Skip to main content
Log in

Evolution of early eukaryotic cells: genomes, proteomes, and compartments

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Eukaryotes arose from an endosymbiotic association of an α-proteobacterium-like organism (the ancestor of mitochondria) with a host cell (lacking mitochondria or plastids). Plants arose by the addition of a cyanobacterium-like endosymbiont (the ancestor of plastids) to the two-member association. Each member of the association brought a unique internal environment and a unique genome. Analyses of recently acquired genomic sequences with newly developed algorithms have revealed (a) that the number of endosymbiont genes that remain in eukaryotic cells—principally in the nucleus—is surprisingly large, (b) that protein products of a large number of genes (or their descendents) that entered the association in the genome of the host are now directed to an organelle derived from an endosymbiont, and (c) that protein products of genes traceable to endosymbiont genomes are directed to the nucleo-cytoplasmic compartment. Consideration of these remarkable findings has led to the present suggestion that contemporary eukaryotic cells evolved through continual chance relocation and testing of genes as well as combinations of gene products and biochemical processes in each unique cell compartment derived from a member of the eukaryotic association. Most of these events occurred during about 300 million years, or so, before contemporary forms of eukaryotic cells appear in the fossil record; they continue today.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abdallah F, Salamini F, Leister D (2000) A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis. Trends Plant Sci 5:141–142

    Article  PubMed  CAS  Google Scholar 

  • Adams KL, Daley DO, Whelan J, Palmer JD (2002) Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell 14:931–943

    Article  PubMed  CAS  Google Scholar 

  • Andersson SG, Dehio C (2000) Rickettsia prowazekii and Bartonella henselae: differences in the intracellular life styles revisited. Int J Med Microbiol 290:135–141

    PubMed  CAS  Google Scholar 

  • Andersson SG, Kurland CG (1999) Origins of mitochondria and hydrogenosomes. Curr Opin Microbiol 2:535–541

    Article  PubMed  CAS  Google Scholar 

  • Assali NE, Martin WF, Sommerville CC, Loiseaux-de Goër S (1991) Evolution of the Rubisco operon from prokaryotes to algae: structure and analysis of the rbcS gene of the brown alga Pylaiella littoralis. Plant Mol Biol 17:853–863

    Article  PubMed  CAS  Google Scholar 

  • Ayliffe MA, Timmis JN (1992) Plastid DNA sequence homologies in the tobacco nuclear genome. Mol Gen Genet 236:105–112

    PubMed  CAS  Google Scholar 

  • Bogorad L (1975) Evolution of organelles and eukaryotic genomes. Science 188:891–898

    Article  PubMed  CAS  Google Scholar 

  • Bogorad L (1982) In: Schiff JA (ed) On the origins of chloroplasts. Elsevier/North-Holland, Inc., New York, pp 277–279

    Google Scholar 

  • Bogorad L (1998) Discovery of chloroplast DNA, genomes and genes. In: Kung S-D, Yang S-F (eds) Discoveries in plant biology, vol II. World Scientific Publishing Co., Singapore, pp 15–43

    Google Scholar 

  • Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780

    Article  PubMed  CAS  Google Scholar 

  • Bubunenko MG, Schmidt J, Subramanian AR (1994) Protein substitution in chloroplast ribosome evolution: a eukaryotic cytosolic protein has replaced its organelle homologue (L23) in spinach. J Mol Biol 240:28–41

    Article  PubMed  CAS  Google Scholar 

  • Butterfield NJ (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386–404

    Article  Google Scholar 

  • Canback B, Andersson SG, Kurland CG (2002) The global phylogeny of glycolytic enzymes. Proc Natl Acad Sci USA 99:6097–6102

    Article  PubMed  CAS  Google Scholar 

  • Chan PH, Wildman SG (1972) Chloroplast DNA codes for the primary structure of the large subunit of fraction I protein. Biochim Biophys Acta 277:677–680

    PubMed  CAS  Google Scholar 

  • Consortium RCS (2003) In-depth view of structure, activity, and evolution of rice chromosome 10. Science 300:1566–1569

    Article  CAS  Google Scholar 

  • Danpure CJ (1995) How can the products of a single gene be localized to more than one intracellular compartment? Trends Cell Biol 5:230–238

    Article  PubMed  CAS  Google Scholar 

  • Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, Galperin MY, Koonin EV, Le Gall F, Makarova KS, Ostrowski M, Oztas S, Robert C, Rogozin IB, Scanlan DJ, De Marsac NT, Weissenbach J, Wincker P, Wolf YI, Hess WR (2003) Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc Natl Acad Sci USA 100:10020–10025

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, von Heijne G (2001) Prediction of organellar targeting signals. Biochim Biophys Acta 1541:114–119

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978–984

    Article  PubMed  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on the N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Farrelly F, Butow RA (1983) Rearranged mitochondrial genes in the yeast nuclear genome. Nature 301:296–301

    Article  PubMed  CAS  Google Scholar 

  • Ferro M, Salvi D, Brugiere S, Miras S, Kowalski S, Louwagie M, Garin J, Joyard J, Rolland N (2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Mol Cell Proteomics 2:325–345

    PubMed  CAS  Google Scholar 

  • Ferro M, Salvi D, Riviere-Rolland H, Vermat T, Seigneurin-Berny D, Grunwald D, Garin J, Joyard J, Rolland N (2002) Integral membrane proteins of the chloroplast envelope: identification and subcellular localization of new transporters. Proc Natl Acad Sci USA 99:11487–11492

    Article  PubMed  CAS  Google Scholar 

  • Forterre P, Philippe H (1999) Where is the root of the universal tree of life? Bioessays 21:871–879

    Article  PubMed  CAS  Google Scholar 

  • Gabriel K, Buchanan SK, Lithgow T (2001) The alpha and the beta: protein translocation across mitochondrial and plastid outer membranes. Trends Biochem Sci 26:36–40

    Article  PubMed  CAS  Google Scholar 

  • Gomez SM, Nishio JN, Faull KF, Whitelegge JP (2002) The chloroplast grana proteome defined by intact mass measurements from liquid chromatography mass spectrometry. Mol Cell Proteomics 1:46–59

    Article  PubMed  CAS  Google Scholar 

  • Gray MW, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biology 2:1018.1–1018.5

    Article  Google Scholar 

  • Hedtke B, Börner T, Weihe A (2000) One RNA polymerase serving two genomes. EMBO Rep 1:435–440

    Article  PubMed  CAS  Google Scholar 

  • Heldt H-W (1997) Plant biochemistry and molecular biology. Oxford University Press, Oxford, UK

    Google Scholar 

  • Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 422:72–76

    Article  PubMed  CAS  Google Scholar 

  • Ikeda TM, Gray MW (1999) Identification and characterization of T3/T7 bacteriophage-like RNA polymerase sequences in wheat. Plant Mol Biol 40:567–578

    Article  PubMed  CAS  Google Scholar 

  • Jansen R, Yu H, Greenbaum D, Kluger Y, Krogan NJ, Chung S, Emili A, Snyder M, Greenblatt JF, Gerstein M (2003) A bayesian networks approach for predicting protein-protein interactions from genomic data. Science 302:449–453

    Article  PubMed  CAS  Google Scholar 

  • Javaux EJ, Knoll AH, Walter MR (2001) Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412:66–69

    Article  PubMed  CAS  Google Scholar 

  • Jukes TH, Osawa S (1990) The genetic code in mitochondria and chloroplasts. Experientia 46:1117–1126

    Article  PubMed  CAS  Google Scholar 

  • Kabeya Y, Hashimoto K, Sato N (2002) Identification and characterization of two phage-type RNA polymerase cDNAs in the moss Physcomitrella patens: implication of recent evolution of nuclear-encoded RNA polymerase of plastids in plants. Plant Cell Physiol 43:245–255

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N., Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    Article  PubMed  CAS  Google Scholar 

  • Kaplan N, Colowick N (1955) Methods in enzymology. Academic Press, San Diego

    Google Scholar 

  • Karlberg EO, Andersson SG (2003) Mitochondrial gene history and mRNA localization: is there a correlation? Nat Rev Genet 4:391–397

    Article  PubMed  CAS  Google Scholar 

  • Karlberg O, Canback B, Kurland CG, Andersson SG (2000) The dual origin of the yeast mitochondrial proteome. Yeast 17:170–187

    Article  PubMed  CAS  Google Scholar 

  • Kawashima N, Wildman SG (1972) Studies on fraction I protein. IV. Mode of inheritance of primary structure in relation to whether chloroplast or nuclear DNA contains the code for a chloroplast protein. Biochim Biophys Acta 262:42–49

    PubMed  CAS  Google Scholar 

  • Kirk JTO, Tilney-Bassett RAE (1967) The plastids: their chemistry, structure, growth and inheritance. W. H. Freeman & Co., San Francisco

    Google Scholar 

  • Knoll AH (2003) Life on a young planet: the first three billion years of evolution of earth. Princeton University Press, Princeton

    Google Scholar 

  • Kumar A, Agarwal S, Heyman JA, Matson S, Heidtman M, Piccirillo S, Umansky L, Drawid A, Jansen R, Liu Y, Cheung KH, Miller P, Gerstein M, Roeder GS, Snyder M (2002) Subcellular localization of the yeast proteome. Genes Dev 16:707–719

    Article  PubMed  CAS  Google Scholar 

  • Lang BF, Burger G, O’Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW (1997) An ancestral mitochondrial DNA resembling a equatorial genome in miniature. Nature 387:493–497

    Article  PubMed  CAS  Google Scholar 

  • Lange T (1998) Molecular biology of gibberellin synthesis. Planta 204:409–419

    Article  PubMed  CAS  Google Scholar 

  • Lange BM, Rujan T, Martin W, Croteau R (2000) Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci USA 97:13172–13177

    Article  PubMed  CAS  Google Scholar 

  • Leustek T, Saito K (1999) Sulfate transport and assimilation in plants. Plant Physiol 120:637–644

    Article  PubMed  CAS  Google Scholar 

  • Lonosky PM, Zhang X, Honavar VG, Dobbs DL, Fu A, Rodermel SR (2004) A proteomic analysis of maize chloroplast biogenesis. Plant Physiol 134:560–574

    Article  PubMed  CAS  Google Scholar 

  • Marcotte EM, Xenarios I, van Der Bliek AM, Eisenberg D (2000) Localizing proteins in the cell from their phylogenetic profiles. Proc Natl Acad Sci USA 97:12115–12120

    Article  PubMed  CAS  Google Scholar 

  • Marechal-Drouard L, Weil JH, Dietrich A (1993) Transfer-RNAs and transfer-RNA genes in plants. Annu Rev Plant Physiol Plant Mol Biol 44:13–32

    CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (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

    Article  PubMed  CAS  Google Scholar 

  • Meeks JC, Elhai J, Thiel T, Potts M, Larimer F, Lamerdin J, Predki P, Atlas R (2001) An overview of the genome of Nostoc punctiforme, a multicellular, symbiotic cyanobacterium. Photosynth Res 70:85–106

    Article  PubMed  CAS  Google Scholar 

  • Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralbl 25:593–604 [English translation: Martin W, Kowallik KV (1999) Annotated English translation of Mereschkowsky’s 1905 paper ‘Über Natur und Ursprung der Chromatophoren im Pflanzenreiche’. Eur J Phycol 34:287–295

    Google Scholar 

  • Mets L, Bogorad L (1971) Mendelian and uniparental alterations in erythromycin binding by plastid ribosomes. Science 174:707–709

    Article  PubMed  CAS  Google Scholar 

  • Mets L, Bogorad L (1972) Altered chloroplast ribosomal proteins associated with erythromycin-resistant mutants in two genetic systems of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 69:3779–3783

    Article  PubMed  CAS  Google Scholar 

  • Obara K, Sumi K, Fukuda H (2002) The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol 43:697–705

    Article  PubMed  CAS  Google Scholar 

  • Peeters N, Small I (2001) Dual targeting to mitochondria and chloroplasts. Biochim Biophys Acta 1541:54–63

    Article  PubMed  CAS  Google Scholar 

  • Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12:319–341

    Article  PubMed  CAS  Google Scholar 

  • Penny D, Poole A (1999) The nature of the last universal common ancestor. Curr Opin Gen Dev 9:672–677

    Article  CAS  Google Scholar 

  • Prime TA, Sherrier DJ, Mahon P, Packman LC, Dupree P (2000) A proteomic analysis of organelles from Arabidopsis thaliana. Electrophoresis 21:3488–3499

    Article  PubMed  CAS  Google Scholar 

  • Reith M (1995) Molecular biology of rhodophyte and chromophyte plastids. Annu Rev Plant Physiol Plant Mol Biol 46:549–575

    Article  CAS  Google Scholar 

  • Reith M, Munholland J (1993) A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell 5:465–475

    Article  PubMed  CAS  Google Scholar 

  • Richter U, Kiessling J, Hedtke B, Decker E, Reski R, Börner T, Weihe A (2002) Two RpoT genes of Physcomitrella patens encode phage-type RNA polymerases with dual targeting to mitochondria and plastids. Gene 290:95–105

    Article  PubMed  CAS  Google Scholar 

  • Ris H, Plaut W (1962) Ultrastructure of DNA-containing areas in the chloroplast of Chlamydomonas. J Cell Biol 13:383–391

    Article  PubMed  CAS  Google Scholar 

  • Sapp J (1994) Evolution by association: a history of symbiosis. Oxford University Press, New York

    Google Scholar 

  • Schimper AFW (1883) Über die Entwicklung der Chlorophyllkörner und Farbkörper. Botani Zeit 41:105–112, 121–131, 137–146, 153–162

    Google Scholar 

  • Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP, Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277:8354–8365

    Article  PubMed  CAS  Google Scholar 

  • Scott NS, Timmis JN (1984) Homologies between nuclear and plastid DNA in spinach. Theor Appl Genet 67:279–288

    Article  CAS  Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

    PubMed  CAS  Google Scholar 

  • Sickmann A, Reinders J, Wagner Y, Joppich C, Zahedi R, Meyer HE, Schonfisch B, Perschil I, Chacinska A, Guiard B, Rehling P, Pfanner N, Meisinger C (2003) The proteome of Saccharomyeces cervisiae mitochondria. Proc Natl Acad Sci USA 100:13207–13212

    Article  PubMed  CAS  Google Scholar 

  • Small I, Wintz H, Akashi K, Mireau H (1998) Two birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol Biol 38:265–277

    Article  PubMed  CAS  Google Scholar 

  • Smith PMC, Mann AJ, Goggin DE, Atkins CA (1998) Air synthetase in cowpea nodules: a single gene product targeted to two organelles? Plant Mol Biol 36:811–820

    Article  PubMed  CAS  Google Scholar 

  • Stegemann S, Hartmann S, Ruf S, Bock R (2003) High-frequency gene transfer from the chloroplast genome to the nucleus. Proc Natl Acad Sci USA 100:8828–8833

    Article  PubMed  CAS  Google Scholar 

  • Stern DB, Lonsdale DM (1982) Mitochondrial and chloroplast genomes of maize have a 12–kilobase DNA sequence in common. Nature 299:698–702

    Article  PubMed  CAS  Google Scholar 

  • Stupar RM, Lilly JW, Town CD, Cheng Z, Kaul S, Buell CR, Jiang J (2001) Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-subunit repeats. Proc Natl Acad Sci USA 98:5099–5103

    Article  PubMed  CAS  Google Scholar 

  • Sugiura M (1998) The discovery of the complete sequence of tobacco and rice chloroplast genomes. In: Kung S-D, Yang S-F (eds) Discoveries in plant biology, vol II. World Scientific Publishing Co., Singapore, pp 45–60

    Google Scholar 

  • The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Thorsness PE, Fox TD (1990) Escape of DNA from mitochondria to the nucleus in Saccharomyces cerevisiae. Nature 346:376–379

    Article  PubMed  CAS  Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61

    Article  PubMed  CAS  Google Scholar 

  • van Wijk JK (2000) Proteomics of the chloroplast: experimentation and prediction. Trends Plant Sci 5:420–425

    Article  Google Scholar 

  • Watanabe N, Che FS, Iwano M, Takayama S, Yoshida S, Isogai A (2001) Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J Biol Chem 276:20474–20481

    Article  PubMed  CAS  Google Scholar 

  • Weeden NF (1981) Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 17:133–139

    Article  PubMed  CAS  Google Scholar 

  • Woese CR (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains archaea, bacteria, eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi K, Subramanian AR (2003) Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. PSRP-2 (U1A-type domains), PSRP-3α/β (ycf65 homologue) and PSRP-4 (Thx homologue). Eur J Biochem 270:190–205

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi K, Prieto S, Beligni MV, Haynes PA, McDonald WH, Yates JR, Mayfield SP (2002) Proteomic characterization of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: identification of a novel S1 Domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. Plant Cell 14:2957–2974

    Article  PubMed  CAS  Google Scholar 

  • Yang D, Oyaizu Y, Oyaizu H, Olsen GJ, Woese CR (1985) Mitochondrial origins. Proc Natl Acad Sci USA 82:4443–4447

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I am indebted to Colleen Cavanaugh and Andrew Knoll for discussions and very helpful comments on earlier versions of this article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lawrence Bogorad.

Additional information

Lawrence Bogorad—Deceased. This manuscript was completed by L. Bogorad just prior to his death in December, 2003. The insights contained within represent his last thoughts on endosymbiosis and organelle evolution—topics that formed a life-long intellectual passion.

For purposes of communication contact Steven R. Rodermel, Department of Genetics, Development and Cell Biology, Iowa State University, 457 Bessey Hall, Ames, IA 50011, USA, e-mail: rodermel@iastate.edu

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bogorad, L. Evolution of early eukaryotic cells: genomes, proteomes, and compartments. Photosynth Res 95, 11–21 (2008). https://doi.org/10.1007/s11120-007-9236-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9236-3

Keywords

Navigation