Abstract
Alterations in mitochondrial gene expression and abnormal floral phenotypes, such as male sterility, characterize alloplasmic plants having the nucleus from Nicotiana tabacum combined with the cytoplasm from Nicotiana repanda. In all Nicotiana species investigated the mitochondrial atp1 gene is co-transcribed with the upstream orf274; however, unique for alloplasmic plants is a marked accumulation of these mitochondrial co-transcripts. In the present work, we show that a major component of the transcript difference is that in the alloplasmic male-sterile plants transcription initiates from novel sites internal to orf274. The sequences surrounding these initiation sites lack the CRTA consensus motif for plant mitochondrial promoters as well as similarity to other known plant mitochondrial promoters. Thus, initiation of transcription is under control of a mitochondrial promoter of a novel non-consensus type. This non-consensus promoter is inactivated when the fertility restoring heritable fragment chromosome from N. repanda is present in the N. tabacum nucleus of the alloplasmic plants. Our data suggest that the fertility-restoring fragment chromosome encodes a factor that represses initiation from this unusual promoter.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Antoshechkin, I. and Bogenhagen, D.F. 1995. Distinct roles for two purified factors in transcription of Xenopus mitochondria. Mol. Cell. Biol. 15: 7032-7042.
Bellaoui, M., Pelletier, G. and Budar F. 1997. The stady-state level of mRNA from the Ogura cytoplasmic male sterility locus in Brassica cybrids is determined post-transcriptionally by its 3' region. EMBO J. 16: 5057-5068.
Bergman, P., Edqvist, J., Farbos, I. and Glimelius, K. 2000. Male-sterile tobacco displays abnormal mitochondrial atp1 transcript accumulation and reduced floral ATP/ADP ratio. Plant Mol. Biol. 42: 531-544.
Binder, S. and Brennicke, A. 1993. Transcription initiation sites in mitochondria of Oenothera berteriana. J. Biol. Chem. 268: 7849-7855.
Binder, S., Marchfelder, A. and Brennicke, A. 1996. Regulation of gene expression in plant mitochondria. Plant Mol. Biol. 32: 303-314.
Boer, P.H. and Gray, M.W. 1986. The URF 5 gene of Chlamydomonas reinhardtii mitochondria: DNA sequence and mode of transcription. EMBO J. 5: 21-28.
Bonnett, H.T., Kofer, W., Håkansson, G. and Glimelius, K. 1991. Mitochondrial involvement in petal and stamen development studied by sexual and somatic hybridization of Nicotiana species. Plant Sci. 80: 119-130.
Braun, C.J., Brown, G.G., Levings, C.S. III and Hermann, R.G. 1992. Cytoplasmic male sterility. In: R.G. Hermann (Ed.) Cell Organelles: Plant Gene Research, Springer-Verlag, Vienna/New York, pp. 219-245.
Burk, L.G. 1967. An interspecific bridge-cross: Nicotiana repanda through N. sylvestris to N. tabacum. J. Hered. 58: 215-218.
Cermakian, N., Ikeda, T.M., Cedergren, R. and Gray, M.W. 1996. Sequence homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucl. Acids Res. 24: 648-654.
Chanut, F.A., Grabau, E.A. and Gesteland, R.F. 1993. Complex organization of the soybean mitochondrial genome: recombination repeats and multiple transcripts at the atpA loci. Curr. Genet. 23: 234-247.
Chase, C.D. 1994. Expression of CMS-unique and flanking mitochondrial DNA sequences in Phaseolus vulgaris L. Curr. Genet. 25: 245-251.
Clayton, D.A. 1992. Transcription and replication of animal mitochondrial DNAs. Int. Rev. Cytol. 141: 217-232.
Cooper, P., Butler, E. and Newton, K.J. 1990. The identification of a maize nuclear gene which influences the size and number of cox2 transcripts in mitochondria of perennial teosintes. Genetics 126: 461-467.
Dombrowski, S., Hoffmann, M., Guha, C. and Binder, S. 1999. Continuos primary sequence requirements in the 18-nucleotide promoter of dicot plant mitochondria. J. Biol. Chem. 274: 10094-10099.
Edqvist, J., Burger, G. and Gray, M.W. 2000. Expression of mitochondrial protein-coding genes in Tetrahymena pyriformis. J. Mol. Biol. 297: 381-393.
Fey, J. and Maréchal-Drouard, L. 1999a. Compilation and analysis of plant mitochondrial promoter sequences: an illustration of divergent evolution between monocot and dicot mitochondria. Biochem. Biophys. Res. Comm. 256: 409-414.
Fey, J. and Maréchal-Drouard, L. 1999b. Expression of two chloroplast-like tRNAAsn genes in potato mitochondria: mapping of transcription initiation sites present in the trnN1-trnY-nad2 cluster and upstream of trnN2. Curr. Genet. 36: 49-54.
Fisher, R.P. and Clayton, D.A. 1988. Purification and characterization of human mitochondrial transcription factor 1. Mol. Cell Biol. 8: 3496-3509.
Gerstel, D.U., Burns, J.A. and Burk, L.G. 1978. Cytoplasmic male sterility in Nicotiana, restoration of fertility, and the nucleolus. Genetics 89: 157-169.
Grill, S., Gualerzi, C.O., Londei, P. and Blasi, U. 2000. Selective stimulation of leaderless mRNA by initiation factor 2: evolutionary implications for translation. EMBO J. 19: 4101-4110.
Gray, M.W. and Lang, B.F. 1998. Transcription in chloroplasts and mitochondria: a tale of two polymerases. Trends Microbiol. 6: 1-3.
Hanson, M.R. 1991. Plant mitochondrial mutations and male sterility. Annu. Rev. Genet. 25: 461-486.
Hedtke, B., Börner, T. and Weihe, A. 1997. Mitochondrial and chloroplast phage-type RNA polymerases in Arabidopsis. Science 277: 809-811.
Håkansson, G. and Glimelius, K. 1991. Extensive nuclear influence on mitochondrial transcription and genome structure in malefertile and male-sterile alloplasmic Nicotiana materials. Mol. Gen. Genet. 229: 380-388.
Ikeda, T.M. and Gray, M.W. 1999. Characterization of a DNA-binding protein implicated in transcription in wheat mitochondria. Mol. Cell Biol. 19: 8113-8122.
Kennell, J.C., Wise, R.P. and Pring, D.R. 1987. Influence of nuclear background on transcription of a maize mitochondrial region associated with Texas male sterile cytoplasm. Mol. Gen. Genet. 210: 399-406.
Lisowsky, T. and Michaelis, G. 1988. A nuclear gene essential for mitochondrial replication suppresses a defect of mitochondrial transcription in Saccharomyces cerevisae. Mol. Gen. Genet. 214: 218-223.
Logemann, J., Schell, J. and Willmitzer, L. 1987. Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163: 16-20.
Mackenzie, S., He, S. and Lyznik, A. 1994. The elusive plant mitochondrion as a genetic system. Plant Physiol. 105: 775-780.
Masters, B.S., Stohl, L.L. and Clayton, D.A. 1987. Yeast mitochondrial RNA polymerase is homologous to those encoded by bacteriophages T3 and T7. Cell 51: 89-99.
Mulligan, R.M., Maloney, A.P. and Walbot, V. 1988. RNA processing and multiple transcription initiation sites result in transcript size heterogeneity in maize mitochondria. Mol. Gen. Genet. 211: 373-380.
Newton, K.J., 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.
Remacle, C. and Maréchal-Drouard, L. 1996. Characterization of the potato mitochondrial transcription unit containing 'native' trnS (GCU), trnF (GAA) and trnP (UGG). Plant Mol. Biol. 30: 553-563.
Sambrook, E., Fritsch, F. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Plainview, NY.
Sprengart, M.L., Fuchs, E. and Porter, A.G. 1996. The downstream box: an efficient and independent translation initiation signal in Escherichia coli. EMBO J. 15: 665-674.
Tracy, R.L and Stern, D.B. 1995. Mitochondrial transcription initiation: promoter structures and RNA polymerases. Curr. Genet. 28: 205-216.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Edqvist, J., Bergman, P. Nuclear identity specifies transcriptional initiation in plant mitochondria. Plant Mol Biol 49, 59–68 (2002). https://doi.org/10.1023/A:1014533023003
Issue Date:
DOI: https://doi.org/10.1023/A:1014533023003