Supernumerary DNAs in Plant Mitochondria

  • R. R. Sederoff
  • C. S. LevingsIII
Part of the Plant Gene Research book series (GENE)


Mitochondria DNA (mtDNA) of higher plants is characterized by exceptional diversity. Measurements of mitochondrial genome sizes have shown a bewildering array of variation both in genome size and in the presence of supernumerary DNAs that are smaller than the complete genome. Mitochondrial genomes in higher plants are the largest known and vary over an order of magnitude from about 200 kb to 2400 kb (Table 1). This result is in striking contrast to the conservation of mitochondrial genome size and structure characteristic of animal mitochondrial genomes. Virtually all animal mitochondrial genomes are between 15kb and 19kb (Wallace, 1982). Fungi also show great divergence in mitochondrial genome size, ranging from about 17kb to 108kb (Clark-Walker and Sriprakash, 1982; Wallace, 1982; Sederoff, 1984). In several protozoa, genome sizes are similar to those of fungi. However, some protozoa show extreme structural variation, particularly in kinetoplast DNA (Borst et al, 1981).


Mitochondrial Genome Cytoplasmic Male Sterility Circular Molecule Normal Maize Nuclear Background 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ariga, H., and Shimojo, H., 1977: Initiation and termination sites of adenovirus 2 DNA replication. Virology 78, 415–424.PubMedCrossRefGoogle Scholar
  2. Augustyniak, H., Borsuk, P., Hirschler, I., Stepien, P. P., and Bartnik, E., 1983: Mitochondrial DNA from lupine: restriction analysis and cloning of fragments coding for tRNA. Gene 22, 69–74.PubMedCrossRefGoogle Scholar
  3. Belliard, G., Vedel, F., and Pelletier, G., 1979: Mitochondrial recombination in cytoplasmic hybrids of Nicotiana tabacum by protoplast fusion. Nature (London) 281, 401–403.CrossRefGoogle Scholar
  4. Bendich, A. J., 1982: Plant mitochondrial DNA: The last frontier. In: Slonimski, P., Borst, P., and Attardi, G. (eds.). Mitochondrial Genes, pp. 477–481. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.Google Scholar
  5. Borck, K. S., and Walbot, V., 1982: Comparison of the restriction endonuclease digestion patterns of mitochondrial DNA from normal and male-sterile cytoplasms of Zea Mays L. Genetics 102, 109–128.PubMedGoogle Scholar
  6. Borst, P., Hoeijmakers, J. H. J., and Hajduk, S. L., 1981: Structure, function and evolution of kinetoplast DNA. Parasitology 82, 81–93.CrossRefGoogle Scholar
  7. Braun, C. J., Sisco, P. H., Sederoff, R. R., and Levings, C. S., III: Nucleotide sequences of inverted repeats and flanking regions of five integrated segments of plasmid-like DNAs from maize mitochondria. Manuscript in preparation.Google Scholar
  8. Brennicke, A., 1980: Mitochondrial DNA from Oenothera berteriana. Plant Physiol. 65, 1207–1210.PubMedCrossRefGoogle Scholar
  9. Brennicke, A, and Blanz, P., 1982: Circular mitochondrial DNA species from Oenothera with unique sequences. Mol. Gen. Genet. 187, 461–466.CrossRefGoogle Scholar
  10. Brown, W. M., Prager, E. M., Wang, A., and Wilson, A. C., 1982: Mitochondrial DNA sequences of primates: Tempo and mode of evolution. J. Mol. Evol. 18,225–239.PubMedCrossRefGoogle Scholar
  11. Carusi, E. A., 1977: Evidence for blocked 5’-termini in human adenovirus DNA. Virology 76, 380–394.PubMedCrossRefGoogle Scholar
  12. Chao, S., Sederoff, R. R, and Levings, C. S. III, 1984: Nucleotide sequence and evolution of the 18 Sribosomal RNA gene in maize mitochondria. Nucleic Acids Res.: In press.Google Scholar
  13. Conde, M. F., Pring, D. R, and Levings, C. S., III, 1979: Maternal inheritance of organelle DNA’s in Zea mays — Zea perennis reciprocal crosses. J. of Heredity 70, 2–4.Google Scholar
  14. Clark-Walker, G. D., and Sriprakash, K. S., 1982: Size diversity and sequence rearrangements in mitochondrial DNAs from yeast. In: Slonimski, P., Borst, P., and Attardi, G. (eds.). Mitochondrial Genes, pp. 349–354. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.Google Scholar
  15. Dale, R. M. K., 1981: Sequence homology among different size classes of plant mtDNAs. Proc. Natl. Acad. Sci., U.S.A. 78, 4454–4457.CrossRefGoogle Scholar
  16. Dale, R. M. K., 1982: Structure of plant mitochondrial DNAs. In: Slonimski, P., Borst, P., and Attardi, G. (eds.). Mitochondrial Genes, pp. 471–476. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.Google Scholar
  17. Dixon, L. K., and Leaver, C. J., 1982: Mitochondrial gene expression and cytoplasmic male sterility in sorghum. Plant Mol. Biol. 1, 89–102.CrossRefGoogle Scholar
  18. Fontarnau, A., and Hernandez-Yago, J., 1982: Characterization of mitochondrial DNA in Citrus. Plant Physiol. 70, 1678–1682.PubMedCrossRefGoogle Scholar
  19. Forde, B. G., and Leaver, C. J., 1980: Nuclear and cytoplasmic genes controlling synthesis of variant mitochondrial polypeptides in male-sterile maize. Proc. Natl. Acad. Sci., U.S.A. 77, 418–422.PubMedCrossRefGoogle Scholar
  20. Freeling, M., 1984: Plant transposable elements and insertion sequences. Ann. Rev. Plant Physiol. 35, 277–298.CrossRefGoogle Scholar
  21. Goblet, J.-P., Boutry, M., Due, G., Briquet, M., 1983: Mitochondrial plasmid-like molecules in fertile and sterile Vicia faba L. Plant Mol. Biol. 2, 305–309.CrossRefGoogle Scholar
  22. Harding, N. E., Ito, J., and David, G. S., 1978: Identification of the protein firmly bound to the ends of bacteriophage 0 29 DNA. Virology 84, 279–292.PubMedCrossRefGoogle Scholar
  23. Harding, N. E., and Ito, J., 1980: DNA replication of bacteriophage 0 29: Characterization of the intermediates and location of the termini of replication. J. of Virology 104, 323–338.CrossRefGoogle Scholar
  24. Hobom, G., Grosschedl, R., Lusky, M., Scherer, G., Schwarz, E., and Kossel, H., 1978: Functional analysis of the replicator structure of lambdoid bacteriophage DNAs. Cold Spring Harbor Symposia on Quantitative Biology 43, 165–178.Google Scholar
  25. Inciarte, M. R, Salas, M., and Sogo, J. M., 1980: Structure of replicating DNA molecules of Bacillus subtilis bacteriophage. J. of Virology 4, 187–199.Google Scholar
  26. Ito, J., 1978: Bacteriophage Ø 29 terminal protein: Its association with the 5’ termini of the Ø 29 genome. Virology 28, 895–904.Google Scholar
  27. Kemble, R. J., and Bedbrook, J. R., 1980: Low molecular weight circular and linear DNA in mitochondria from normal and male-sterile Zea mays cytoplasm. Nature (London) 284, 565–566.CrossRefGoogle Scholar
  28. Kemble, R. J., and Mans, R. J., 1983: Examination of the mitochondrial genomes of revertant progeny from S cms maize with cloned S-1 and S-2 hybridization probes. J. Mol. Appl. Genet. 2, 161–171.PubMedGoogle Scholar
  29. Kemble, R. J., and Thompson, R. D., 1982: S-1 and S-2, the linear mitochondrial DNAs present in a male sterile line of maize possess terminally attached proteins. Nucleic Acids Res. 10, 8181–8190.PubMedCrossRefGoogle Scholar
  30. Kemble, R. J., Mans, R. J., Gabay-Laughnan, S., and Laughnan, J. R., 1982: Sequences homologous to episomal mitochondrial DNAs in the maize nuclear genome. Nature (London) 304, 744–747.CrossRefGoogle Scholar
  31. Koncz, C., Janos, S., Udvardy, A, Racsmany, M., and Dudits, D., 1981: Cloning of mtDNA fragments homologous to mitochondrial S-2 plasmid-like DNA in maize. Mol. Gen. Genet. 183, 449–458CrossRefGoogle Scholar
  32. Kuntzel, H., Kochel, H. G., Lazarus, C. M., and Lunsdorf, H., 1982: Mitochondrial genes inAspergillus. In: Slonimski, P., Borst, P., and Attardi, G., (eds.). Mitochondrial Genes, pp. 391–403. Cold Spring Harbor Laboratory, Cold Spring Harbor, N. Y.Google Scholar
  33. Laughnan, J. R., and Gabay, S. J., 1973: Mutation leading to nuclear restoration of fertility in S male-sterile cytoplasm in maize. Theor. Appl. Genet. 43, 109–116.CrossRefGoogle Scholar
  34. Laughnan, J. R, and Gabay, S. J., 1975 a: Nuclear and cytoplasmic mutations to fertility in S male-sterile maize. In: Walden, D. B. (ed.). International Maize Symposium: Genetics and Breeding, p. 427. New York: Wiley.Google Scholar
  35. Laughnan, J. R, and Gabay, S. J., 1975 b: An episomal basis for instability of S male sterility in maize and some implications for plant breeding. In: Birky, C. W., Perlman, P. S., and Beyers, T. J. (eds.), Genetics and Biogenesis of Mitochondria and Chloroplasts, pp. 340–349. Columbus: Ohio State Univ. Press.Google Scholar
  36. Laughnan, J. R., and Gabay-Laughnan, S. J., 1983: Cytoplasmic male sterility in maize. Ann. Rev. Genet. 17, 27–48.PubMedCrossRefGoogle Scholar
  37. Laughnan, J. R, Gabay-Laughnan, S. J., and Carlson, J. E., 1981: Characteristics of cms-S reversion to male fertility in maize. Stadler Genet. Symp. 13, 93–114.Google Scholar
  38. Lechner, R. L., and Kelly, Jr., T. J., 1977: The structure of replicating adenovirus 2 DNA molecules. Cell 12, 1007–1020.PubMedCrossRefGoogle Scholar
  39. Levings, C. S., III, and Pring, D. R., 1976: Restriction endonuclease analysis of mitochondrial DNA from normal and Texas cytoplasmic male-sterile maize. Science 193, 158–160.PubMedCrossRefGoogle Scholar
  40. Levings, C. S., III, and Pring, D. R., 1978: The mitochondrial genome of higher plants. Stadler Genet. Symp. 10, 77–94.Google Scholar
  41. Levings, C. S., III, and Sederoff, R. R, 1983: Nucleotide sequence of the S-2 mitochondrial DNA from the S cytoplasm of maize. Proc. Natl. Acad. Sci., U. S. A. 80, 4055–4059.PubMedCrossRefGoogle Scholar
  42. Levings, C. S., III, Sederoff, R. R, Hu, W. W. L, and Timothy, D. H., 1983: Relationships among plasmid-like DNAs of the maize mitochondria. In: Structure and Function of Plant Genomes, pp. 363–374. New York: Plenum.Google Scholar
  43. Levings, C. S., III, Shah, D. M., Hu, W. W. L., Pring, D. R, and Timothy, D. H., 1979: Molecular heterogeneity among mitochondrial DNAs from different maize cytoplasms. In: Cummings, D. J., Fox, C. F., Borst, P., Dawid, I. G., and Weissman, S. M., (eds.), Extrachromosomal DNA, pp. 63–73. ICN-UCLA Symposia on Molecular and Cellular Biology, New York: Academic Press.Google Scholar
  44. Levings, C. S., III, Kim, B. D., Pring, D. L, Conde, M. F., Mans, R. J., Laughnan, J. R, and Gabay-Laughnan, S. J., 1980: Cytoplasmic reversion of cms-S in maize: Association with a transpositional event. Science 209, 1021–1023.PubMedCrossRefGoogle Scholar
  45. Lockhart, L., and Levings, C. S. III. Unpublished results.Google Scholar
  46. Lonsdale, D. M., Thompson, R. D., and Hodge, T. P., 1981: The integrated forms of the S-1 and S-2 DNA elements of maize male sterile mitochondrial DNA are flanked by a large repeated sequence. Nucleic Acids Res. 9, 3657.PubMedCrossRefGoogle Scholar
  47. Lonsdale, D. M., Hodge, T. P., Fauron, C. M.-R, and Flavell, R. B., 1983 a: A predicted structure for the mitochondrial genome from the fertile cytoplasm of maize. In: Goldberg, R. B. (ed.). Plant Molecular Biology (UCLA Symposia on Molecular and Cellular Biology, New Series, Vol. 12), pp. 445–456. New York: Alan R. Liss, Inc.Google Scholar
  48. Lonsdale, D. M., Fauron, C. M.-R, Hodge, T. P., Pring, D. R, and Stern, D. B., 1983 b: Structural alterations in the mitochondrial genome of maize associated with cytoplasmic male sterility. In: Chater, K. F., Cullis, C. A., Hopwood, D. A., Johnson, A. W. B., and Woolhouse, H. W. (eds.). Genetic Rearrangement, pp. 183–206. London: Croom Helm.Google Scholar
  49. McClintock, B., 1978: Mechanisms that rapidly reorganize the genome. Stadler Genet. Symp. 10, 25–48.Google Scholar
  50. McNay, J. W., Chourey, P. S., and Pring, D. R., 1984: Molecular analysis of genomic stability of mitochondrial DNA in tissue cultured cells of maize. Theor. Appl. Genet. 67, 433–437.CrossRefGoogle Scholar
  51. Meints, R. H., Schuster, A, Hu, W. W. L., Timothy, D. H., and Levings, C. S., III: The structural nature of cytoplasmic male sterility associated plasmids in maize mitochondria. Manuscript in preparation.Google Scholar
  52. Messer, W., Meijer, M., Bergmans, H. E. N., Hansen, F. G., von Meyenburg, K., Beck, E., and Schaller, H., 1978: Origin of replication, oriC, of the Escherichia colilLll chromosome: Nucleotide sequence. Cold Spring Harbor Symposia on Quantitative Biology 43, 139–145.Google Scholar
  53. Moore, D. D., Denniston-Thompson, K., Kruger, K. E., Furth, M. E., Williams, B. G., Daniels, D. L., and Blattner, F. R., 1978: Dissection and comparative anatomy of the origins of replication of lambdoid phages. Cold Spring Harbor Symposia on Quantitative Biology 43, 155–163.Google Scholar
  54. Nikiforova, I. D., and Negruk, V. L, 1983: Comparative electrophoretic analysis of plasmid-like mitochondrial DNAs in Vicia faba and in some other legumes. Planta 157, 81–84.CrossRefGoogle Scholar
  55. Paillard, M., Sederoff, R. R, and Levings, C. S. III, 1985: Nucleotide sequence of the S-1 mitochondrial DNA from the S cytoplasm of maize. EMBO J.Google Scholar
  56. Palmer, J. D., and Shields, C. R, 1984: Tripartite structure of the Brassica campestris mitochondrial genome. Nature (London) 307, 437–441.CrossRefGoogle Scholar
  57. Palmer, J. D., Shields, C. R, Cohen, D. B., and Orton, T. J., 1983: An unusual mitochondrial DNA plasmid in the genus Brassica. Nature (London) 301, 725–728.CrossRefGoogle Scholar
  58. Fowling, A., 1981: Species of small DNA molecules found in mitochondria from sugar-beet with normal and male-sterile cytoplasms. Mol. Gen. Genet. 183, 82–84.CrossRefGoogle Scholar
  59. Fowling, A., and Ellis, T. H. N., 1983: Studies on the organelle genomes of sugarbeet with male-fertile and male-sterile cytoplasms. Theor. and Appl. Genet. 65, 323–328.Google Scholar
  60. Pring, D. R, and Levings, C. S., III, 1978: Heterogeneity of maize cytoplasmic genomes among male-sterile cytoplasms. Genetics 89, 121–136.PubMedGoogle Scholar
  61. Pring, D. R, Conde, M. F., and Schertz, K. F., 1982: Organelle genome diversity on sorghum: Male-sterile cytoplasms. Crop Sci. 22, 414–421.CrossRefGoogle Scholar
  62. Pring, D. R, Levings, C. S., III, Hu, W. W. L., and Timothy, D. H., 1977: Unique DNA associated with mitochondria in the “S” type cytoplasm of male-sterile maize. Proc. Natl. Acad. Sci., U.S.A. 74, 2904–2908.PubMedCrossRefGoogle Scholar
  63. Quetier, F., and Vedel, F., 1977: Heterogeneous population of mitochondrial DNA molecules in higher plants. Nature (London) 268, 365–368.CrossRefGoogle Scholar
  64. Rekosh, D. M. K., Russell, W. C., Bellet, A. J. D., Robinson, A. J., 1977: Identification of a protein linked to the ends of adenovirus DNA. Cell 11, 283–295.PubMedCrossRefGoogle Scholar
  65. Ronald, P., Bedinger, P., Rivin, C., Walbot, V, Bland, M., Levings, C., III, Sederoff, R.: Maize mitochondrial plasmid S-1 sequences share homology with chloroplast gene psbK (photogene 32). Submitted for publication.Google Scholar
  66. Salas, M., Mellado, R. P., and Vinuela, E., 1978: Characterization of a protein covalently linked to the 5’ termini of the DNA of Bacillus subtilis phage Ø 29. J. Mol. Biol. 119, 269–291.PubMedCrossRefGoogle Scholar
  67. Sederoff, R. R, 1984: Structural variation in mitochondrial DNA. In: Advances in Genetics 22, 1–108.PubMedCrossRefGoogle Scholar
  68. Sederoff, R. R, Levings, C. S., III, Timothy, D. H., and Hu, W. W. L, 1981: Evo Supernumerary mtDNA 109 lution of DNA sequence organization in mitochondrial genomes ofZea. Proc. Natl. Acad. Sci., U.S.A. 78, 5953–5957.PubMedCrossRefGoogle Scholar
  69. Shah, D. M., and Levings, C. S., III, 1974: Mitochondrial DNA from maize hybrids with normal and Texas cytoplasms. Crop Science 14, 852–853.CrossRefGoogle Scholar
  70. Sparks, R. B., Jr., and Dale, R. M. K., 1980: Characterization of 3H-labeled supercoiled mitochondrial DNA from tobacco suspension culture cells. Mol. Gen. Genet. 180, 351–355.CrossRefGoogle Scholar
  71. Spencer, D. F., Schnare, M. N., and Gray, M. W., 1984: Pronounced structural similarities between the small subunit ribosomal RNA genes of wheat mitochondria and Escherichia coli. Proc. Natl. Acad. Sci., U.S.A. 81, 493–497.PubMedCrossRefGoogle Scholar
  72. Spruill, W. M., Levings, C. S., III, and Sederoff, R. R, 1981: Organization of mitochondrial DNA in normal and Texas male sterile cytoplasms of maize. Dev. Genet. 2, 319–336.CrossRefGoogle Scholar
  73. Stern, D. B., and Palmer, J. D., 1984: Extensive and widespread homologies between mitochondrial DNA and chloroplast DNA in plants. Proc. Natl. Acad. Sci., U.S.A. 81, 1946–1950.PubMedCrossRefGoogle Scholar
  74. Stern, D. B., and Lonsdale, D. M., 1982: Mitochondrial and chloroplast genomes of maize have a 12kb DNA sequence in common. Nature (London) 299, 698–702.CrossRefGoogle Scholar
  75. Sussenbach, J. S., and Kuijk, M. G., 1977: Studies on the mechanism of replication of adenovirus DNA: V. The location of termini of replication. Virology 77, 149–157.PubMedCrossRefGoogle Scholar
  76. Synenki, R. M., Levings, C. S., III, and Shah, D. M., 1978: Physicochemical characterization of mitochondrial DNA from soybean. Plant Physiol. 61, 460–464.PubMedCrossRefGoogle Scholar
  77. Timothy, D. H., Levings, C. S., III, Hu, W. W. L, and Goodman, M. M., 1983: Plasmid-like DNAs in diploperennial teosinte. Maydica 28, 139–149.Google Scholar
  78. Timothy, D. H., Levings, C. S., III, Pring, D. R, Conde, M. F., and Kermicle, J. L., 1979: Organelle DNA variation and systematic relationships in the genus Zea: Teosinte. Proc. Natl. Acad. Sci., U.S.A. 76, 4220–4224.PubMedCrossRefGoogle Scholar
  79. Wallace, D. C., 1982: Structure and evolution of organelle genomes. Microbiol. Rev. 46, 208–240.PubMedGoogle Scholar
  80. Ward, B. L., Anderson, R. S., and Bendich, A. J., 1981: The size of the mitochondrial genome is large and variable in a family of plants (Curcurbitaceae). Cell 25, 793–803.PubMedCrossRefGoogle Scholar
  81. Weissinger, A. K., Timothy, D. H., Levings, C. S., III, and Goodman, M. M., 1983: Patterns of mitochondrial DNA variation in indigenous maize races of Latin America. Genetics 104, 365–379.PubMedGoogle Scholar
  82. Weissinger, A. K., Timothy, D. H., Levings, C. S., III, Hu, W. W. L, and Goodman, M. M., 1982: Unique plasmid-like mitochondrial DNAs from indigenous maize races of Latin America. Proc. Natl. Acad. Sci., U.S.A. 79, 1.PubMedCrossRefGoogle Scholar
  83. Winnacker, E.-L., 1978: Adenovirus DNA: Structure and function of a novel replicón. Cell 14, 761–773.PubMedCrossRefGoogle Scholar
  84. Wright, R. M., Horrum, M. A, and Cummings, D. J., 1982: Are mitochondrial structural genes selectively amplified during senescence inPodospora anserina ? Cell 29, 505–515.PubMedCrossRefGoogle Scholar
  85. Yehle, C. O., 1978: Genome-linked protein associated with the 5’ termini of bacteriophage Ø 29 DNA. Virology 27, 776–783.Google Scholar
  86. Yoshikawa, H., and Ito, J., 1981: Terminal proteins and short inverted terminal repeats of the small Bacillus bacteriophage genomes. Proc. Natl. Acad. Sci., U.S.A. 78, 2596–2600.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag/Wien 1985

Authors and Affiliations

  • R. R. Sederoff
    • 1
  • C. S. LevingsIII
    • 1
  1. 1.Department of GeneticsNorth Carolina State UniversityRaleighUSA

Personalised recommendations