Skip to main content
SpringerLink
Log in

Alloplasmic male sterility in Brassica napus (CMS 'Tournefortii-Stiewe') is associated with a special gene arrangement around a novel atp9 gene

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

To identify regions of the mitochondrial genome potentially involved in the expression of alloplasmic 'Tournefortii-Stiewe' cytoplasmic male sterility (CMS) in Brassica napus, transcripts of 25 mitochondrial genes were analysed in fertile and near isogenic male-sterile plants (BC8 generation). Differences were detected in the transcription of genes for subunit 9 of ATP synthase (atp9), cytochrome b (cob) and subunit 2 of NADH dehydrogenase (nad2). Structural analysis of these gene regions revealed differences in genome organisation around atp9 between male-sterile and fertile plants. Three atp9 genes, two of which were hitherto unknown, are present in the mitochondria of CMS plants, and rearrangements upstream of one of these genes have generated a chimeric 193-codon ORF, designated orf193. This region is transcribed as a CMS specific bi-cistronic mRNA of 1.58 kb comprising orf193 and atp9. The level of the aberrant 1.58-kb transcript is reduced in plants restored to fertility by as yet uncharacterized nuclear genes. orf193 encodes a polypeptide of 22.7 kDa which exhibits partial sequence identity to the subunit 6 of the ATP synthase complex. However, as it forms an uninterrupted ORF with one of the newly discovered atp9 genes it may also be translated as a chimeric 30.2-kDa protein. It is likely that either or both gene products interfere with the function or assembly of the mitochondrial F0F1-ATP synthase, thus impairing the highly ATP-dependent process of pollen development. The novel molecular features of alloplasmic 'Tournefortii-Stiewe' CMS are discussed with respect to the other known mechanisms of CMS in B. napus.

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

Fig. 1A, B.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

References

  • Bailey-Serres J, Hanson DK, Fox TD, Leaver CJ (1986) Mitochondrial genome rearrangement leads to extension and relocation of the cytochrome c oxidase subunit I gene in sorghum. Cell 47:567–576

    CAS  PubMed  Google Scholar 

  • Bellaoui M, Pelletier G, 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

    Article  CAS  PubMed  Google Scholar 

  • Bonhomme S, Budar F, Ferault M, Pelletier G (1991) A Nco I fragment of Ogura radish mitochondrial DNA is correlated with cytoplasmic male sterility in Brassica cybrids. Curr Genet 19:121–127

    CAS  Google Scholar 

  • Bonhomme S, Budar F, Lancelin D, Small I, Defrance MC, Pelletier G (1992) Sequence and transcript analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male sterility in Brassica cybrids. Mol Gen Genet 235:340–348

    CAS  PubMed  Google Scholar 

  • Brad AR, Merthens BJ, Mackenzie SA (1995) Specific expression in reproductive tissues and fate of a mitochondrial sterility-associated protein in cytoplasmic male-sterile bean. Plant Cell 7:271-285

    CAS  PubMed  Google Scholar 

  • Budar F, Pelletier G (2001) Male sterility in plants: occurrence, determinism, significance and use. C R Acad Sci III 324:543–50

    Article  CAS  PubMed  Google Scholar 

  • Canal L, Crouzillat D, Quetier F, Ledoigt G (2001) A transcriptional alteration on the atp9 gene is associated with a sunflower male-sterile cytoplasm. Theor Appl Genet 102:1185–1189

    Article  Google Scholar 

  • Devon RS, Porteous DJ, Brookes AJ (1995) Splinkerettes—improved vectorettes for greater efficiency in PCR walking. Nucleic Acids Res 23:1644–1645

    CAS  PubMed  Google Scholar 

  • Dewey RE, Levings CS, Timothy DH (1986) Novel recombinations in the maize mitochondrial genome produce a unique transcriptional unit in the Texas male-sterile cytoplasm. Cell 44:439–449

    CAS  PubMed  Google Scholar 

  • Ducos E, Touzet P, Boutry M (2001) The male sterile G cytoplasm of wild beet displays modified mitochondrial respiratory complexes. Plant J 26:171–180

    Article  CAS  PubMed  Google Scholar 

  • Engelke T, Tatlioglu T (2002) A PCR-marker for the CMS1 inducing cytoplasm in chives derived from recombination events affecting the mitochondrial gene atp9. Theor Appl Genet 104:698–702

    Article  Google Scholar 

  • Fang GH, McVetty PBE (1989) Inheritance of male fertility restoration and allelism of restorer genes for the Polima cytoplasmic male sterility system in oilseed rape. Genome 32:1044–1047

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Grelon M, Budar F, Bonhomme S, 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

    CAS  PubMed  Google Scholar 

  • Hakansson G, Glimelius K (1991) Extensive nuclear influence on mitochondrial transcription and genome structure in male-fertile and male-sterile alloplasmic Nicotiana materials. Mol Gen Genet 229:380–388

    CAS  PubMed  Google Scholar 

  • Handa H (1993) RNA editing of rapeseed mitochondrial atp9 transcript: RNA editing changes four amino acids, but termination codon is already encoded by genomic sequence. Jpn J Genet 68:47–54

    CAS  PubMed  Google Scholar 

  • Handa H, Mizobuchi-Fukuoka R, Pinyarat W (1997) The rapeseed mitochondrial gene for subunit 2 of the NADH dehydrogenase complex: a trans-spliced structure is conserved in one of the smallest plant mitochondrial genomes. Curr Genet 31:336–342

    Article  CAS  PubMed  Google Scholar 

  • Horn R, Köhler RH, Zetsche K (1991) A mitochondrial 16 kDa protein is associated with cytoplasmic male sterility in sunflower. Plant Mol Biol 17:29–36

    CAS  PubMed  Google Scholar 

  • Iwabuchi M, Kyozuka J, 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

    CAS  PubMed  Google Scholar 

  • Kadowaki K, Suzuki T, Kazama S (1990) A chimeric gene containing the 5′ portion of atp6 is associated with cytoplasmic male-sterility of rice. Mol Gen Genet 224:10–16

    CAS  PubMed  Google Scholar 

  • Köhler RH, Horn R, Lössl A, Zetsche K (1991) Cytoplasmic male sterility in sunflower is correlated with the co-transcription of a new open reading frame with the atpA gene. Mol Gen Genet 227:369–376

    Google Scholar 

  • Landgren M, Zetterstrand M, Sundberg E, Glimelius K (1996) Alloplasmic male-sterile Brassica lines containing B. tournefortii mitochondria express an ORF3′ of the atp6 gene and a 32 kDa protein. Plant Mol Biol 32 5:879–890

    Google Scholar 

  • Mackenzie SA, Chase CD (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

    Article  CAS  PubMed  Google Scholar 

  • Mathias R (1985) Transfer of cytoplasmic male sterility from brown mustard ( Brassica juncea L.) into rapeseed ( Brassica napus L.). Z Pflanzenzüchtung 95:371–374

  • Mihr C, Baumgärtner M, Dieterich JH, Schmitz UK, Braun HP (2001) Proteomic approach for investigation of cytoplasmic male steriltiy (CMS) in Brassica. J Plant Physiol 158:787–794

    CAS  Google Scholar 

  • Moneger F, Smart CJ, Leaver CJ (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

    PubMed  Google Scholar 

  • Nakajima Y, Yamamoto T, Muranaka T, Oeda K (2001) A novel orfB -related gene of carrot mitochondrial genomes that is associated with homeotic cytoplasmic male sterility (CMS). Plant Mol Biol 46:99–107

    Article  CAS  PubMed  Google Scholar 

  • Paulmann W, Röbbelen G (1988) Effective transfer of cytoplasmic male sterility from radish (Raphanus sativus L.) to rape (Brassica napus L.) Plant Breeding 100:299–309

    Google Scholar 

  • Pelletier G, Primard C, Vedel F, Chetrit P, Remy R, Rouselle P, Renard M (1983) Intergenetic cytoplasmic hybridization in Cruciferae by protoplast fusion. Mol Gen Genet 191:244-250

    CAS  Google Scholar 

  • Pradhan AK, Mukhopadhyay A, Pental D (1991) Identification of the putative cytoplasmic donor of a CMS system in Brassica juncea. Plant Breeding 106:204-208

    Google Scholar 

  • Rawat DS, Anand IJ (1979) Male sterility in Indian mustard. Indian J Genet Plant Breed 39:412–414

    Google Scholar 

  • Sakamoto W, Tan SH, Murata M, Motoyoshi F (1997) An unusual mitochondrial atp9-rpl16 cotranscript found in the maternal distorted leaf mutant of Arabidopsis thaliana: Implication of GUG as an initiation codon in plant mitochondria. Plant Cell Physiol 38:975–979

    CAS  PubMed  Google Scholar 

  • Sarria R, Lyznik A, Vallejos CE, Mackenzie SA (1998) A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated. Plant Cell 10:1217–1228

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Hsia AP, Nikolaus BJ (1998) Genetic recombination in plants. Curr Opin Plant Biol 1:123–129

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sodhi YS, Pradhan AK, Verma JK, Arumugam N, Mukhopadhyay, Pental D (1994) Identification and inheritance of Fertility Restorer genes for 'tour' CMS in rapeseed ( Brassica napus L). Plant Breeding 112:223–227

    Google Scholar 

  • Stiewe G, Röbbelen G (1994) Establishing cytoplasmic male sterility in Brassica napus by mitochondrial recombination with B. tournefortii. Plant Breeding 113:294–304

    CAS  Google Scholar 

  • Stiewe G, Witt U, Hansen S, Theis R, Abel WO, Röbbelen G (1995) Natural and experimental evolution of CMS for rapeseed breeding. Adv Plant Breeding 18:59–76

    Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61

    CAS  PubMed  Google Scholar 

  • Warmke HE, Sheu-Ling JL (1978) Pollen abortion in T cytoplasmic male-sterile corn ( Zea mays): a suggested mechanism. Science 200:561–563

    CAS  Google Scholar 

  • Ye F, Bernhardt J, Abel WO (1993) Genes for ribosomal proteins S3, L16, L5 and S 14 are clustered in the mitochondrial genome of Brassica napus L. Curr Genet 24:323–9

    CAS  PubMed  Google Scholar 

  • Young EG, Hanson MR (1987) A fused mitochondrial gene associated with cytoplasmic male sterility is developmentally regulated. Cell 50:41–49

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We wish to thank Drs. H. Becker, G. Stiewe, W. Ecke and C. Möllers, Göttingen, for providing plant material of B. napus and to Dr. Albaum, Hamburg, for providing B. napus CMS 'Juncea' plants. Thanks are also due to D. Lewejohann for expert technical assistance. All the experiments described in this paper comply with the current laws of Germany. This work was supported by a grant from the Deutsche Forschungsgemeinschaft (Schm 698/8-2) to UKS and a grant from the Fonds der Chemischen Industrie to HPB

Author information

Author notes

  1. J.-H. Dieterich

    Present address: Max-Planck-Institut for Molecular Plant Physiology, Am Mühlenberg 1, 14476, Golm, Germany

Authors and Affiliations

  1. Institut für Angewandte Genetik, Universität Hannover, Herrenhäuser Str. 2, 30419, Hannover, Germany

    J.-H. Dieterich, H.-P. Braun & U. K. Schmitz

Authors
  1. J.-H. Dieterich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H.-P. Braun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. U. K. Schmitz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H.-P. Braun.

Additional information

Communicated by R. Hagemann

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dieterich, JH., Braun, HP. & Schmitz, U.K. Alloplasmic male sterility in Brassica napus (CMS 'Tournefortii-Stiewe') is associated with a special gene arrangement around a novel atp9 gene. Mol Gen Genomics 269, 723–731 (2003). https://doi.org/10.1007/s00438-003-0886-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-003-0886-3

Keywords

Search

Navigation