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Homeotic-like modification of stamens to petals is associated with aberrant mitochondrial gene expression in cytoplasmic male sterile OguraBrassica juncea

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Abstract

We have previously reported correction of severe leaf chlorosis in the cytoplasmic male sterile Ogura (also called Ogu)Brassica juncea line carrying Ogura cytoplasm by plastid substitution via protoplast fusion. Two cybrids obtained from the fusion experiment, Og1 and Og2, were green and carried the plastid genome ofB. juncea cv. RLM198. While Og1 displayed normal flower morphology comparable to that of its euplasmicB. juncea counterpart except for sterile anthers, Og2 retained homeotic-like floral modification of stamens to petal-like structures and several other floral deformities observed in the chlorotic (Ogu)B. juncea cv. RLM198 (or OgRLM). With respect to the mitochondrial genome, Og1 showed 81% genetic similarity to the fertile cultivar RLM while Og2 showed 93% similarity to OgRLM. In spite of recombination and rearrangements in the mitochondrial genomes in the cybrids, expression patterns of 10 out of 11 mitochondrial genes were similar in all the three CMS lines; the only exception wasatp6, whose expression was altered. While Og1 showed normalatp6 transcript similar to that in RLM, in Og2 and OgRLM weak expression of a longer transcript was detected. These results suggest that the homeotic-like changes in floral patterning leading to petaloid stamens in Og2 and OgRLM may be associated with aberrant mitochondrial gene expression.

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References

  • Bannerot H., Boulidard L., Couderon Y. and Temple J. (ed.) 1974 Transfer of cytoplasmic male sterility fromRaphanus sativus toBrassica oleracea. Wills A. B., Invergavrie, UK.

    Google Scholar 

  • Bellaoui M., Grelon M., Pelletier G. and Budar F. 1999 The restorerRfo 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.

    Article  PubMed  CAS  Google Scholar 

  • Belliard G., Vedei F. and Pelletier G. 1979 Mitochondrial recombination in cytoplasmic hybrids ofNicotiana tabacum by protoplast fusion.Nature 281, 401–403.

    Article  CAS  Google Scholar 

  • Bereterbide A., Hernould M., Farbos I., Glimelius K. and Mouras A. 2002 Restoration of stamen development and production of functional pollen in an alloplasmic CMS tobacco line by ectopic expression of theArabidopsis thaliana SUPERMAN gene.Plant J. 29, 607–615.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Duroc Y., Gaillard C., Hiard S., Defrance M. C., Pelletier G. and Budar F. 2005 Biochemical and functional characterization of ORF138, a mitochondrial protein responsible for Ogura cytoplasmic male sterility in Brassiceae.Biochimie 12, 1089–1100.

    Article  CAS  Google Scholar 

  • Farbos I., Mouras A., Bereterbide A. and Glimelius K. 2001 Defective cell proliferation in the floral meristem of alloplasmic plants ofNicotiana tabacum leads to abnormal floral organ development and male sterility.Plant J. 26, 131–142.

    Article  PubMed  CAS  Google Scholar 

  • Fitter J. T., Thomas M. R., Niu C. and Rose R. J. 2005 Investigation ofNicotiana tabacum (+)N. suaveolens cybrids with carpelloid stamens.J. Plant Physiol. 162, 225–235.

    Article  PubMed  CAS  Google Scholar 

  • Geddy R., Mahe L. and Brown G. G. 2005 Cell-specific regulation of aBrassica napus CMS-associated gene by a nuclear restorer with related effects on a floral homeotic gene promoter.Plant J. 41, 333–345.

    Article  PubMed  CAS  Google Scholar 

  • Gerstel D. J., Burns J. A. and Burk L. G. 1978 Cytoplasmic male sterility inNicotiana, restoration of fertility, and the nucleolus.Genetics 89, 157–169.

    PubMed  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-sterileBrassica cybrids.Mol. Gen. Genet. 243, 540–547.

    Article  PubMed  CAS  Google Scholar 

  • Howad W. and Kempken F. 1997 Cell type-specific loss of atp6 RNA editing in cytoplasmic male sterileSorghum bicolor.Proc. Natl. Acad. Sci. USA 94, 11090–11095.

    Article  PubMed  CAS  Google Scholar 

  • Kirti P. B., Banga S.S., Prakash S. and Chopra V. L. 1995a Transfer ofogu cytoplasmic male sterility toB. juncea and improvement of the male sterile line through somatic cell fusion.Theor. Appl. Genet. 91, 517–521.

    Article  CAS  Google Scholar 

  • Kirti P. B., Mohapatra T., Baldev A., Prakash S. and Chopra V. L. 1995b A stable cytoplasmic male sterile line ofBrassica juncea carrying restructured organelle genomes from the somatic hybrid ofTrachystoma balli + B. juncea.Plant Breed. 114, 434–438.

    Article  Google Scholar 

  • Kofer W., Glimelius K. and Bonnett H. T. 1991 Modifications of mitochondrial DNA cause changes in floral development in homeotic-like mutants of tobacco.Plant Cell 3, 759–769.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  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. 26, 935–946.

    Article  PubMed  CAS  Google Scholar 

  • Kumashiro T., Asahi T. and Nakakido F. 1989 Transfer of cytoplasmic factors by asymmetric fusion from a cross-incompatible species,Nicotiana repanda, toN. tabacum, and characterization of cytoplasmic genomes.Plant Sci. 61, 137–144.

    Article  Google Scholar 

  • Leino M., Teixeira R., Landgren M. and Glimelius K. 2003Brassica napus lines with rearrangedArabidopsis mitochondria display CMS and a range of developmental aberrations.Theor.Appl. Genet. 106, 1156–1163.

    CAS  Google Scholar 

  • Leino M., Landgren M. and Glimelius K. 2005 Alloplasmic effects on mitochondrial transcriptional activity and RNA turnover result in accumulated transcripts ofArabidopsis orfs in cytoplasmic male-sterileBrassica napus.Plant J. 42, 469–480.

    Article  PubMed  CAS  Google Scholar 

  • Linke B., Nothnagel T. and Borner T. 2003 Flower development in carrot CMS plants: mitochondria affect the expression ofMADS box genes homologous toGLOBOSA andDEFICIENS.Plant J. 34, 27–37.

    Article  PubMed  CAS  Google Scholar 

  • Makaroff C. A., Apel I. J. and Palmer J. D. 1989 The atp6 coding region has been disrupted and a novel reading frame generated in the mitochondrial genome of cytoplasmic male-sterile radish.J. Biol. Chem. 264, 11706–11713.

    PubMed  CAS  Google Scholar 

  • Makaroff C. A., Apel I. J. and Palmer J. D. 1990 Characterization of radish mitochondrialatpA: influence of nuclear background on transcription ofatpA -associated sequences and relationship with male sterility.Plant Mol. Biol. 15, 735–746.

    Article  PubMed  CAS  Google Scholar 

  • Makaroff C. A., Apel I. J. and Palmer J. D. 1991 The role ofcoxI- associated repeated sequences in plant mitochondrial DNA rearrangements and radish cytoplasmic male sterility.Curr. Genet. 19, 183–190.

    Article  PubMed  CAS  Google Scholar 

  • Murai K., Takumi S., Koga H. and Ogihara Y. 2002 Pistillody, homeotic transformation of stamens into pistil-like structures, caused by nuclear-cytoplasm interaction in wheat.Plant J. 29, 169–181.

    Article  PubMed  Google Scholar 

  • Nakajima Y., Yamamoto T., Muranaka T. and 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  PubMed  CAS  Google Scholar 

  • Nei M. and Li W. 1979 Mathematical model for studying genetic variation in terms of restriction endonucleases.Proc. Natl. Acad. Sci. USA 76, 5269–5273.

    Article  PubMed  CAS  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 

  • Pathania A., Bhat S. R., Dinesh Kumar V., Ashutosh, Kirti P. B., Prakash S. and Chopra V. L. 2003 Cytoplasmic male sterility in alloplasmicBrassica juncea carryingDiplotaxis catholica cytoplasm: molecular characterization and genetics of fertility restoration.Theor. Appl. Genet. 107, 455–461.

    Article  PubMed  CAS  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.

    Article  CAS  Google Scholar 

  • Polowick P. and Sawhney V. 1987 A scanning electron microscopic study on the influence of temperature on the expression of cytoplasmic male sterility inBrassica napus.Can. J. Bot. 65, 807–814.

    Google Scholar 

  • Polowick P. and Sawhney V. 1991 Microsporogenesis in a normal line and in the ogu cytoplasmic male-sterile line ofBrassica napus. II. The influence of intermediate and low temperatures.Sex. Plant Reprod. 4, 22–27.

    Article  Google Scholar 

  • Prakash S., Ahuja I., Upreti H. C., Dinesh Kumar V., Bhat S. R., Kirti P. B. and Chopra V. L. 2001 Expression of male sterility in alloplasmicBrassica juncea withErucastrum canariense cytoplasm and the development of a fertility restorer system.Plant Breed. 120, 479–482.

    Article  Google Scholar 

  • Sanger F., Nicklen S. and Coulson A. R. 1977 DNA sequencing with chain-terminating inhibitors.Proc. Natl. Acad. Sci. USA 74, 5463–5467.

    Article  PubMed  CAS  Google Scholar 

  • Song J. and Hedgecoth C. 1994 A chimeric gene (orf256) is expressed as protein only in cytoplasmic male sterile lines of wheat.Plant Mol. Biol. 26, 535–539.

    Article  PubMed  CAS  Google Scholar 

  • Teixeira R. T., Farbos I. and Glimelius K. 2005 Expression levels of meristem identity and homeotic genes are modified by nuclearmitochondrial interactions in alloplasmic male-sterile lines ofBrassica napus.Plant J. 42, 731–742.

    Article  PubMed  CAS  Google Scholar 

  • TheiΒen G. 2001 Development of floral organ identity: stories from the MADS house.Curr. Opin. Plant Biol. 4, 75–85.

    Article  Google Scholar 

  • Weigel D. and Meyerowitz E. M. 1993 Activation of floral homeotic genes inArabidopsis.Science 261, 1723–1726.

    Article  PubMed  CAS  Google Scholar 

  • Zubko M. K., Zubko E. I., Adler K., Grimm B. and Gleba Y. Y. 2003 New CMS-associated phenotypes in cybridsNicotiana tabacum L. (+Hyoscyamus niger L.).Ann. Bot. (London) 92, 281–288.

    Article  Google Scholar 

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Correspondence to P. B. Kirti.

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Meur, G., Gaikwad, K., Bhat, S.R. et al. Homeotic-like modification of stamens to petals is associated with aberrant mitochondrial gene expression in cytoplasmic male sterile OguraBrassica juncea . J Genet 85, 133–139 (2006). https://doi.org/10.1007/BF02729019

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  • DOI: https://doi.org/10.1007/BF02729019

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