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Selective transcription and post-transcriptional processing of the heteroplasmic mitochondrial orf156 copies in the nucleus-cytoplasm hybrids of wheat

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Abstract

Transcript profile and post-transcriptional processing of the mitochondrial orf156 were compared among the nucleus-cytoplasm (NC) hybrids of tetraploid and hexaploid wheat and their parental lines. These NC hybrids, in which the plasmon from the maternal Aegilops squarrosa parent is combined with the nuclear genomes of the paternal parents, and their parental lines were previously shown to have heteroplasmic copies of the polycistronic transcriptional unit nad3-orf156 in different sub-stoichiometries. Despite the heteroplasmic conditions, only single transcript types were detected among reverse transcription-PCR products of the orf156 mRNA in the respective lines. In the NC hybrids only a major maternal copy was transcribed and edited, likewise in the parental lines only single major copies were transcribed and edited. RNA gel blot analysis using the orf156 probe showed that the NC hybrids had the transcripts similar to the parental lines but unlike the maternal line. Primer extension analysis further revealed the orf156 transcripts with different 5′ termini, which most probably resulted from the alternative post-transcriptional cleavages of the precursor mRNA. These cleaved transcripts were polymorphic not only among the lines but also among four different tissues. The cleavages were highly selective and the paternal-type cleavages predominated in the NC hybrids, irrespective of the tissues studied. This seemingly neutral polymorphisms in wheat could make this system convenient for further analysis of mitochondrial gene expression in plants.

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References

  • Arrieta-Montiel, M., Lyznik, A., Woloszynska, M., Janska, H., Tohme, J. and Mackenzie, S. 2001. Tracing evolutionary and developmental implications of mitochondrial stoichiometric shifting in the common bean. Genetics 158: 851–864.

    PubMed  Google Scholar 

  • Asakura, N., Nakamura, C. and Ohtsuka, I. 1997. RAPD markers linked to the nuclear gene from Triticum timopheevi that confers compatibility with Aegilops squarrosa cytoplasm on alloplasmic durum wheat. Genome 40: 201–210.

    Google Scholar 

  • Asakura, N., Nakamura, C. and Ohtsuka, I. 2000. Homoeoallelic gene Ncc-tmp of Triticum timopheevii conferring compatibility with the cytoplasm of in the tetraploid wheat nuclear background. Genome 43: 503–511.

    PubMed  Google Scholar 

  • Bentolila, S., Alfonso, A. A. and Hanson, M. R. 2002. A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99: 10887–10892.

    Google Scholar 

  • Chesser, R.K. 1998. Heteroplasmy and organellar gene dynamics. Genetics 150: 1309–1327.

    PubMed  Google Scholar 

  • Chinnery, P.F., Thorburn, D.R., Samuels, D.C., White, S.L., Dahl, H.M., Turnbull, D.M., Lightowlers, R.N. and Howell, N. 2000. The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends Genet 16: 500–505.

    PubMed  Google Scholar 

  • Cooper, P., Butler, E. and Newton, K.J. 1990. Identification of a maize nuclear gene which influences the size and number of cox2 transcripts in mitochondria of perennial teosintes. Genetics 126: 461–467.

    PubMed  Google Scholar 

  • Gagliardi, D. and Leaver, C.J. 1999. Polyadenylation accelerates the degradation of the mitochondrial mRNA associated with cytoplasmic male sterility in sunflower. EMBO J. 18: 3757–3766.

    PubMed  Google Scholar 

  • Gagliardi, D., Perrin, R., Marechal-Drouard, L., Grienenberger, J.M. and Leaver, C.J. 2001. Plant mitochondrial polyadenylated mRNAs are degraded by a 3_-to 5_-exoribonuclease activity, which proceeds unimpeded by stable secondary structures. J. Biol. Chem. 276: 43541–43547.

    PubMed  Google Scholar 

  • Giege, P., Hoffmann, M., Binder, S. and Brennicke, A. 2000. RNA degradation buffers asymmetries of transcription in Arabidopsis mitochondria. EMBO Rep. 1: 164–170.

    PubMed  Google Scholar 

  • Gualberto, J.M., Bonnard, G., Lamattina, L. and Grienenburger, J.M. 1991. Expression of the wheat mitochondrial nad3-rps12 transcription unit: correlation between editing and mRNA maturation. Plant Cell 3: 1109–1120.

    PubMed  Google Scholar 

  • Hattori, N., Kitagawa, K., Takumi, S. and Nakamura, C. 2002. Mitochondrial DNA heteroplasmy in wheat, Aegilops and their nucleus-cytoplasm hybrids. Genetics 160: 1619–1630.

    PubMed  Google Scholar 

  • Hedtke, N., Borner, T. and Weihe, A. 1997. Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277: 809–811.

    PubMed  Google Scholar 

  • Hedtke, B., Borner, T. and Weihe, A. 2000. One RNA polymerase serving two genomes. EMBO Rep 1: 435–440.

    PubMed  Google Scholar 

  • Hirose, T. and Sugiura, M. 2001. Involvement of a site-specific trans-acting factor and a common RNA-binding protein in the editing of chloroplast mRNAs: development of a chloroplast in vitro RNA editing system. EMBO J. 20: 1144–1152.

    PubMed  Google Scholar 

  • Hoffmann, M., Kuhn, J., Daschner, K. and Binder, S. 2001. The RNA world of plant mitochondria. Progr. Nucl. Acids Res. Mol. Biol. 70: 119–154.

    Google Scholar 

  • Ikeda, T.M. and Gray, M.W. 1999. Identification and characterization of T3/T7 bacteriophage-like RNA polymerase sequences in wheat. Plant Mol. Biol. 40: 567–578.

    PubMed  Google Scholar 

  • Iwabuchi, M., Kyozuka, J. and Shimamoto, K. 1993. Processing followed by complete editing of an altered mitochondrial atp6 RNA restores fertility of cytoplasmic male sterile rice. EMBO J. 12: 1437–1446.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Kennell, J.C. and Pring, D.R. 1989. Initiation and processing of atp6, T-urf13 and orf221 transcripts from mitochondria of T cytoplasm maize. Mol. Gen. Genet. 216: 16–24.

    Google Scholar 

  • Kitagawa, K., Takumi, S. and Nakamura, C. 2002. Evidence of paternal transmission of mitochondrial DNA in a nucleuscytoplasm hybrid of timopheevi wheat. Genes Genet. Syst. 77 (in press).

  • Kubo, T., Nishizawa, S., Sugawara, A., Itchoda, N., Estiati, A. and Mikami, T. 2000. The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNA(Cys)(GCA). Nucl. Acids Res. 28: 2571–2576.

    PubMed  Google Scholar 

  • Kuhn, J., Tengler, U. and Binder, S. 2001. Transcript lifetime is balanced between stabilizing stem-loop structures and degradationpromoting polyadenylation in plant mitochondria. Mol. Cell Biol. 21: 731–742.

    PubMed  Google Scholar 

  • Laser, B. and Kück, U. 1995. The mitochondrial atpA/atp9 cotranscript in wheat and triticale: RNA processing depends on the nuclear genotype. Curr. Genet. 29: 50–57.

    PubMed  Google Scholar 

  • Laser, B., Mohr, S. Odenbach, W., Oettler, G. and Kück, U. 1997. Paternal and novel copies of the mitochondrial orf25 gene in the hybrid crop-plant triticale: predominant trancriptional expression of the maternal gene copy. Curr. Genet. 32: 337–347.

    PubMed  Google Scholar 

  • Lu, B. and Hanson, M.R. 1992. A single nuclear gene specifies the abundance and extent of RNA editing of a plant mitochondrial transcript. Nucl. Acids Res. 20: 5699–5703.

    PubMed  Google Scholar 

  • Mackenzie, S. and Chase, C. 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.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Manfredi, G., Fu, J., Ojaimi, J., Sadlock, J.E., Kwong, J. Q., Guy, J. and Schon, E.A. 2002. Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitohondrial DNA-encoded gene, to the nucleus. Nature Genet. 30: 394–399.

    PubMed  Google Scholar 

  • McFarland, R., Clark, K.M., Morris, A.A., Taylor, R.W., Macphail, S., Lightowlers, R.N. and Turnbull, D.M. 2002. Multiple neonatal deaths due to a homoplasmic mitochondrial DNA mutation. Nature Genet. 30: 145–146.

    PubMed  Google Scholar 

  • Newton, K.J. and Cor, E.H. 1986. Mitochondrial DNA changes in abnormal growth mutants of maize. Proc. Natl. Acad. Sci. USA 83: 7363–7366.

    Google Scholar 

  • Newton, K.J., Knudsen, C., Gabay-Laughnan, S. and Laughnan, J.R. 1990. An abnormal growth mutant in maize has a defective mitochondrial cytochrome oxidase gene. Plant Cell 2: 107–113.

    PubMed  Google Scholar 

  • Ogihara, Y., Kurihara, Y., Futami, K., Tsuji, K. and Murai, K. 1999. Photoperiod-sensitive cytoplasmic male sterility in wheat: nuclear-mitochondrial incompatibility results in differential processing of the mitochondrial orf25 gene. Curr. Genet. 36: 354–362.

    PubMed  Google Scholar 

  • Ohtsuka, I. 1991. Genetic differentiation in wheat nuclear genomes in relation to compatibility with Aegilops squarrosa cytoplasm and application to phylogeny of polyploid wheat. J. Fac. Agric. Hokkaido Univ. 65 (part 2): 127–198.

    Google Scholar 

  • Pruitt, K.D. and Hanson, M.R. 1991. Transcription of the Petunia mitochondrial CMS-associated Pcf locus in male-sterile and fertility restored lines. Mol. Gen. Genet. 227: 348–355.

    PubMed  Google Scholar 

  • Rocheford, T.R., Kennell, J.C. and Pring, D.R. 1992. Genetic analysis of nuclear control of T-urf13/orf221 transcription in T cytoplasm maize. Theor. Appl. Genet. 84: 891–898.

    Google Scholar 

  • Sakamoto, W., Kondo, H., Murata, M. and Motoyoshi, F. 1996. Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8: 1377–1390.

    PubMed  Google Scholar 

  • Singh, M. and Brown, G.G. 1991. Suppression of cytoplasmic sterility by nuclear gene alters expression of a novel mitochondrial gene region. Plant Cell 3: 1349–1362.

    PubMed  Google Scholar 

  • Singh, M. and Brown, G.G. 1993. Characterization of expression of a mitochondrial gene region associated with the Brassica 'Polima' CMS: developmental influences. Curr. Genet. 24: 316–322.

    PubMed  Google Scholar 

  • Tsuji, S. and Murata, M. 1976. Specific interaqction between the D genome and the three alien cytoplasms in wheat. II. Seed inviability induced by the alien cytoplasms. Jpn. J. Genet. 51: 327–336.

    Google Scholar 

  • Tsukamoto, N., Asakura, N., Hattori, N., Takumi, S., Mori, N. and Nakamura, C. 2000. Identification of paternal mitochondrial DNA sequences in the nucleus-cytoplasm hybrids of tetraploid and hexaploid wheat with D and D2 plasmons from Aegilops species. Curr. Genet. 38: 208–217.

    PubMed  Google Scholar 

  • Tsunewaki, K. 1996. Plasmon analysis as the counterpart of genome analysis. In: P.P. Jauhar (Ed.) Methods of Genome Analysis in Plants, CRC Press, Boca Raton, FL, pp. 271–299.

    Google Scholar 

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Correspondence to Chiharu Nakamura.

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Kitagawa, K., Takumi, S. & Nakamura, C. Selective transcription and post-transcriptional processing of the heteroplasmic mitochondrial orf156 copies in the nucleus-cytoplasm hybrids of wheat. Plant Mol Biol 53, 609–619 (2003). https://doi.org/10.1023/B:PLAN.0000019075.31353.77

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