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The mat-r open reading frame is transcribed from a non-canonical promoter and contains an internal promoter to co-transcribe exonsnad1e and nad5III in wheat mitochondria

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Abstract

The expression of the mat-r locus (mat-r-nad1e-nad5III) was studied in wheat mitochondria. Transcription initiation sites were mapped by S1 protection, primer extension and capping experiments. Two different transcription initiation sites were found. One, non-canonical promoter of low expression level generates a transcript containing the complete mat-r open reading frame (orf), suggesting that this form is the maturase-reverse transcriptase mRNA. A second transcription initiation site, found within the coding region of the mat-r orf, directs the transcription of an abundant co-transcript containing the carboxy-terminal region of the mat-r orf, exon e of the nad1 gene, exon III of the nad5 gene and their respective trans-introns. The co-transcript promoter carries the consensus motif of plant mitochondrial promoters. Analysis of transcript sequences reveals the presence of editing sites in analogous positions in both nad1e and nad5III trans-introns, suggesting that RNA editing is necessary for the trans-splicing process.

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References

  • Araya, A., Bégu, D. and Litvak, S. 1994. RNA editing in plants. Physiol. Plant. 91: 543–550.

    Article  Google Scholar 

  • Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.A., Smith, J.A. and Struhl, K. 1989. Current Protocols in Molecular Biology. Greene Publishing Associates/Wiley Interscience, New York.

    Google Scholar 

  • Bégu, D., Mercado, A., Farré, J.C., Moenne, A., Holuigue, L., Araya, A. and Jordana, X. 1998. Editing status of mat-rtranscripts in mitochondria from two plant species: C-to-U changes occur in putative functional RT and maturase domains. Curr. Genet. 33: 420–428.

    PubMed  Google Scholar 

  • Binder, S., Marchfelder, A., Brennicke, A. and Wissinger, B. 1992. RNA editing in trans-splicing intron sequences of nad2mRNAs in Oenotheramitochondria. J. Biol. Chem. 267: 7615–7623.

    PubMed  Google Scholar 

  • Binder, S., Marchfelder, A. and Brennicke, A. 1996. Regulation of gene expression in plant mitochondria. Plant Mol. Biol. 32: 303–314.

    PubMed  Google Scholar 

  • Bland, M.M., Levings III, C.S. and Matzinger, D.F. 1986. The tobacco mitochondrial ATPase subunit 9 gene is closely linked to an open reading frame for a ribosomal protein. Mol. Gen. Genet. 204: 8–16.

    PubMed  Google Scholar 

  • Börner, G.V., Mörl, M., Wissinger, B., Brennicke, A. and Schmelzer, C. 1995. RNA editing of a group II intron in Oenotheraas a prerequisite for splicing. Mol. Gen. Genet. 246: 739–744.

    PubMed  Google Scholar 

  • Brennicke, A., Grohmann, L., Hiesel, R., Knoop, V. and Schuster, W. 1993. The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants. FEBS Lett. 325: 140–145.

    PubMed  Google Scholar 

  • Carrillo, C. and Bonen, L. 1997. RNA editing status of nad7intron domains in wheat mitochondria. Nucl. Acids Res. 25: 403–409.

    PubMed  Google Scholar 

  • Chapdelaine, Y. and Bonen, L. 1991. The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a trans-splicing model for this gene-in-pieces. Cell 65: 645–672.

    Google Scholar 

  • Conklin, P.C., Wilson, R.K. and Hanson, M.R. 1991. Multiple transsplicing events are required to produce a mature nad1transcript in a plant mitochondrion. Genes Dev. 5: 1407–1415.

    PubMed  Google Scholar 

  • Covello, P.S. and Gray, M.W. 1991. Sequence analysis of wheat mitochondrial transcripts capped in vitro: definitive identification of transcript initiation sites. Curr. Genet. 20: 245–251.

    PubMed  Google Scholar 

  • Garignani, G., Groudinsky, O., Frezza, D., Schiavon, E., Bergantino, E. and Slonimski, P. 1983. An mRNA maturase is encoded by the first intron of the mitochondrial gene for the subunit I of cytochrome oxidase in S.cerevisiae. Cell 35: 733–742.

    PubMed  Google Scholar 

  • Haouazine, N., Takvorian, A., Jubier, M.F., Michel, F. and Lejeune, B. 1993. The nad6gene and the exon d of nad1are co-transcribed in wheat mitochondria. Curr. Genet. 24: 533–538.

    PubMed  Google Scholar 

  • Kapoor, S., Wakasugi, T., Deno, H. and Sugiura, M. 1994. An atpEspecific promoter within the coding region of the atpBgene in tobacco chloroplast DNA. Curr. Genet. 26: 263–268.

    PubMed  Google Scholar 

  • Liu, A.W., Narayanan, K., André, C.P., Kaleikau, E.K. and Walbot, V. 1992. Co-transcription of orf25and coxIIIin rice mitochondria. Curr. Genet. 21: 507–513.

    PubMed  Google Scholar 

  • Lonsdale, D. 1984. A review of the structure and organization of the mitochondrial genome of higher plants. Plant Mol. Biol. 3: 201–206.

    Google Scholar 

  • MacKeown, M. 1992. Alternative mRNA splicing. Annu. Rev. Cell Biol. 8: 133–155.

    PubMed  Google Scholar 

  • Malek, O., Brennicke, A. and Knoop, V. 1997. Evolution of transsplicing plant mitochondrial introns in pre-Permian times. Proc. Natl. Acad. Sci. USA 94: 553–558.

    PubMed  Google Scholar 

  • Michel, F. and Ferat, J.L. 1995. Structure and activities of group-II introns. Annu. Rev. Biochem. 64: 435–431.

    PubMed  Google Scholar 

  • Michel, F., Umesono, K. and Ozeki, H. 1989. Comparative and functional anatomy of group-II catalytic introns: a review. Gene 82: 5–30.

    PubMed  Google Scholar 

  • Mohr, G.P., Perlman, S. and Lambowitz, A.M. 1993. Evolutionary relationships among group-II intron-encoded proteins and identification of a conserved domain that may be related to maturase function. Nucl. Acids Res. 21: 4991–4997.

    PubMed  Google Scholar 

  • Morawala-Patell, V., Gualberto, J.M., Lamattina, L., Grienenberger, J.M. and Bonnard, G. 1998. Cis-and trans-splicing and RNA editing are required for the expression of nad2in wheat Mitochondria. Mol. Gen. Genet. 258: 503–511.

    PubMed  Google Scholar 

  • Nakazono, M., Itadani, H., Wakasugi, T., Tsutsumi, N., Sugiura, M. and Hirai, A. 1995. The rps3-rpl16-nad3-rps12gene cluster in rice mitochondrial DNA is transcribed from alternative promoters. Curr. Genet. 27: 184–189.

    PubMed  Google Scholar 

  • Newton, K.L., Winberg, B., Yamato, K., Lupold, S. and Stern, D.B. 1995. Evidence for a novel mitochondrial promoter preceding the cox2 gene of perennial teosintes. EMBO J. 14: 585–593.

    PubMed  Google Scholar 

  • Nugent, J.M. and Palmer, J.D. 1991. RNA-mediated transfer of the gene coxIIfrom the mitochondrion to the nucleus during flowering plant evolution. Cell 66: 473–481.

    Article  PubMed  Google Scholar 

  • Pereira de Souza, A., Juvier, M.F., Delcher, E., Lancelin, D. and Lejeune, B. 1991. A trans-splicing model for the expression of the tripartite nad5gene in wheat and maize mitochondria. Plant Cell 3: 1363–1378.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Rapp, W.D., Lupold, D.S., Mack, S. and Stern, D.B. 1993. Architecture of the maize mitochondrial atp1promoter as determined by linker-scanning and point mutagenesis. Mol. Cell. Biol. 13: 7232–7238.

    PubMed  Google Scholar 

  • Ricard, B., Lejeune, B. and Araya, A. 1986. Studies on wheat mitochondrial DNA organization, comparison of mitochondrial DNA from normal and cytoplasmic male-sterile varieties of wheat. Plant Sci. 43: 141–149.

    Google Scholar 

  • Sambrook, J.E., Fritsch, F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Thomson, M.C., Macfarlane, J.L., Beagley, C.T. and Wolstenholme, D.R. 1994. RNA editing of mat-rtranscripts in maize and soybean increases similarity of the encoded protein to fungal and bryophyte group-II intron maturases: evidence that mat-rencodes a functional protein. Nucl. Acids Res. 22: 5745–5752.

    PubMed  Google Scholar 

  • Wahleithner, J.A., Macfarlane, J.L. and Wolstenholme, D.R. 1990. A sequence encoding a maturase-related protein in a group-II intron of a plant mitochondial nad1gene. Proc. Natl. Acad. Sci. USA 87: 548–552.

    PubMed  Google Scholar 

  • Wissinger, B., Schuster, W. and Brennicke, A. 1991. Trans-splicing in Oenotheramitochondria: nad1mRNAs are edited in exon and trans-splicing group-II intron sequences. Cell 65: 473–482.

    Article  PubMed  Google Scholar 

  • Xiong, Y. and Eickbush, T.H. 1988. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol. Biol. Evol. 5: 675–690.

    PubMed  Google Scholar 

  • Xiong, Y. and Eickbush, T.H. 1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9: 3353–3362.

    PubMed  Google Scholar 

  • Yao, W.B., Meng, B.Y., Tanaka, M. and Sugiura, M. 1989. An additional promoter within the protein-coding region of the psbDpsbCgene cluster in tobacco chloroplast DNA. Nucl. Acids Res. 17: 5745–5752.

    Google Scholar 

  • Zanlungo, S., Quiñ ones, V, Moenne, A., Holuigue, L. and Jordana, X. 1995. Splicing and editing of rps10transcripts in potato Mitochondria. Curr. Genet. 27: 565–571.

    PubMed  Google Scholar 

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Farré, JC., Araya, A. The mat-r open reading frame is transcribed from a non-canonical promoter and contains an internal promoter to co-transcribe exonsnad1e and nad5III in wheat mitochondria. Plant Mol Biol 40, 959–967 (1999). https://doi.org/10.1023/A:1006296422485

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