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.
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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.
Albert, B., B. Godelle & P.H. Gouyon, 1998. Evolution of plant mitochondrial genome: duplication and deletion of sequences. J. Mol. Evol. 46: 155–158.
Bendich, A.J., 1993. Reaching for the ring: the study of mitochondrial genome structure. Curr. Genet. 24: 279–290.
Brennicke, A. & P. Bland, 1982. Mitochondrial DNA species from Oenothera with unique sequences. Mol. Gen. Genet. 18: 461–466.
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.
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.
Dale, R.M.K., D.H. Duesing & D. Keene, 1981. Supercoiled mitochondrial DNAs from plant tissue culture cells. Nucl. Acids Res. 18: 4583–4593.
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.
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.
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.
Fauron, C.M.R., M. Casper, Y. Gao & B. Moore, 1995. The maize mitochondrial genome: dynamic, yet functional. Trends Genet. 11: 228–235.
Godelle, B. & X. Reboud, 1995. Why are organelle uniparentally inherited? Proc. R. Soc. London B 259: 27–33.
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.
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.
Hanson, M.R., 1991. Plant mitochondrial mutations and male sterility. Ann. Rev. Genet. 25: 461–486.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Nosek, J., L. Tomaska, H. Fukuhara, Y. Suyama & L. Kovac, 1998. Linear mitochondrial genomes: 30 years down the line. Trends Genet. 14: 184–188.
Palmer, J.D. & C.R. Shields, 1984. Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307: 437–440.
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.
Prat, D., 1983. Genetic variability induced in N. sylvestris by protoplast culture. Theor. Appl. Genet. 64: 223–230.
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.
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.
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.
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.
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.
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.
Small, I.D., R. Suffolk & C.J. Leaver, 1989. Evolution of plant mitochondrial genomes via substoichiometric intermediates. Cell 58: 69–76.
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.
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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
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DOI: https://doi.org/10.1023/A:1022356330794