitochondrial genome of a tertiary endosymbiont retains genes for electron transport proteins. J Eukaryot Microbiol 2007, 54:146-153.
28. Ishida K., Green B.R. 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 2002, 99:9294-9299.
29. Jackson C.J., Norman J.E., Schnare M.N., Gray M.W., Keeling P.J., Waller R.F. Broad genomic and transcriptional analysis reveals a highly derived genome in dinoflagellate mitochondria. BMC Biol 2007, 5:41.
30. Karlberg O., Canback B., Kurland C.G., Andersson S.G. The dual origin of the yeast mitochondrial proteome. Yeast 2000, 17:170-187.
31. Keeling P.J. Diversity and evolutionary history of plastids and their hosts. Am J Bot 2004, 91:1481-1493.
32. Keeling P.J. The endosymbiotic origin, diversification and fate of plastids. Philos Trans R Soc Lond B Biol Sci 2010, 365:729-748.
33. Leander B.S., Keeling P.J. Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from Hsp90 and actin phylogenies. J Phycol 2004, 40:341-350.
34. Martin W., Herrmann R.G. Gene transfer from organelles to the nucleus: how much, what happens, and why?. Plant Physiol 1998, 118:9-17.
35. Martin W., Schnarrenberger C. The evolution of the Calvin cycle from prokaryotic to eukaryotic chromosomes: a case study of functional redundancy in ancient pathways through endosymbiosis. Curr Genet 1997, 32:1-18.
36. Martin W., Stoebe B., Goremykin V., Hapsmann S., Hasegawa M., Kowallik K.V. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 1998, 393:162-165.
37. Martin W., Rujan T., Richly E., Hansen A., Cornelsen S., Lins T., Leister D., Stoebe B., Hasegawa M., Penny D. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 2002, 99:12246-12251.
38. Minge M.A., Shalchian-Tabrizi K., Torresen O.K., Takishita K., Probert I., Inagaki Y., Klaveness D., Jakobsen K.S. A phylogenetic mosaic plastid proteome and unusual plastid-targeting signals in the green-colored dinoflagellate Lepidodinium chlorophorum. BMC Evol Biol 2010, 10:191.
39. Moreira D., Le Guyader H., Philippe H. The origin of red algae and the evolution of chloroplasts. Nature 2000, 405:69-72.
40. Nosenko T., Lidie K.L., Van Dolah F.M., Lindquist E., Cheng J.F., Bhattacharya D. Chimeric plastid proteome in the Florida "red tide" dinoflagellate Karenia brevis. Mol Biol Evol 2006, 23:2026-2038.
41. Patron N.J., Waller R.F. Transit peptide diversity and divergence: A global analysis of plastid targeting signals. Bioessays 2007, 29:1048-1058.
42. Patron N.J., Waller R.F., Keeling P.J. A tertiary plastid uses genes from two endosymbionts. J Mol Biol 2006, 357:1373-1382.
43. Patron N.J., Waller R.F., Archibald J.M., Keeling P.J. Complex protein targeting to dinoflagellate plastids. J Mol Biol 2005, 348:1015-1024.
44. Reyes-Prieto A., Hackett J.D., Soares M.B., Bonaldo M.F., Bhattacharya D. Cyanobacterial contribution to algal nuclear genomes is primarily limited to plastid functions. Curr Biol 2006, 16:2320-2325.
45. Schmidt H.A., von Haeseler A. Maximum-likelihood analysis using TREE-PUZZLE. Current Protocols in Bioinformatics 2003, Wiley, New York, vol. unit 6.6, pp 6.6.1-6.6.25. D. Baxevanis, R.D.M. Davison, G. Page, G.B. Stromo, L. Stein (Eds.).
46. Schnepf E., Elbrächter M. Dinophyte chloroplasts and phylogeny: A review. Grana 1999, 38:81-97.
47. Shalchian-Tabrizi K., Minge M.A., Cavalier-Smith T., Nedreklepp J.M., Klaveness D., Jakobsen K.S. Combined heat shock protein 90 and ribosomal RNA sequence phylogeny supports multiple replacements of dinoflagellate plastids. J Eukaryot Microbiol 2006, 53:217-224.
48. Takishita K., Ishida K., Maruyama T. Phylogeny of nuclear-encoded plastid-targeted GAPDH gene supports separate origins for the peridinin- and the fucoxanthin derivative-containing plastids of dinoflagellates. Protist 2004, 155:447-458.
49. Takishita K., Yamaguchi H., Maruyama T., Inagaki Y. A hypothesis for the evolution of nuclear-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase genes in "chromalveolate" members. PLoS One 2009, 4:e4737.
50. Tamura T., Shimada S., Horiguchi T. Galeidiniium rugatum gen. et sp. nov. (Dinophyceae), a new coccoid dinoflagellate with a diatom endosymbiont. J Phycol 2005, 41:658-671.
51. Taylor F.J.R. Implications and extensions of the serial endosymbiosis theory of the origin of eukaryotes. Taxon 1974, 23:229-258.
52. The Biology of Dinoflagellates 1987, Blackwell Scientific, Oxford. F.J.R. Taylor (Ed.).
53. Tengs T., Dahlberg O.J., Shalchian-Tabrizi K., Klaveness D., Rudi K., Delwiche C.F., Jakobsen K.S. Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin. Mol Biol Evol 2000, 17:718-729.
54. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882.
55. Timmis J.N., Ayliffe M.A., Huang C.Y., Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 2004, 5:123-135.
56. Waller R.F., Slamovits C.H., Keeling P.J. Lateral gene transfer of a multigene region from cyanobacteria to dinoflagellates resulting in a novel plastid-targeted fusion protein. Mol Biol Evol 2006, 23:1437-1443.
57. Waller R.F., Patron N.J., Keeling P.J. Phylogenetic history of plastid-targeted proteins in the peridinin-containing dinoflagellate Heterocapsa triquetra. Int J Syst Evol Microbiol 2006, 56:1439-1447.
58. Weeden N.F. Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 1981, 17:133-139.
59. Xia Z.X., Mathews F.S. Molecular structure of flavocytochrome b2 at 2.4 A resolution. J Mol Biol 1990, 212:837-863.
60. Yoon H.S., Hackett J.D., Bhattacharya D. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci USA 2002, 99:11724-11729.
61. Yoon H.S., Hackett J.D., Ciniglia C., Pinto G., Bhattacharya D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 2004, 21:809-818.
62. Yoon H.S., Hackett J.D., Van Dolah F.M., Nosenko T., Lidie K.L., Bhattacharya D. Tertiary endosymbiosis driven genome evolution in dinoflagellate algae. Mol Biol Evol 2005, 22:1299-1308.
63. Zhang H., Hou Y., Miranda L., Campbell D.A., Sturm N.R., Gaasterland T., Lin S. Spliced leader RNA trans-splicing in dinoflagellates. Proc Natl Acad Sci USA 2007, 104:4618-4623.