Skip to main content
SpringerLink
Log in

Mitochondria and chloroplasts as descendants of prokaryotes

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

In this article, I have attempted to present an up-to-date review of the salient features of mitochondria and chloroplasts which point to their one-time autonomy as independent organisms. The present-day organelles are contrasted with independent organisms, and the evolution of the present-day organelles from prokaryotes is discussed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aloni, Y., and Attardi, G. (1971). Expression of the mitochondrial genome in HeLa cells. IV. Titration of mitochondrial genes for 16s, 12s and 4s RNA. J. Mol. Biol. 55271.

    Google Scholar 

  • Altmann, R. (1890). Die Elementarorganismen und ihre Beziehungen zu den Zellen, Veit. Co., Leipzig.

    Google Scholar 

  • Attardi, G., and Ojala, D. (1971). Mitochondrial ribosomes in HeLa cells. Nature New Biol. 229133.

    Google Scholar 

  • Barnett, W. E., Brown, D. H., and Epler, J. L. (1967). Mitochondrial-specific aminoacyltRNA synthetases. Proc. Natl. Acad. Sci. 571775.

    Google Scholar 

  • Beattie, D. S. (1968). Studies on the biogenesis of mitochondrial protein components in rat liver slices. J. Biol. Chem. 2434027.

    Google Scholar 

  • Bell, P. R., Freywissling, A., and Mülethaler, K. (1966). Evidence for the discontinuity of plastids in the sexual reproduction of a plant. J. Ultrastruct. Res. 15108.

    Google Scholar 

  • Bernadi, G., and Timasheff, S. N. (1970). Optical rotary dispersion and circular dichroism, properties of yeast mitochondrial DNA's. J. Mol. Biol. 4843.

    Google Scholar 

  • Bisalputra, T., and Burton, H. (1969). The ultrastructure of the chloroplast of a brown alga. II. Association between chloroplast DNA and the photosynthetic lamellae. J. Ultrastruct. Res. 29224.

    Google Scholar 

  • Borst, P. (1970). Mitochondrial DNA: Structure, information content, replication and transcription. In “Control of Organelle Development”. Soc. Exptl. Biol. Symp. 24201.

    Google Scholar 

  • Brawerman, G. (1966). In. Goodwin, T. W. (ed.), The Biochemistry of Chloroplasts, Vol. 1, Academic Press, New York, p. 301.

    Google Scholar 

  • Brega, A., and Vesco, C. (1971). Ribonucleoprotein particles involved in HeLa mitochondrial protein synthesis. Nature New Biol. 229136.

    Google Scholar 

  • Buck, C. A., and Nass, M. M. K. (1969). Studies on mitochondrial tRNA from animal cells. A comparison of mitochondrial and cytoplasmic tRNA and animoacyl-tRNA synthetases. J. Mol. Biol. 4167.

    Google Scholar 

  • Burkard, G., Eclancher, B., and Weil, J. H. (1969). Presence of N-formylmethionyl transfer RNA in bean chloroplasts. FEBS Letters 4285.

    Google Scholar 

  • Dawid, I. B. (1970). The nature of mitochondrial RNA in oocytes of Xenopus laevis and its relation to mitochondrial DNA. In “Control of Organelle Development.” Soc. Exptl. Biol. Symp. 24227.

    Google Scholar 

  • Diacumakos, E. C., Garnjobst, L., and Tatum, E. L. (1965). A cytoplasmic character in Neurospora crassa. J. Cell Biol. 26427.

    Google Scholar 

  • Diers, L. (1970). Origin of chloroplasts: Cytological results and interpretation including some genetical aspects. In “Control of Organelle Development.” Soc. Exptl. Biol. Symp. 24129.

    Google Scholar 

  • Dupraw, E. J. (1968). Cell and Molecular Biology, Academic Press, New York and London.

    Google Scholar 

  • Dure, L. S., Epler, J. L., and Barnett, W. E. (1967). Sedimentation properties of mitochondrial and cytoplasmic ribosomal RNA's from Neurospora. Proc. Natl. Acad. Sci. 581883.

    Google Scholar 

  • Ellis, R. J. (1970). Further similarities between chloroplast and bacterial ribosomes. Planta (Berl.) 91329.

    Google Scholar 

  • Famintzin, A. (1907). Biol. Zentr. 27353.

    Google Scholar 

  • Firkin, F. C., and Linnane, A. W. (1969). Phylogenetic differences in the sensitivity of mitochondrial protein synthesizing systems to antibiotics. FEBS Letters 2 330.

    Google Scholar 

  • Flavell, R. B. (1971). The mitochondrion as a multifunctional organelle. Nature 230504.

    Google Scholar 

  • Fukuhara, H. (1970). Transcriptional origin of RNA in a mitochondrial fraction of yeast and its bearing on the problem of sequence homology between mitochondrial and nuclear DNA. Mol. Gen. Genet. 10758.

    Google Scholar 

  • Galper, J. B., and Darnell, J. E. (1969). The presence of N-formylmethionyl-tRNA in HeLa cell mitochondria. Biochem. Biophys. Res. Commun. 34205.

    Google Scholar 

  • Ganesan, A. T., and Lederberg, J. (1965). A cell-membrane bound fraction of bacterial DNA. Biochem. Biophys. Res. Commun. 18824.

    Google Scholar 

  • Gibson, I. (1970). The genetics of protozoan organelles. In “Control of Organelle Development.” Soc. Exptl. Biol. Symp. 24379.

    Google Scholar 

  • Gillham, N. W., Boynton, J. E., and Burkholder, B. (1970). Mutations altering chloroplast ribosome phenotype in Chlamydamonas I. Non-Mendelian mutations. Proc. Natl. Acad. Sci. 671026.

    Google Scholar 

  • Goldring, E. S., Grossman, L. T., Krupnick, D., Cryer, D. R., and Marmur, J. (1970). The petite mutation in yeast. Loss of mitochondrial deoxyribonucleic acid during induction of petites with ethidium bromide. J. Mol. Biol. 52323.

    Google Scholar 

  • Green, P. B. (1964). Cinematic observations on the growth and division of chloroplasts in Nitella. Am. J. Bot. 51334.

    Google Scholar 

  • Gualerzi, C., and Cammarano, P. (1969). Comparative electrophoretic studies on the protein of chloroplast and cytoplasmic ribosomes of spinach leaves. Biochim. Biophys. Acta 190170.

    Google Scholar 

  • Hawley, E. S., and Wagner, R. P. (1967). Synchronous mitochondrial division in Neurospora crassa. J. Cell Biol. 35489.

    Google Scholar 

  • Herrman, R. G., and Kowallik, K. U. (1970). Selective presentation of DNA regions and membranes in chloroplasts and mitochondria. J. Cell Biol. 45198.

    Google Scholar 

  • Hoober, J. K., and Blobel, G. (1969). Characterisation of the chloroplastic and cytoplasmic ribosomes of Chlamydamonas reinhardii. J. Mol. Biol. 41121.

    Google Scholar 

  • Housman, D., Jacobs-Lorena, M., Rajbhandary, U. L., and Lodish, F. (1970). Initiation of haemoglobin synthesis by methionyl tRNA. Nature 227913.

    Google Scholar 

  • Ingle, J., Possingham, J. V., Wells, R., Leaver, C. J., and Loening, U. E. (1970). The properties of chloroplast ribosomal RNA. In “Control of Organelle Development.” Soc. Exptl. Biol. Symp. 24303.

    Google Scholar 

  • Kadenbach, B. (1967). Synthesis of mitochondrial proteins. Demonstration of a transfer of proteins from microsomes into mitochondria. Biocheim. Biophys. Acta 134430.

    Google Scholar 

  • Kalf, G. F. (1964). Deoxyribonucleic acid in mitochondria and its role in protein synthesis. Biochemistry 31702.

    Google Scholar 

  • Kalf, G. F., and Ch'ih, J. J. (1968). Purification and properties of deoxyribonucleic acid polymerase from rat liver mitochondria. J. Biol. Chem. 2434904.

    Google Scholar 

  • Kalf, G. F., and Faust, A. S. (1969). The inner membrane of the rat liver mitochondrion as the site of incorporation of radioactively labelled precursors into nucleic acid and protein in vitro. Arch. Biochem. Biophys. 134103.

    Google Scholar 

  • Kirk, J. T. O., and Tilney-Bassett, R. A. E. (1967). The Plastids, Freeman and Co., London and San Francisco.

    Google Scholar 

  • Kirschner, R. H., Wolstenholme, D. R., and Gros, N. J. (1968). Replicating molecules of circular mitochondrial DNA. Proc. Natl. Acad. Sci. 601466.

    Google Scholar 

  • Knippers, R., and Stratlind, W. (1970). The DNA replicating capacity of isolated E. Coli cell wall-membrane complexes. Nature 226713.

    Google Scholar 

  • Kuntzel, H. (1969a). Proteins of mitochondrial and cytoplasmic ribosomes from Neurospora crassa. Nature 222142.

    Google Scholar 

  • Kuntzel, H. (1969b). Specificity of mitochondrial and cytoplasmic ribosomes from Neurospora crassa in polyU- dependent cell free systems. FEBS Letters 4140.

    Google Scholar 

  • Kuntzel, H., and Noll, H. (1967). Mitochondrial and cytoplasmic polysomes from Neurospora crassa. Nature 2151340.

    Google Scholar 

  • Kuntzel, H., and Schäfer, K. P. (1971). Mitochondrial RNA polymerase from Neurospora crassa. Nature 231265.

    Google Scholar 

  • Lizardi, P. M., and Luck, D. J. L. (1971). Absence of a 5s RNA component in the mitochondrial ribosomes of Neurospora crassa. Nature New Biol. 229140.

    Google Scholar 

  • Loening, U. E., and Ingle, J. (1967). Diversity of RNA components in green plant tissues. Nature 215363.

    Google Scholar 

  • Luck, D. J. L. (1963). Genesis of mitochondria in Neurospra crassa. Proc. Natl. Acad. Sci. 49233.

    Google Scholar 

  • Makino, F., and Tsuzuki, J. (1971). Absence of histone in the blue-green alga Anabaena cylindrica. Nature 231446.

    Google Scholar 

  • Manning, J. E., Wolstenholme, D. R., Ryan, R. S., Hunter, J. A., and Richards, B. C. (1971). Circular chloroplast DNA from Euglena gracilis. Proc. Natl. Acad. Sci. 681169.

    Google Scholar 

  • Manton, I. (1959). Electron microscopical observations on a very small flagellate: The problem of Chromulina pusilla Butcher. J. Marine Biol. Ass. U.K. 38319.

    Google Scholar 

  • Manton, I. (1961). Some problems of mitochondrial growth. J. Exptl. Bot. 12421.

    Google Scholar 

  • Margulis, L. (1970). The Origin of Eucaryotic cells, Yale University Press, New Haven.

    Google Scholar 

  • Mereschowsky, C. (1910). Biol. Zentr. 30278, 321, 353.

    Google Scholar 

  • Meyer, R. R., and Simpson, M. V. (1968). DNA biosynthesis in mitochondria: Partial purification of a distinct DNA polymerase from isolated rat liver mitochondria. Proc. Natl. Acad. Sci. 61130.

    Google Scholar 

  • Mühlethaler, K., and Bell, P. R. (1962). Untersuchungen über die Kontinuität von Plastiden und Mitochondrien un der Eizelle von Pteridium aquilinum (L) Kuhn. Naturwissenschaften 4963.

    Google Scholar 

  • Naegeli, C. (1846). Z. Bot. 394.

    Google Scholar 

  • Nagley, P., and Linnane, A. W. (1970). Mitochondrial DNA deficient mutants of yeast. Biochem. Biophys. Res. Commun. 5989.

    Google Scholar 

  • Nass, M. M. K., Nass, S., and Afzelius, B. A. (1965). The general occurrence of mitochondrial DNA. Exptl. Cell Res. 37516.

    Google Scholar 

  • Nass, S. (1969). Similarities of bacteria and mitochondria. Internat. Rev. Cytol. 2555.

    Google Scholar 

  • Nass, S., and Nass, M. M. K. (1963). An electron histochemical study of mitochondrial fibrous inclusions. J. Roy. Microscop. Soc. 81209.

    Google Scholar 

  • Needleman, S. B., and Blair, T. T. (1969). Homology of Pseudomonas cytochrome-c 551 with eucaryotic c-cytochromes. Proc. Natl. Acad. Sci. 631227.

    Google Scholar 

  • Neubert, D., Helge, H., and Merker, H. J. (1965). Zum Nachweis einer RNS-polymerase activitat in Mitochondrien tierischer Zellen. Biochem. Z. 34344.

    Google Scholar 

  • Parsons, J. A., and Rustad, R. C. (1968). The distribution of DNA among dividing mitochondria of Tetrahymena pyriformis. J. Cell Biol. 37683.

    Google Scholar 

  • Perlman, P. S., and Mahler, H. R. (1970). Formation of yeast mitochondria. Biochemical properties of mitochondria isolated from a cytoplasmic mutant. Bioenergetics 1113.

    Google Scholar 

  • Piko, L., Blair, D. G., Tyler, A., and Vinograd, J., (1968). Cytoplasmic DNA in the unfertilised sea urchin egg—physical properties of circular mitochondrial DNA and the occurrence of catenated forms. Proc. Natl. Acad. Sci. 59838.

    Google Scholar 

  • Plattner, H., Salpeter, M. M., Satzgaber, J., and Schatz, G. (1970). Primitochondria of anaerobically grown yeast. IV. Conversion into respiring mitochondria. Proc. Natl. Acad. Sci. 661252.

    Google Scholar 

  • Portier, P. (1918). Les Symbiotes, Masson, Paris.

    Google Scholar 

  • Possingham, J. V., and Saurer, W. (1969). Changes in chloroplast number per cell during leaf development in spinach. Planta (Berl.) 86186.

    Google Scholar 

  • Pringsheim, E. G., and Pringsheim, O. (1952). Experimental elimination of chromatophores and eye spot in Euglena gracilis. New Phytol. 5165.

    Google Scholar 

  • Raven, P. H. (1970). A multiple origin for plastids and mitochondria. Science 169641.

    Google Scholar 

  • Ray, D. S., and Hanawalt, P. C. (1965). Satellite DNA components in Euglena gracilis cells lacking chloroplasts. J. Mol. Biol. 11760.

    Google Scholar 

  • Reich, E., and Luck, D. J. L. (1966). Replication and inheritance of mitochondrial DNA. Proc. Natl. Acad. Sci. 551600.

    Google Scholar 

  • Richter, D., and Lipmann, F. (1970). Separation of mitochondrial and cytoplasmic peptide chain elongation factors from yeast. Biochemistry 95065.

    Google Scholar 

  • Ridley, S. M., and Leech, R. M. (1970). Division of chloroplasts in an artificial environment. Nature 227463.

    Google Scholar 

  • Rifkin, M. R., Wood, D. D., and Luck, D. J. L. (1967). Ribosomal RNA and ribosomes from mitochondria of Neurospora crassa. Proc. Natl. Acad. Sci. 581025.

    Google Scholar 

  • Ris, H., and Plaut, W. (1962). Ultrastructure of DNA-containing areas in the chloroplasts of Chlamydamonas. J. Cell. Biol. 13383.

    Google Scholar 

  • Roodyn, D. B., and Wilkie, D. (1968). The Biogenesis of Mitochondria, Methuen and Co., London.

    Google Scholar 

  • Rouslin, W., and Schatz, G. (1969). Interdependence between promitochondrial and cytoplasmic protein synthesis during respiratory adaptation in baker's yeast. Biochem. Biophys. Res. Commun. 371002.

    Google Scholar 

  • Sackin, M. J. (1971). Crossassociation: A method of comparing protein sequences. Biochem. Genet. 5287.

    Google Scholar 

  • Sagan, L. (1967). On the origin of mitosing cells. J. Theoret. Biol. 14225.

    Google Scholar 

  • Sager, R. (1970). Genetic studies of chloroplast DNA in Chlamydamonas. Soc. Exptl. Biol. Symp. 24401.

    Google Scholar 

  • Schmerling, Z. G. (1969). The effect of rifamycin on RNA synthesis in rat liver mitochondria. Biochem. Biophys. Res. Commun. 37965.

    Google Scholar 

  • Schnaitman, C. A. (1969). Comparison of rat liver mitochondrial and microsomal membrane proteins. Proc. Natl. Acad. Sci. 63412.

    Google Scholar 

  • Schotz, F. (1970). Effects of the disharmony between genome and plastome on the differentiation of the thylakoid system of Oenothera. Soc. Exptl. Biol. Symp. 2439.

    Google Scholar 

  • Schwartz, J. H., Meyer, R., Eisenstadt, J. M., and Brawerman, G. (1967). Involvement of N-formylmethionine in initiation of protein synthesis in cell-free extracts of Euglena gracilis. J. Mol. Biol. 25571.

    Google Scholar 

  • Smith, A. E., and Marcker, K. A. (1968). N-formylmethionyl transfer RNA in mitochondria from yeast and rat liver. J. Mol. Biol. 38241.

    Google Scholar 

  • Smith, D., Tauro, P., Schweizer, E., and Halvorson, H. O. (1968). The replication of mitochondrial DNA during the cell cycle in Saccheromyces lactis. Proc. Natl. Acad. Sci. 60936.

    Google Scholar 

  • South, D. J., and Mahler, H. R. (1968). RNA synthesis in yeast mitochondria: A derepressible activity. Nature 2181226.

    Google Scholar 

  • Spencer, D., and Whitfield, P. R. (1967). DNA synthesis in isolated chloroplasts. Biochem. Biophys. Res. Commun. 28538.

    Google Scholar 

  • Spencer, D., and Wildman, S. G. (1964). The incorporation of amino acids into protein by cell-free extracts from tobacco leaves. Biochemistry 3954.

    Google Scholar 

  • Stainer, R. Y., and van Niel, C. B. (1962). The concept of a bacterium. Arch. Mikrobiol. 4217.

    Google Scholar 

  • Stegeman, W. J., Cooper, C. S., and Avers, C. J. (1970). Physical characterisation of ribosomes from purified mitochondria of yeast. Biochem. Biophys. Res. Commun. 3969.

    Google Scholar 

  • Stutz, E., and Noll, H. (1967). Characteristics of cytoplasmic and chloroplast polysomes in plants: Evidence for three classes of r-RNA in nature. Proc. Natl. Acad. Sci. 57774.

    Google Scholar 

  • Surzycki, S. J. (1969). Genetic functions of the chloroplast of Chlamydamonas reinhardii: Effect of rifampin on chloroplast DNA-dependent RNA polymerase. Proc. Natl. Acad. Sci. 631327.

    Google Scholar 

  • Suyama, Y. (1967). The origins of mitochondrial ribonucleic acids in Tetrahymena pyriformis. Biochemistry 62829.

    Google Scholar 

  • Taylor, D. L. (1970). Chloroplasts as symbiotic organelles. Internat. Rev. Cytol. 2729.

    Google Scholar 

  • Tewari, K. K., and Wildman, S. G. (1970). Information content in the chloroplast DNA. In “Control of Organelle Development.” Soc. Exptl. Biol. Symp. 24147.

    Google Scholar 

  • Tewari, K. K., Votsch, W., Mahler, H. R., and Mackler, B. (1966). Biochemical correlates of respiratory deficiency. VI. Mitochondrial DNA. J. Mol. Biol. 20453.

    Google Scholar 

  • Tsai, M. J., Michaelis, G., and Criddle, R. S. (1971). DNA-dependent RNA polymerase from yeast mitochondria. Proc. Natl. Acad. Sci. 68473.

    Google Scholar 

  • Vogel, H. J. (1965). Lysine biosynthesis and evolution. In Bryson, V., and Vogel, H. J. (eds.), Evolving Genes and Proteins, Academic Press, New York, p. 25.

    Google Scholar 

  • Wells, R., and Ingle, J. (1970). The constancy of the buoyant density of chloroplast and mitochondrial deoxyribonucleic acids in a range of higher plants. Plant Physiol. 46178.

    Google Scholar 

  • Wintersberger, V., and Wintersberger, E. (1970). Studies of deoxyribonucleic acid polymerases from yeast.2. Partial purification and characterisation of mitochondrial DNA polymerase from wild type and respiration deficient yeast cells. Europ. J. Biochem. 1320.

    Google Scholar 

  • Wolstenholme, D. R., and Gros, N. J. (1968). The form and size of mitochondrial DNA of the red bean Phaseolus vulgaris. Proc. Natl. Acad. Sci. 61245.

    Google Scholar 

  • Wood, D. B., and Luck, D. J. L. (1969). Hybridisation of mitochondrial ribosomal RNA. J. Mol. Biol. 41211.

    Google Scholar 

  • Woodward, D. O., Edwards, D. L., and Flavell, R. B. (1970). Nucleocytoplasmic interactions in the control of mitochondrial structure and function in Neurospora. In “Control of Organelle Development.” Soc. Exptl. Biol. Symp. 2455.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Breeding Institute, Trumpington, Cambridge, England

    Richard Flavell

Authors
  1. Richard Flavell
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Flavell, R. Mitochondria and chloroplasts as descendants of prokaryotes. Biochem Genet 6, 275–291 (1972). https://doi.org/10.1007/BF00486121

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00486121

Keywords

Search

Navigation