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. 2003 Nov 7;270(Suppl 2):S168–S171. doi: 10.1098/rsbl.2003.0058

Evidence for Golgi bodies in proposed 'Golgi-lacking' lineages.

Joel B Dacks 1, Lesley A M Davis 1, Asa M Sjögren 1, Jan O Andersson 1, Andrew J Roger 1, W Ford Doolittle 1
PMCID: PMC1809936  PMID: 14667372

Abstract

Golgi bodies are nearly ubiquitous in eukaryotic cells. The apparent lack of such structures in certain eukaryotic lineages might be taken to mean that these protists evolved prior to the acquisition of the Golgi, and it raises questions of how these organisms function in the absence of this crucial organelle. Here, we report gene sequences from five proposed 'Golgi-lacking' organisms (Giardia intestinalis, Spironucleus barkhanus, Entamoeba histolytica, Naegleria gruberi and Mastigamoeba balamuthi). BLAST and phylogenetic analyses show these genes to be homologous to those encoding components of the retromer, coatomer and adaptin complexes, all of which have Golgi-related functions in mammals and yeast. This is, to our knowledge, the first molecular evidence for Golgi bodies in two major eukaryotic lineages (the pelobionts and heteroloboseids). This substantiates the suggestion that there are no extant primitively 'Golgi-lacking' lineages, and that this apparatus was present in the last common eukaryotic ancestor, but has been altered beyond recognition several times.

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Selected References

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  1. Altschul S. F., Madden T. L., Schäffer 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 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bapteste Eric, Brinkmann Henner, Lee Jennifer A., Moore Dorothy V., Sensen Christoph W., Gordon Paul, Duruflé Laure, Gaasterland Terry, Lopez Philippe, Müller Miklós. The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1414–1419. doi: 10.1073/pnas.032662799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bullerwell C. E., Forget L., Lang B. F. Evolution of monoblepharidalean fungi based on complete mitochondrial genome sequences. Nucleic Acids Res. 2003 Mar 15;31(6):1614–1623. doi: 10.1093/nar/gkg264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cavalier-Smith T. Archamoebae: the ancestral eukaryotes? Biosystems. 1991;25(1-2):25–38. doi: 10.1016/0303-2647(91)90010-i. [DOI] [PubMed] [Google Scholar]
  5. Cavalier-Smith T. Eukaryotes with no mitochondria. 1987 Mar 26-Apr 1Nature. 326(6111):332–333. doi: 10.1038/326332a0. [DOI] [PubMed] [Google Scholar]
  6. Cavalier-Smith T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol. 2002 Mar;52(Pt 2):297–354. doi: 10.1099/00207713-52-2-297. [DOI] [PubMed] [Google Scholar]
  7. Dacks J. B., Doolittle W. F. Reconstructing/deconstructing the earliest eukaryotes: how comparative genomics can help. Cell. 2001 Nov 16;107(4):419–425. doi: 10.1016/s0092-8674(01)00584-0. [DOI] [PubMed] [Google Scholar]
  8. Dacks J. B., Silberman J. D., Simpson A. G., Moriya S., Kudo T., Ohkuma M., Redfield R. J. Oxymonads are closely related to the excavate taxon Trimastix. Mol Biol Evol. 2001 Jun;18(6):1034–1044. doi: 10.1093/oxfordjournals.molbev.a003875. [DOI] [PubMed] [Google Scholar]
  9. Ghosh S. K., Field J., Frisardi M., Rosenthal B., Mai Z., Rogers R., Samuelson J. Chitinase secretion by encysting Entamoeba invadens and transfected Entamoeba histolytica trophozoites: localization of secretory vesicles, endoplasmic reticulum, and Golgi apparatus. Infect Immun. 1999 Jun;67(6):3073–3081. doi: 10.1128/iai.67.6.3073-3081.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Katz L. A., Curtis E. A., Pfunder M., Landweber L. F. Characterization of novel sequences from distantly related taxa by walking PCR. Mol Phylogenet Evol. 2000 Feb;14(2):318–321. doi: 10.1006/mpev.1999.0695. [DOI] [PubMed] [Google Scholar]
  11. Keeling P. J. Foraminifera and Cercozoa are related in actin phylogeny: two orphans find a home? Mol Biol Evol. 2001 Aug;18(8):1551–1557. doi: 10.1093/oxfordjournals.molbev.a003941. [DOI] [PubMed] [Google Scholar]
  12. Keeling P. J., Luker M. A., Palmer J. D. Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol Biol Evol. 2000 Jan;17(1):23–31. doi: 10.1093/oxfordjournals.molbev.a026235. [DOI] [PubMed] [Google Scholar]
  13. Luján H. D., Marotta A., Mowatt M. R., Sciaky N., Lippincott-Schwartz J., Nash T. E. Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J Biol Chem. 1995 Mar 3;270(9):4612–4618. doi: 10.1074/jbc.270.9.4612. [DOI] [PubMed] [Google Scholar]
  14. Marti Matthias, Li Yajie, Schraner Elisabeth M., Wild Peter, Köhler Peter, Hehl Adrian B. The secretory apparatus of an ancient eukaryote: protein sorting to separate export pathways occurs before formation of transient Golgi-like compartments. Mol Biol Cell. 2003 Apr;14(4):1433–1447. doi: 10.1091/mbc.E02-08-0467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nothwehr S. F., Bruinsma P., Strawn L. A. Distinct domains within Vps35p mediate the retrieval of two different cargo proteins from the yeast prevacuolar/endosomal compartment. Mol Biol Cell. 1999 Apr;10(4):875–890. doi: 10.1091/mbc.10.4.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. O'Kelly C. J., Farmer M. A., Nerad T. A. Ultrastructure of Trimastix pyriformis (Klebs) Bernard et al.: similarities of Trimastix species with retortamonad and jakobid flagellates. Protist. 1999 Aug;150(2):149–162. doi: 10.1016/S1434-4610(99)70018-0. [DOI] [PubMed] [Google Scholar]
  17. Patterson DJ. The Diversity of Eukaryotes. Am Nat. 1999 Oct;154(S4):S96–S124. doi: 10.1086/303287. [DOI] [PubMed] [Google Scholar]
  18. Robinson M. S., Bonifacino J. S. Adaptor-related proteins. Curr Opin Cell Biol. 2001 Aug;13(4):444–453. doi: 10.1016/s0955-0674(00)00235-0. [DOI] [PubMed] [Google Scholar]
  19. Roger AJ. Reconstructing Early Events in Eukaryotic Evolution. Am Nat. 1999 Oct;154(S4):S146–S163. doi: 10.1086/303290. [DOI] [PubMed] [Google Scholar]
  20. Roger Andrew J., Silberman Jeffrey D. Cell evolution: mitochondria in hiding. Nature. 2002 Aug 22;418(6900):827–829. doi: 10.1038/418827a. [DOI] [PubMed] [Google Scholar]
  21. Simpson Alastair G. B., MacQuarrie Erin K., Roger Andrew J. Eukaryotic evolution: early origin of canonical introns. Nature. 2002 Sep 19;419(6904):270–270. doi: 10.1038/419270a. [DOI] [PubMed] [Google Scholar]
  22. Simpson Alastair G. B., Roger Andrew J. Eukaryotic evolution: getting to the root of the problem. Curr Biol. 2002 Oct 15;12(20):R691–R693. doi: 10.1016/s0960-9822(02)01207-1. [DOI] [PubMed] [Google Scholar]
  23. Simpson Alastair G. B., Roger Andrew J., Silberman Jeffrey D., Leipe Detlef D., Edgcomb Virginia P., Jermiin Lars S., Patterson David J., Sogin Mitchell L. Evolutionary history of "early-diverging" eukaryotes: the excavate taxon Carpediemonas is a close relative of Giardia. Mol Biol Evol. 2002 Oct;19(10):1782–1791. doi: 10.1093/oxfordjournals.molbev.a004000. [DOI] [PubMed] [Google Scholar]
  24. Sogin M. L. Early evolution and the origin of eukaryotes. Curr Opin Genet Dev. 1991 Dec;1(4):457–463. doi: 10.1016/s0959-437x(05)80192-3. [DOI] [PubMed] [Google Scholar]
  25. Springer S., Spang A., Schekman R. A primer on vesicle budding. Cell. 1999 Apr 16;97(2):145–148. doi: 10.1016/s0092-8674(00)80722-9. [DOI] [PubMed] [Google Scholar]
  26. Takvorian P. M., Cali A. Enzyme histochemical identification of the Golgi apparatus in the microsporidian, Glugea stephani. J Eukaryot Microbiol. 1994 Sep-Oct;41(5):63S–64S. [PubMed] [Google Scholar]
  27. 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 Dec 15;25(24):4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vorísek J. Functional morphology of the secretory pathway organelles in yeast. Microsc Res Tech. 2000 Dec 15;51(6):530–546. doi: 10.1002/1097-0029(20001215)51:6<530::AID-JEMT4>3.0.CO;2-Q. [DOI] [PubMed] [Google Scholar]

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