Skip to main content
SpringerLink
Log in

The restorer Rfo gene acts post-translationally on the stability of the ORF138 Ogura CMS-associated protein in reproductive tissues of rapeseed cybrids

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

This paper describes the analysis of the effect of the restorer gene Rfo on the expression of the ORF138 protein associated with Ogura cytoplasmic male sterility (CMS) which has been engineered in rapeseed by protoplast fusion. We show that the presence of the Rfo gene in the genome of the plants decreases the amount of ORF138 protein in floral buds, this effect being the most dramatic in anthers at the stage of development when the sterile phenotype is normally expressed. However, the amount of orf138 transcripts is not affected by the Rfo gene in the same organs at the same stages. Total polysome analyses of buds and anthers show that the orf138 transcripts are translated with the same efficiency in sterile and restored plants. From these results we infer that the Rfo gene product acts on the post-translational stability of the ORF138 protein, leading to a decrease in the accumulation of the protein and a restoration of fertility.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abad, A.R., Mehrtens, B.J. and Mackenzie, S.A. 1995. Specific expression in reproductive tissues and fate of a mitochondrial sterility-associated protein in cytoplasmic male-sterile bean. Plant Cell 7: 271–285.

    Google Scholar 

  • Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. 1990. Current Protocols in Molecular Biology. Greene/Wiley-Interscience, New York.

    Google Scholar 

  • Bannerot, H., Boulidard, L., Cauderon, Y. and Tempé, J. 1974. Transfer of cytoplasmic male sterility from Raphanus sativus to Brassica oleracea. Proceedings EUCARPIA Crop Section Cruciferae 25: 52–54.

    Google Scholar 

  • Barkan, A., Walker, M., Nolasco, M. and Jonhson, D. 1994. A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 13: 3170–3181.

    Google Scholar 

  • Bellaoui, M., Pelletier, G. and Budar, F. 1997. The steady-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.

    Google Scholar 

  • Bonhomme, S., Budar, F., Férault, M. and Pelletier, G. 1991. A 2.5 kb NcoI fragment of Ogura radish mitochondrial DNA is correlated with cytoplasmic male-sterility in Brassica cybrids. Curr. Genet. 19: 121–127.

    Google Scholar 

  • Bonhomme, S., Budar, F., Lancelin, D., Small, I., Defrance, M.-C. and Pelletier, G. 1992. Sequence and transcript analysis of Nco2.5 Ogura specific fragment correlated with cytoplasmic male sterility in Brassica cybrids. Mol. Gen. Genet. 235: 240–248.

    Google Scholar 

  • Bonnet, A. 1975. Introduction et utilisation d'une stérilité mâle cytoplasmique dans des variétés précoces européennes de radis Raphanus sativus L. Ann. Amélior. Plantes 25: 381–397.

    Google Scholar 

  • Chase, C.D. 1994. Expression of CMS-unique and flanking mitochondrial DNA sequences in Phaseolus vulgaris L. Curr. Genet. 25: 245–251.

    Google Scholar 

  • Cui, X., Wise, R.P. and Schnable, P.S. 1996. The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science 272: 1334–1336.

    Google Scholar 

  • Damerval, C., De Vienne, D., Zivy, M. and Thiellement, H. 1986. Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7: 52–54.

    Google Scholar 

  • Delourme, R., Eber, F. and Renard, M. 1991. Radish cytoplasmic male sterility in rapeseed: breeding restorer lines with a good female fertility. In: 8th International Rapeseed Conference (Saskatoon, Saskatechewan, Canada), Vol. 5, p. 1056.

    Google Scholar 

  • Dewey, R.E., Timothy, D.H. and Levings CS III. 1987. A mitochondrial protein associated with cytoplasmic male sterility in the T cytoplasm of maize. Proc. Natl. Acad. Sci. USA 84: 5374–5378.

    Google Scholar 

  • Dill, C.L., Wise, R.P. and Schnable, P.S. 1997. Rf8 and Rf_ mediate unique T-urf13 transcript accumulation, revealing a conserved motif associated with RNA processing and restoration of pollen fertility in T-cytoplasm maize. Genetics 147: 1367–1379.

    Google Scholar 

  • Gourret, J., Delourme, R. and Renard, M. 1992. Expression of ogu cytoplasmic male sterility in cybrids of Brassica napus. Theor. Appl. Genet. 83: 549–556.

    Google Scholar 

  • Gray, M.W., Lang, B.F., Cedergren, R., Golding, G.B., Lemieux, C., Sankoff, D., Turmel, M., Brossard, N., Delage, E., Littlejohn, T.G., Plante, I., Rioux, P., Saint-Louis, D., Zhu, Y. and Burger, G. 1998. Genome structure and gene content in protist mitochondrial DNAs. Nucl. Acids Res. 26: 865–878.

    Google Scholar 

  • Grelon, M., Budar, F., Bonhomme, S. and Pelletier, G. 1994. Ogura cytoplasmic male-sterility (CMS)-associated orf138 is translated into a mitochondrial membrane polypeptide in male-sterile Brassica cybrids. Mol. Gen. Genet. 243: 540–547.

    Google Scholar 

  • He, S., Yu, Z.-H., Vallejos, C.E. and Mackenzie, S.A. 1995. Pollen fertility restoration by nuclear gene Fr in CMS common bean: an Fr linkage map and the mode of Fr action. Theor. Appl. Genet. 90: 1056–1062.

    Google Scholar 

  • Hernould, M., Suharsono, S., Litvak, S., Araya, A. and Mouras, A. 1993. Male-sterility induction in transgenic tobacco plants with an unedited atp9 mitochondrial gene from wheat. Proc. Natl. Acad. Sci. USA 90: 2370–2374.

    Google Scholar 

  • Heyn, F.W. 1976. Transfer of restorer genes from Raphanus to cytoplasmic male-sterile Brassica napus. Cruciferae Newsl. 1: 15–16.

    Google Scholar 

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

    Google Scholar 

  • Kennel, J.C. and Pring, D.R. 1989. Initiation and processing of atp6, T-urf13 and ORF221 transcripts from mitochondria of T cytoplasm of maize. Mol. Gen. Genet. 216: 16–24.

    Google Scholar 

  • Krishnasamy, S. and Makaroff, C.A. 1993. Characterization of the radish mitochondrial orfB locus: possible relationship with male sterility in Ogura radish. Curr. Genet. 24: 156–163.

    Google Scholar 

  • Krishnasamy, S. and Makaroff, C.A. 1994. Organ-specific reduction in the abundance of a mitochondrial protein accompanies fertility restoration in cytoplasmic male-sterile radish. Plant Mol. Biol. 32: 879–890.

    Google Scholar 

  • Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685.

    Google Scholar 

  • Li, X.Q., Jean, M., Landry, B.S. and Brown, G.G. 1998. Restorer genes for different forms of Brassica cytoplasmic male sterility map to a single nuclear locus that modifies transcripts of several mitochondrial genes. Proc. Natl. Acad. Sci. USA 95: 10032–10037.

    Google Scholar 

  • Monéger, F., Smart, C.J. and Leaver, J.C. 1994. Nuclear restoration of cytoplasmic male sterility in sunflower is associated with the tissue-specific regulation of a novel mitochondrial gene. EMBO J. 13: 8–17.

    Google Scholar 

  • Ogura, H. 1968. Studies on the new male sterility in Japanese radish, with special reference to the utilization of this sterility towards the practical raising of hybrid seeds. Mem. Fac. Agric. Kagoshima Univ. 6: 39–78.

    Google Scholar 

  • Pellan-Delourme, R. and Renard, M. 1988. Cytoplasmic male sterility in rapeseed (Brassica napus L.): female fertility of restored rapeseed with ‘Ogura’ and cybrid cytoplasms. Genome 30: 234–238.

    Google Scholar 

  • Pelletier, G., Primard, C., Vedel, F., Chétrit, P., Rémy, R., Rousselle, P. and Renard, M. 1983. Intergeneric cytoplasmic hybridization in Cruciferae by protoplast fusion. Mol. Gen. Genet. 191: 244–250.

    Google Scholar 

  • Pelletier, G., Primard, C., Vedel, F., Chétrit, P., Renard, M., Pellan-Delourme, R. and Mesquida, J. 1987. Molecular, phenotypic and genetic characterization of mitochondrial recombinants in rapeseed. In: 7th International Rapeseed Conference (Poznan, Poland), pp. 113–118.

  • Pring, D.R., Chen, W., Tang, H.V., Howad, W. and Kempken, F. 1998. Interaction of mitochondrial RNA editing and nucleolytic processing in the restoration of male fertility in sorghum. Curr. Genet. 33: 429–436.

    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.

    Google Scholar 

  • Rep, M. and Grivell, L.A. 1996. The role of protein degradation in mitochondrial function and biogenesis. Curr. Genet. 30: 367–380.

    Google Scholar 

  • Sarria, R., Lyznik, A., Vallejos, C.E. and Mackenzie, S.A. 1998. A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell 10: 1217–1228.

    Google Scholar 

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

    Google Scholar 

  • Singh, M., Hamel, N., Menassa, R., Li, X.-Q., Young, B., Jean, M., Landry, B.S. and Brown, G.G. 1996. Nuclear genes associated with a single Brassica CMS restorer locus influence transcripts of three different mitochondrial gene regions. Genetics 143: 505–516.

    Google Scholar 

  • Tang, H.V., Pring, D.R., Shaw, L.C., Salazar, R.A., Muza, F.R., Yan, B. and Schertz, K.F. 1996. Transcript processing internal to a mitochondrial open reading frame is correlated with fertility restoration in male-sterile sorghum. Plant J. 10: 123–133.

    Google Scholar 

  • Vierstra, R.D. 1996. Proteolysis in plants: mechanisms and functions. Plant Mol. Biol. 32: 275–302.

    Google Scholar 

  • Yamagishi, H. and Terachi, T. 1996. Molecular and biological studies on male-sterile cytoplasm in the Cruciferae. III. Distribution of Ogura-type cytoplasm among Japanese wild radishes and Asian radish cultivars. Theor. Appl. Genet. 93: 325–332.

    Google Scholar 

  • Yamagishi, H. and Terachi, T. 1997. Molecular and biological studies on male-sterile cytoplasm in the Cruciferae. IV. Ogura-type cytoplasm found in the wild radish, Raphanus raphanistrum. Plant Breed. 116: 323–329.

    Google Scholar 

Download references

Author information

Author notes

  1. Mohammed Bellaoui

    Present address: Department of Plant and Microbial Biology, University of California, 211 Koshland Hall, Berkeley, CA, 94720-3102, USA

Authors and Affiliations

  1. Station de Génétique et d'Amélioration des Plantes, INRA, route de Saint-Cyr, 78026, Versailles cedex, France

    Mathilde Grelon, Georges Pelletier & Françoise Budar

Authors
  1. Mohammed Bellaoui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mathilde Grelon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Georges Pelletier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Françoise Budar
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bellaoui, M., Grelon, M., Pelletier, G. et al. The restorer Rfo gene acts post-translationally on the stability of the ORF138 Ogura CMS-associated protein in reproductive tissues of rapeseed cybrids. Plant Mol Biol 40, 893–902 (1999). https://doi.org/10.1023/A:1006223908044

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1006223908044

Search

Navigation