Skip to main content
Log in

Amplification of Nicotiana Sylvestris Mitochondrial Subgenomes is under Nuclear Control and is Associated with Phenotypic Changes

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

We have previously shown the presence in a Nicotiana sylvestris protoplast-derived plant of both a nuclear mutation conferring male sterility (ms4) and a mtDNA reorganisation, named U, characterised by the amplification of substoichiometric mtDNA fragments generated by recombination in the parent T mtDNA. Here we show by physical mapping that the recombining repeats are in direct orientation, thus generating two subgenomes both of which are amplified in the U organisation to the detriment of the parent molecule, and are maintained through sexual reproduction. The nuclear ms4 mutation is likely to have play a role in the shift in mitochondrial molecule equilibrium, as higher levels of recombinant fragments were present in protoplast-derived T calli carrying the ms4 allele than in wild type calli or leaves. The MS4 gene could then lead to conflictual situation. However, subgenomic molecules were counter-selected during the regeneration process, suggesting the existence of different selective pressures in differentiated and non-differentiated cells. The U organisation is associated with higher stem height and late flowering, characters that may not be neutral from a selection point of view. The U equilibrium is an unusual example of sudden mtDNA reorganisation, without obvious differences in genetic information and with only a limited phenotypic impact.

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.

Similar content being viewed by others

References

  • Albert, B., B. Godelle, A. Atlan, R. De Paepe & P.H. Gouyon, 1996. Evolution of plant mitochondrial genome: model of a three-level selection process. Genetics 144: 369–382.

    Google Scholar 

  • Albert, B., B. Godelle & P.H. Gouyon, 1998. Evolution of plant mitochondrial genome: duplication and deletion of sequences. J. Mol. Evol. 46: 155–158.

    Google Scholar 

  • Bendich, A.J., 1993. Reaching for the ring: the study of mitochondrial genome structure. Curr. Genet. 24: 279–290.

    Google Scholar 

  • Brennicke, A. & P. Bland, 1982. Mitochondrial DNA species from Oenothera with unique sequences. Mol. Gen. Genet. 18: 461–466.

    Google Scholar 

  • Chétrit, P., R. Rios, R. De Paepe, V. Vitart, S. Gutierres & F. Vedel, 1992. Cytoplasmic male sterility is associated with large deletions in the mitochondrial DNA of two Nicotiana sylvestris protoclones. Curr. Genet. 21: 131–137.

    Google Scholar 

  • Chupeau, M.C., C. Bellini, P. Guerche, B. Maisonneuve, G. Vastra & Y. Chupeau, 1989. Transgenic plants of lettuce (Lactuca sativa) obtained through electroporation of protoplasts. Biotechnology 7: 503–508.

    Google Scholar 

  • Dale, R.M.K., D.H. Duesing & D. Keene, 1981. Supercoiled mitochondrial DNAs from plant tissue culture cells. Nucl. Acids Res. 18: 4583–4593.

    Google Scholar 

  • Dale, R.M.K., M. Wu & M.C.C. Kiernan, 1983. Analysis of four tobacco mitochondrial DNA size classes. Nucl. Acid Res. 11: 1673–1685.

    Google Scholar 

  • De Paepe, R., A. Koulou, J.L. Pham & S.C. Brown, 1990. Nuclear DNA content and separation of Nicotiana sylvestris vegetative and generative nuclei at various stages of male gametogenesis. Plant Sci. 70: 255–265.

    Google Scholar 

  • Escote-Carlson, L.J., S. Gabay-Laughnan & J.R. Laughnan, 1990. Nuclear genotype affects mitochondrial genome organization of CMS-S in maize. Mol. Gen. Genet. 223: 457–464.

    Google Scholar 

  • Fauron, C.M.R., M. Casper, Y. Gao & B. Moore, 1995. The maize mitochondrial genome: dynamic, yet functional. Trends Genet. 11: 228–235.

    Google Scholar 

  • Godelle, B. & X. Reboud, 1995. Why are organelle uniparentally inherited? Proc. R. Soc. London B 259: 27–33.

    Google Scholar 

  • Gutierres, S., C. Lelandais, R. De Paepe, F. Vedel & P. Chétrit, 1997a. A mitochondrial sub-stoichiometric orf87-nad3-nad1 exonA co-transcription unit present in Solanaceae was amplified in the genus Nicotiana. Curr. Genet. 31: 55–62.

    Google Scholar 

  • Gutierres, S., M. Sabar, C. Lelandais, P. Chétrit, P. Diolez, H. Degand, M. Boutry, F. Vedel, Y. de Kouchkovsky & R. De Paepe, 1997b. Lack of mitochondrial and nuclear encoded subunits of Complex I and alteration of respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc. Natl. Acad. Sci. 94: 3436–3441.

    Google Scholar 

  • Hanson, M.R., 1991. Plant mitochondrial mutations and male sterility. Ann. Rev. Genet. 25: 461–486.

    Google Scholar 

  • Hartmann, C., J. De Buyser, Y. Henry, M.C. Morère-Le Paven, T. Dyer & A. Rode, 1992. Nuclear genes control changes in the organization of the mitochondrial genome in tissue cultures derived from immature embryos of wheat. Curr. Genet. 21: 515–520.

    Google Scholar 

  • Hartmann, C., Y. Henry, J. Treagar & A. Rode, 2000. Nuclear control of mitochondrial genome reorganization characterized using cultured cells of ditelosomic and nullisomic-tetrasomic wheat lines. Curr. Genet. 38: 156–162.

    Google Scholar 

  • He, S., A. Lyznik & S. Mackenzie, 1995. Pollen fertility restoration by nuclear gene Fr in CMS Bean: nuclear-directed alteration of a mitochondrial population. Genetics 139: 955–962.

    Google Scholar 

  • Janska, H., R. Sarria, M. Woloszynska, A. Arrieta-Montiel & S.A. Mackenzie, 1998. Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10: 1163–1180.

    Google Scholar 

  • Kanazawa, A., N. Tsutsumi & A. Hirai, 1994. Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 138: 865–870.

    Google Scholar 

  • Kubo, N., K. Ozawa, T. Hino & K.I. Kadowaki, 1996. A ribosomal protein L2 gene is transcribed, spliced and edited at one site in rice mitochondria. Plant Mol. Biol. 31: 853–862.

    Google Scholar 

  • Lelandais, C., B. Albert, S. Gutierres, R. De Paepe, B. Godelle, F. Vedel & P. Chétrit, 1998. Organization and expression of the mitochondrial genome in the Nicotiana sylvestris CMSII mutant. Genetics 150: 873–882.

    Google Scholar 

  • Lonsdale, D., M.T. Brears, T.P. Hodge, S.E. Melville & W.H. Rottmann, 1988. The plant mitochondrial genome: homologous recombination as a mechanism for generating heterogeneity. Phil. Trans. R. Soc. London B 319: 149–163.

    Google Scholar 

  • Loublier, Y., P. Douault & M.H. Pham-Delègue, 1986. Méthode de comptage automatique des grains de pollen: étude de la production pollinique chez le tournesol (Helianthus annuus L., Composite). Apidologie 17: 245–256.

    Google Scholar 

  • Mackenzie, S.A. & C.D. Chase, 1990. Fertility restoration is associated with loss of a portion of the mitochondrial genome in cytoplasmic male-sterile common bean. Plant Cell 2: 905–912.

    Google Scholar 

  • Mackenzie, S.A., D.R. Pring, M.J. Basset & C.D. Chase, 1988. Mitochondrial DNA rearrangement associated with fertility restoration and cytoplasmic reversion to fertility in cytoplasmic male sterile Phaseolus vulgaris L. Proc. Natl. Acad. Sci. USA 85: 2714–2717.

    Google Scholar 

  • Martinez-Zapater, J.M., P. Gil, J. Capel & C. Somerville, 1992. Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell 4: 889–899.

    Google Scholar 

  • Mulcahy, G.B. & D.L.Mulcahy, 1983. A comparison of pollen tube growth in bi-and trinucleate pollen, pp. 35–41 in Pollen Biology and Implications for Plant Breeding, edited by D.L. Mulcahy & E. Ottaviano. Elsevier Science Publishing, New York.

    Google Scholar 

  • Newton, K.J., E.H. Coe, Jr., S. Gabay-Laughnan & J. R. Laughnan, 1989. Abnormal growth phenotypes and mitochondrial mutations in maize. Maydica 34: 291–296.

    Google Scholar 

  • Nosek, J., L. Tomaska, H. Fukuhara, Y. Suyama & L. Kovac, 1998. Linear mitochondrial genomes: 30 years down the line. Trends Genet. 14: 184–188.

    Google Scholar 

  • Palmer, J.D. & C.R. Shields, 1984. Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307: 437–440.

    Google Scholar 

  • Pla, M., C. Mathieu, R. De Paepe, P. Chétrit & F. Vedel, 1995. Deletion of the last two exons of the mitochondrial nad7 gene results in lack of the NAD7 polypeptide in a Nicotiana sylvestris CMS mutant. Mol. Gen. Genet. 248: 79–88.

    Google Scholar 

  • Prat, D., 1983. Genetic variability induced in N. sylvestris by protoplast culture. Theor. Appl. Genet. 64: 223–230.

    Google Scholar 

  • Reenan, R.A. & R.D. Kolodner, 1992. Characterisation of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH1 genes: evidence for separate mitochondrial and nuclear functions. Genetics 132: 975–985.

    Google Scholar 

  • Rode, A., C. Hartmann, D. Falconet, B. Lejeune, F. Quetier, A. Benslimane, Y. Henry & J. De Buyser, 1987. Extensive mitochondrial DNA variation in somatic tissue cultures initiated from wheat immature embryos. Curr. Genet. 12: 369–376.

    Google Scholar 

  • Rottman, W.H., T. Brears, T.P. Hodge & D.M. Lonsdale, 1987. A mitochondrial gene is lost via homologous recombination during reversion of CMS-T maize to fertility. EMBO J. 6: 1541–1546.

    Google Scholar 

  • Schuster, W. & A. Brennicke, 1994. The plant mitochondrial genome: physical structure, information content, RNA editing and gene migration to the nucleus. Ann. Rev. Plant Physiol. Plant Mol. Biol. 45: 61–78.

    Google Scholar 

  • Shirzadegan, M., J.D. Palmer, M. Christy & E.D. Earle, 1991. Patterns of mitochondrial instability in Brassica campestris cultured cells. Plant Mol. Biol. 16: 21–37.

    Google Scholar 

  • Small, I.O., P. Isaac & J. Leaver, 1987. Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the mitochondrial genome diversity in maize. EMBO J. 6: 865–869.

    Google Scholar 

  • Small, I.D., R. Suffolk & C.J. Leaver, 1989. Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58: 69–76.

    Google Scholar 

  • Vitart, V., R. De Paepe, C. Mathieu, C. Chétrit & F. Vedel, 1992. Amplification of substoichiometric recombinant mitochondrial DNA sequences in a nuclear male sterile mutant regenerated from protoplast culture in Nicotiana sylvestris. Mol. Gen. Genet. 233: 193–200.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Béatrice Albert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Albert, B., Lelandais, C., Pla, M. et al. Amplification of Nicotiana Sylvestris Mitochondrial Subgenomes is under Nuclear Control and is Associated with Phenotypic Changes. Genetica 117, 17–25 (2003). https://doi.org/10.1023/A:1022356330794

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022356330794

Navigation