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Cytoplasmic male sterility in hybrids of sterile wild beet (Beta vulgaris ssp. maritima) and O-type fertile sugar beet (Beta vulgaris L.): molecular analysis of mitochondrial and nuclear genomes

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Abstract

The organization of the mitochondrial genome of B3, B4 and B5generations of hybrids created by backcrossing sterile wild beet Betamaritima with a fertile O-type sugar beet line was studied usingrestriction fragment length polymorphism (RFLP) analysis. Random amplifiedpolymorphic DNA (RAPD) analysis was used to study restoration of the fertile(O-type) sugar beet genotype in hybrids after multiple backcrossings.Restriction of mtDNAs from the cytoplasm of B. maritimaandhybrids revealed BamHI, EcoRI andXhoI restriction patterns different from those for sterileand fertile sugar beet lines. The most conspicuous feature of our accession ofsterile wild beet mtDNA was the absence of the 10.7-kbEcoRI fragment detected in the cytoplasm of S-type sterileB. maritima and sugar beet. The hybridization of digestedmtDNAs with coxII, atpA andatp6 homologous probes revealed alterations within thesegene loci that distinguished wild beet and hybrids from sugar beets.Characteristic hybridization profiles for the wild beet and B3, B4 and B5hybrids were observed for all probes regardless of the restrictase used todigest mtDNA. Notable changes in atpA andatp6 genes resulted when probes that comprised the5′flanking sequences of these genes and a small part of the coding sequences wereused. RFLP analysis of the sterile B. maritimamitochondrial genome further supported the unique character of this source ofwild beet sterility. The genotypic differences between hybrids and parentalaccessions were determined by scoring PCR-RAPD reaction products for nineselected primers. The diversity of the B. maritimagenotyperesulted in a lower genetic similarity index in comparison with hybrids,sterileand fertile lines of sugar beet. The dendrogram obtained after cluster analysisdistinguished hybrids as a group that differed from wild beet and themaintainersugar beet line used for backcrossing. These results may indicate incompleterestoration of the fertile sugar beet genotype in hybrids.

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References

  • Boutin V., Pannenbecker G., Ecke W., Schewe G., Saumitou-Laprade P., Jean R. et al. 1987. Cytoplasmic male sterility and nuclear restorer genes in a natural population of Beta maritima: genetical and molecular aspects. Theor. Appl. Genet. 73: 625–629.

    Google Scholar 

  • Brears T., Curtis G.J. and Lonsdale D.M. 1989. A specific rearrangement of mitochondrial DNA induced by tissue culture. Theor. Appl. Genet. 77: 620–624.

    Google Scholar 

  • Coe G.E. and Stewart D. 1977. Cytoplasmic male sterility, self fertility, and monogermness in Beta maritima L. Am. Soc. Sugar Beet Technol. 19: 257–261.

    Google Scholar 

  • Dalke L. and Szota M. 1993. Utilizing Male Sterility from Beta maritima in Sugarbeet Breeding. Am. Soc. Sugar Beet Technol. 30: 253–260.

    Google Scholar 

  • Davis L.G., Dibner M.D. and Leder J.F. 1986. Basic Methods in Molecular Biology. Elsevier Science Publishing, 42–43.

  • Desplanque B., Viard F., Bernard J., Forcioli D., Saumitou-Laprade P., Cuguen J. et al. 2000. The linkage disequilibrium between chloroplast DNA and mitochondrial DNA haplotypes in Beta vulgaris ssp. maritima (L.): the usefulness of both genomes for population genetic studies. Mol. Ecol. 9: 141–154.

    Google Scholar 

  • Dikalova A.E., Dudarewa N.A., Kubalkova M. and Salganik R.I. 1993. Rearrangements in sugar beet mitochondrial DNA induced by cell suspension, callus cultures and regeneration. Theor. Appl. Genet. 86: 699–704.

    Google Scholar 

  • Duchenne M., Lejune B., Fouillard P. and Quetier F. 1989. Comparison of the organization and expression of mtDNA of fertile and male-sterile sugar beet varieties (Beta vulgaris L). Theor. Appl. Genet. 78: 633–640.

    Google Scholar 

  • Ducos E., Touzet P., Saumitou-Laprade P. and Vernet P. 2001. Nuclear effect on mitochondrial protein expression of the CMS Owen cytoplasm in sugar beet. Theor. Appl. Genet. 102: 1299–1304.

    Google Scholar 

  • Dudarewa N.A., Veprev S.G., Popovsky A.V., Maletsky S.I., Gileva I.P. and Salganik R.I. 1990. High-rate spontaneous reversion to cytoplasmic male sterility in sugar beet: a characterization of the mitochondrial genomes. Theor. Appl. Genet. 79: 817–824.

    Google Scholar 

  • Halldén C., Bryngelsson T. and Bosemark N.O. 1988. Two new types of cytoplasmic male sterility found in wild Beta beets. Theor. Appl. Genet. 75: 561–568.

    Google Scholar 

  • Halldén C., Lind C., Säll T., Bosemark N.O. and Bengtsson B.O. 1990. Cytoplasmic male sterility in Beta is associated with structural rearrangements of the mitochondrial DNA and is not due to interspecific organelle transfer. J. Mol. Evol. 31: 365–372.

    Google Scholar 

  • Hanson M.R. 1991. Plant mitochondrial mutations and male sterility. Annu. Rev. Genet. 25: 461–486.

    Google Scholar 

  • Jassem B. 1985. Variation of maritime beet (Beta maritima L.) from Brittany. Gen. Pol. 26: 463–469.

    Google Scholar 

  • Jung C., Pillen K., Frese L. and Melchinger A.E. 1993. Phylogenetic relationships between cultivated and wild species of the genus Beta revealed by DNA "fingerprinting". Theor. Appl. Genet. 86: 449–457.

    Google Scholar 

  • Kinoshita T. 1976. Genetical studies on cytoplasmic male sterility induced by gamma ray irradiation in sugar beets. Jpn. J. Breed. 26: 256–265.

    Google Scholar 

  • Kinoshita T., Takahashi M. and Mikami T. 1982. Cytoplasmic mutation of male sterility induced by chemical mutagens in sugar beets. Proc. Jpn. Acad. Ser. B 58: 319–322.

    Google Scholar 

  • Kubo T., Nishizawa S. and Mikami T. 1999. Alterations in organization and transcription of the mitochondrial genome of cytoplasmic male sterile sugar beet (Beta vulgaris L.). Mol. Gen. Genet. 262: 283–290.

    Google Scholar 

  • Kubo T., Satoh Y., Muro T., Kinoshita T. and Mikami T. 1995. Physical and gene organization of mitochondrial DNA from the fertile cytoplasm of sugar beet (Beta vulgaris L.). Curr. Genet. 28: 235–241.

    Google Scholar 

  • Laporte V., Merdinoglu D., Saumitou-Laprade P., Butterlin G., Vernet P. and Cuguen J. 1998. Identification and mapping of RAPD and RFLP markers linked to a fertility restorer gene for a new source of cytoplasmic male sterility in Beta vulgaris ssp. maritima. Theor. Appl. Genet. 96: 989–996.

    Google Scholar 

  • Levings C.S. and Siedow J.N. 1992. Molecular basis of disease susceptibility in the Texas cytoplasm of maize. Plant. Mol. Biol. 19: 135–147.

    Google Scholar 

  • Makaroff C.A. and Palmer J.D. 1989. Mitochondrial DNA rearrangements and transcriptional alterations in male-sterile cytoplasm of Ogura radish. Mol. Cell Biol. 8: 1474–1480.

    Google Scholar 

  • Manniatis T., Fritsch E.F. and Sambrook J. 1982. Molecular Cloning. Cold Spring Harbor Laboratory, New York, 109–112.

    Google Scholar 

  • Mann V., McIntosh L., Theurer C. and Hirschberg J. 1989. A new cytoplasmic male sterile genotype in the sugar beet Beta vulgaris L.: a molecular analysis. Theor. Appl. Genet. 78: 293–297.

    Google Scholar 

  • Mann V., Ekstein I., Nissen H., Hiser C., McIntosh L. and Hirschberg J. 1991. The cytochrome oxidase II gene in mitochondria of the sugar-beet Beta vulgaris L. Plant Mol. Biol. 17: 559–566.

    Google Scholar 

  • McGrath J.M., Derico C.A. and Yu Y. 1999. Genetic diversity in selected, historical US sugarbeet germplasm and Beta vulgaris ssp. maritima. Theor. Appl. Genet. 98: 968–976.

    Google Scholar 

  • Mikami T., Harada T., Kishima Y., Sugiura M. and Kinoshita T. 1986. Variation in organelle genome organization associated with male sterile cytoplasms in sugar beet. Gamma Field Symposia 25: 131–149.

    Google Scholar 

  • Nei M. and Li W.H. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. 79: 5269–5273.

    Google Scholar 

  • Onodera Y., Yamamoto M.P., Kubo T. and Mikami T. 1999. Heterogeneity of the atp6 presequences in normal and different sources of male-sterile cytoplasms of sugar beet. J. Plant Physiol. 155: 656–660.

    Google Scholar 

  • Owen F.V. 1945. Cytoplasmically inherited male-sterility in sugar beet. J. Agr. Res. 71: 423–440.

    Google Scholar 

  • Powling A. and Ellis T.H.N. 1983. Studies on the organelle genomes of sugarbeet with male-fertile and male-sterile cytoplasms. Theor. Appl. Genet. 65: 323–328.

    Google Scholar 

  • Rohlf F.J. 1989. NTSYS-pc Numerical Taxonomy and Multivariate Analysis System. vs 1.50. Exeter Publ. LTD, Setauket, NY, USA.

    Google Scholar 

  • Saumitou-Laprade P., Rouwendal G.J.A., Cuguen J., Krens F.A. and Michaelis G. 1993. Different CMS sources found in Beta vulgaris ssp. maritima: mitochondrial variability in wild populations revealed by a rapid screening procedure. Theor. Appl. Genet. 85: 529–535.

    Google Scholar 

  • Sadoch Z. and Goc A. 1997. Molecular characterization of fertile and sterile cytoplasm in Beta spp. Plant Breeding 116: 409–414.

    Google Scholar 

  • Senda M., Harada T., Mikami T., Sagiura M. and Kinoshita T. 1991. Genomic organization and sequence analysis of the cytochrome oxidase subunit II gene from normal and male-sterile mitochondria in sugar beet. Curr. Genet. 19: 175–181.

    Google Scholar 

  • Senda M., Onodera Y. and Mikami T. 1998. Recombination events across the atpA-associated repeated sequences in the mitochondrial genomes of beets. Theor. Appl. Genet. 96: 964–968.

    Google Scholar 

  • Szklarczyk M., Oczkowski M., Augustyniak H., Börner T., Linke B. and Michalik B. 2000. Organisation and expression of mitochondrial atp9 genes from CMS and fertile carrots. Theor. Appl. Genet. 100: 263–270.

    Google Scholar 

  • Wilson A.J. and Chourey P.S. 1984. A rapid inexpensive method for the isolation of restrictable mitochondrial DNA from various plant sources. Plant Cell Reports 3: 237–239.

    Google Scholar 

  • Xue Y., Collin S., Davies D.R. and Thomas C.M. 1994. Differential screening of mitochondrial cDNA libraries from male-fertile and cytoplasmic male-sterile sugar-beet reveals genome rearrangements at atp6 and atpA loci. Plant Mol. Biol. 25: 91–103.

    Google Scholar 

  • Yesodi V., Hauschner H., Tabib Y. and Firon N. 1997. An intact F1ATPase α-subunit gene and a pseudogene with differing genomic organization are detected in both male-fertile and CMS petunia mitochondria. Curr. Genet. 32: 348–357.

    Google Scholar 

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Sadoch, Z., Goc, A., Wierzchosławski, R. et al. Cytoplasmic male sterility in hybrids of sterile wild beet (Beta vulgaris ssp. maritima) and O-type fertile sugar beet (Beta vulgaris L.): molecular analysis of mitochondrial and nuclear genomes. Molecular Breeding 11, 137–148 (2003). https://doi.org/10.1023/A:1022450430434

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