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The smallest known eukaryotic genomes encode a protein gene: towards an understanding of nucleomorph functions

Abstract

Cryptomonads are unicellular algae with plastids surrounded by four membranes. Between the two pairs of membranes lies a periplastidal compartment that harbours a DNA-containing organelle, termed the nucleomorph. The nucleomorph is the vestigial nucleus of a phototrophic, eukaryotic endosymbiont. Subcloning of parts of one nucleomorph chromosome revealed a gene coding for an Hsp70 protein. We demonstrate the expression of this nucleomorph protein-coding gene and present a model for protein transport from the host to the endosymbiont compartment.

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References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

  2. Chappell TG, Welch WJ, Schlossman DM, Palter KB, Schlesinger MJ, Rothman JE (1986) Uncoating ATPase is a member of the 70 kilodalton family of stress proteins. Cell 45:3–13

  3. Douglas SE, Murphy CA, Spencer DF, Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151

  4. Douglas SE (1992) A SecY-homologue is found in the plastid genome of Cryptomonas ϕ. FEBS Lett 298:93–96

  5. Engman DM, Fehr SC, Donelson JE (1992) Specific function domains of mitochondrial Hsp70s suggested by sequence comparison of the trypanosome and yeast proteins. Mol Biochem Parasitol 37:285–288

  6. Eschbach S, Hofmann CJB, Maier U-G, Sitte P, Hansmann P (1991) A eukaryotic genome of 660 kb: karyotype of nucleomorph and cell nucleus of the cryptomonad alga, Pyrenomonas salina. Nucleic Acids Res 19:1779–1781

  7. Georgopoulos C (1992) The emergence of the chaperone machines. Trends Biochem Sci 17:295–299

  8. Gething M-J, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45

  9. Gibbs SP (1979) The route of entry of cytoplasmatically synthesized proteins into chloroplasts of algae possessing chloroplast ER. J Cell Sci 35:253–266

  10. Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment. Comp Appl Biosciences 8:189–191

  11. Horst M, Kronidou NG, Schatz G (1993) Protein translocation: through the inner mitochondrial membrane. Curr Biol 3:175–177

  12. Hunt C, Morimoto RI (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of human hsp70. Proc Natl Acad Sci USA 82:6455–6459

  13. Igloi GL, Schiefermayr E (1993) Enzymatic addition of fluorescin- or biotin-riboUTP to oligonucleotides results in primers suitable for DNA sequencing and PCR. BioTechniques 15:486–497

  14. Maid U, Steinmüller R, Zetsche K (1992) Structure and expression of a plastid-encoded groEL homologous heat shock gene in a thermophilic red alga. Curr Genet 21:521–525

  15. Maier U-G, Hofmann CJB, Eschbach S, Wolters J, Igloi GL (1991) Demonstration of nucleomorph-encoded eukaryotic small subunit RNA in cryptomonads. Mol Gen Genet 230:155–160

  16. Maier U-G (1992) The four genomes of the alga Pyrenomonas salina (Cryptophyta). BioSystems 28:69–73

  17. Martin W, Lagrange T, Li Y-F, Bisanz-Seyer C, Mache R (1990) Hypothesis for the evolutionary origin of the chloroplast ribosomal protein L21 of spinach. Curr Genet 18:553–556

  18. McFadden GI (1990) Evidence that cyroptomonad chloroplasts evolved from photosynthetic endosymbionts. J Cell Sci 95:303–308

  19. McFadden GI (1993) Second-hand chloroplasts: evolution of cryptomonad algae. Adv Bot Res 19:190–239

  20. Müller FW, Igloi GL, Beck CF (1992) Structure of a gene encoding heatshock protein HSP70 from the unicellular alga Chlamydomonas reinhardtii. Gene 111:165–173

  21. Reusing SA, Maier U-G (1994) Phylogenetic analysis of the stress-70 protein family. J Mol Evol, in the press

  22. Rochester DE, Winer JA, Shah DM (1986) Structure and expression of maize genes encoding the major heat shock protein, hsp70. EMBO J 5:451–458

  23. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning; a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

  24. Sitte P (1987) Zellen in Zellen: Endocytobiose und die Folgen. In: Lust R (ed) Beobachtung, Experiment und Theorie in Naturwissenschaft and Medizin. Wiss. Verlagsges. Stuttgart, pp 431–446

  25. Sitte P (1993) Symbiogenetic evolution of complex cells and complex plastids. Europ J Protistol 29:131–143

  26. Valentin K (1993) SecA is plastid-encoded in a red alga: implications for the evolution of plastid genomes and the thylakoid protein import apparatus. Mol Gen Genet 235:147–152

  27. Wang S, Liu XQ (1991) The plastid genome of Cryptomonas ϕ encodes as hsp70-like protein, a histone-ike protein, and an acyl carrier protein. Proc Natl Sci USA 88:10783–10787

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Author information

Correspondence to U. -G. Maier.

Additional information

This paper is dedicated to Prof. Dr. Peter Sitte on the occasion of his 65th birthday

Communicated by H. Saedler

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Hofmann, C.J.B., Rensing, S.A., Häuber, M.M. et al. The smallest known eukaryotic genomes encode a protein gene: towards an understanding of nucleomorph functions. Molec. Gen. Genet. 243, 600–604 (1994). https://doi.org/10.1007/BF00284209

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Key words

  • Cryptomonads
  • Periplastidal
  • Hsp70
  • Transport