Summary
In the origin of the mitochondrion and plastid, gene transfer from the ancestral endosymbiont to the host was proposed to be a crucial event. For this genic integration to proceed, products of transferred genes had to return to and enter the endosymbionts. The limiting event was the crossing of the barrier presented by the two semipermeable membranes bounding the proto-organelle. In this paper it is suggested that spontaneous transport allowed transferred gene encoded proteins to enter the endosymbionts before receptors evolved. The effects of these events, including the degeneration of the endosymbiont genome, are discussed. Although the presumed gene transfer had profound effects on the metabolic relationships between host and endosymbionts it probably cannot account for all examples of organelle/cytoplasmic isozyme pairs or the absence of amino acid synthetic enzymes in animal cells.
Similar content being viewed by others
References
Berry DR (1975) The environmental control of the physiology of filamentous fungi. In: Smith JE, Berry DR (eds) The Filamentous Fungi, vol 1. Industrial Mycology, Edward Arnold, London, p 16
Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nacent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67:835–851
Bogorad L (1975) Evolution of organelles and eukaryotic genomes. Science 188:891–898
Borst P, Grivell LA (1978) The mitochondrial genome of yeast. Cell 15:705–723
Borst P, Grivell LA (1981a) One gene's intron is another gene's exon. Nature 289:439–440
Bos JL, Heyting C, Borst P, Arnberg AC, Van Bruggen EFJ (1978) An insert in the single gene for the large ribosomal RNA in yeast mitochondrial DNA. Nature 275:336–337
Bretscher MS (1973) Membrane structure: some general principles. Science 181:622–629
Burnett JH (1976) Fundamentals of Mycology, 2nd edn. Edward Arnold, London
Cavalier-Smith T (1975) The origin of nuclei and eukaryotic cells. Nature 256:463–468
Chua N, Schmidt GW (1979) Transport of proteins into mitochondria and chloroplasts. J Cell Biol 81:461–483
Drummond M (1979) Crown gall disease. Nature 281:343–347
Engelman DM, Steitz TA (1981) The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell 23:411–422
Fox GE, Stackebrandt E, Hespell RB, Gibson J, Maniloff J, Dyer TA, Wolfe RS, Balch WE, Tanner RS, Magrum LJ, Zablen LB, Blakemore R, Gupta R, Bonnen L, Lewis BJ, Stahl DA, Luehrsen KR, Chen KN, Woese CR (1980) The phylogeny of prokaryotes. Science 209:457–463
Fox TD (1981) More surprises from mitochondria. Nature 292: 109–110
Gaber RF, Leonard TJ (1981) Unilateral internuclear gene transfer and cell differentiation inSchizophyllum. Nature 291: 342–344
Harington A, Thornley A (1980) Endosymbiosis, gene transfer and the mitochondrial genetic code. S Afr J Sci 76:162–165
Kagamiyama H, Sakakibara R, Wada H, Tanase S, Morino Y (1977) The complete amino acid sequence of mitochondrial aspartate aminotransferase from pig heart. J Biochem 82: 291–294
Lazowska J, Jacq C, Slonimsky PP (1980) Sequence of introns and flanking exons in wildtype andbox3 mutants of cytochrome b reveals an interlaced splicing protein coded by an intron. Cell 22:333–348
Lehninger AL (1975) Biochemistry, 2nd edn. Worth, New York
McIntosh L, Poulsen C, Bogorad L (1980) Chloroplast gene sequence for the large subunit of ribulose bisphosphatecar-boxylase of maize. Nature 288:556–560
Margulis L (1976) Genetic and evolutionary consequences of symbiosis. Exp Parasit Rev 29:277–349
Margulis L (1981) Symbiosis in Cell Evolution. Freeman and Company, San Francisco
Martin JP, Fridovich I (1981) Evidence for a natural gene transfer from the Ponyfish to its bioluminecent bacterial symbiontPhotobacter leiognathi. J Biol Chem 265:6080–6089
Mulligan RC, Berg P (1980) Expression of a bacterial gene in mammalian cells. Science 209:1422–1427
Neupert W, Schatz G (1981) How proteins are transported into mitochondria. TIBS 6:1–4
News and Views (1980) Maverick mitochondria. Nature 287: 9–10
Raff RA, Mahler HR (1972) The non symbiotic origin of mitochondria. Science 177:575–582
Raff RA, Mahler HR (1975) The symbiont that never was: An enquiry into the evolutionary origin of the mitochondrion. In: Jennings DH, Lee DL (eds) Symposia of the Society for Experimental Biology, vol 29. Cambridge University Press, Cambridge, p 41
Reijnders L (1975) The origin of mitochondria. J Mol Evol 5: 167–176
Rochaix JD, Malnoe P (1978) Anatomy of the chloroplast ribosomal DNA ofChlamydomonas reinhardii. Cell 15:661–670
Schatz G (1979) How mitochondria import proteins from the cytoplasm. FEBS Lett 103:203–211
Schwartz RM, Dayhoff MO (1978) Origins of prokaryotes, eukaryotes, mitochondria and chloroplasts. Science 199: 395–403
Smith DC (1979) From extracellular to intracellular: the establishment of symbiosis. Proc R Soc Lond B 204:115–130
Sonderegger P, Christen P (1978) Comparison of the evolution rates of cytosolic and mitochondrial aspartate aminotransferase. Nature 275:157–159
Steinman HM, Hill RL (1973) Sequence homologies among bacterial and mitochondrial superoxide dismutases. Proc Natl Acad Sci USA 70:3725–3729
Taylor FJR (1979) Symbionticism revisited: a discussion of the evolutionary impact of intracellular symbioses. Proc R Soc Lond B 204:267–286
Thornley AL, Harington A (1981) Diploidy and sex as the selective advantages for retaining genes transferred from mitochondrial and plastid ancestors in the nuclear genome. J Theor Biol 91:515–523
Weeden NF (1981) Genetic and biochemical implications of the endosymbiotic origin of the chloroplast. J Mol Evol 17: 133–139
Whatley JM, John P, Whatley FR (1979) From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc R Soc Lond B 204:165–187
Wickner W (1976) Asymmetric orientation of phage M13 coat protein inEsherichia coli cytoplasmic membranes and in synthetic lipid vesicles. Proc Natl Acad Sci 73:1159–1163
Woese CR (1977) Endosymbionts and mitochondrial origins. J Mol Evol 10:93–96
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Harington, A., Thornley, A.L. Biochemical and genetic consequences of gene transfer from endosymbiont to host genome. J Mol Evol 18, 287–292 (1982). https://doi.org/10.1007/BF01733893
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF01733893