Skip to main content
Log in

Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Uniparental activity of ribosomal RNA genes (rDNA) in interspecific hybrids is known as nucleolar dominance (ND). To see if difference in rDNA intergenic spacers (IGS) might be correlated with ND, we have used artificial Solanum allopolyploids and back-crossed lines. Combining fluorescence in situ hybridization and quantification of the level of the rRNA precursor by real-time PCR, we demonstrated that an expression hierarchy exists: In leaves, roots, and petals of the respective allopolyploids, rDNA of S lycopersicum (tomato) dominates over rDNA of S. tuberosum (potato), whereas rDNA of S. tuberosum dominates over that of the wild speciesS. bulbocastanum. Also in a monosomic addition line carrying only one NOR-bearing chromosome of tomato in a potato background the dominance effect was maintained. These results demonstrate that there is possible correlation between transcriptional dominance and number of conservative elements downstream of the transcription start in the Solanum rDNA. In anthers and callus tissues under-dominant rDNA was slightly (S. lycopersicum/S. tuberosum) or strongly (S. tuberosum/S. bulbocastanum) expressed indicating developmental modulation of ND. In leaves and petals, repression of the respective parental rDNA correlated with cytosine methylation at certain sites conserved in the IGS, whereas activation of under-dominant rDNA in anthers and callus tissues was not accompanied by considerable changes of the methylation pattern.

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

Access this article

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

  • Arumuganathan, K. and Earle, E.D. 1991. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9: 208–218.

    Google Scholar 

  • Bennett, R.I. and Smith, A.G. 1976. Nuclear DNA amounts in angiosperms. Phils. Trans. R. Soc. London B274: 227–274.

    Google Scholar 

  • Bennett, R.I. and Smith, A.G. 1991. The complete nucleotide sequence of the intergenic spacer region of an rDNA operon from Brassica oleracea and its comparison with other crucifers. Plant Mol. Biol. 16: 1095–1098.

    PubMed  Google Scholar 

  • Bhatia, S., Singth Negi, M. and Lakshmikumaran, M. 1996. Structural analysis of the rDNA intergenic spacer of Brassica nigra: evolutionary divergence of the spacers of the three diploid Brassica species. J. Mol. Evol. 43: 460–468.

    PubMed  Google Scholar 

  • Borisjuk, N., Borisjuk, L., Komarnytsky, S., Timeva, S., Hemleben, V., Gleba, Y. and Raskin, I. 2000. Tobacco ribosomal DNA spacer element stimulates amplification and expression of heterologous genes. Nat. Biotechnol. 18: 1303–1306.

    PubMed  Google Scholar 

  • Borisjuk, N., Borisjuk, L., Petjuch, G. and Hemleben, V. 1994. Comparison of nuclear ribosomal RNA genes among Solanum species and other Solanaceae. Genome 37: 271–279.

    PubMed  Google Scholar 

  • Borisjuk, N.V., Davidjuk, Y.M., Kostishin, S.S., Miroshnichenko, G.P., Velasco, R., Hemleben, V. and Volkov, R.A. 1997. Structural analysis of rDNA in the genus Nicotiana. Plant Mol. Biol. 35: 655–660.

    PubMed  Google Scholar 

  • Borisjuk. N. and Hemleben, V. 1993. Nucleotide sequence of potato rDNA intergenic spacer. Plant Mol. Biol. 21: 381–384.

    PubMed  Google Scholar 

  • Borisjuk, N.V., Momot, V.P. and Gleba Y. 1988. Novel class of rDNA repeat units in somatic hybrids between Nicotiana and Atropa. Theor. Appl. Genet. 76: 108–112.

    Google Scholar 

  • Busby, S.J. and Reeder, R.H. 1983. Spacer sequences regulate transcription of ribosomal gene plasmids injected into Xenopus embryos. Cell 34: 989–996.

    PubMed  Google Scholar 

  • Caudy, A.A. and Pikaard, C.S. 2002. Xenopus ribosomal RNA gene intergenic spacer elements conferring transcriptional enhancement and nucleolar dominance-like competition in oocytes. J. Biol. Chem. 277: 31577–31584.

    PubMed  Google Scholar 

  • Chen, Z.J., Comai, L. and Pikaard, C.S. 1998. Gene dosage and stochastic effects determine the severiti and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proc. Natl. Acad. Sci. USA 95: 14891–14896.

    PubMed  Google Scholar 

  • Chen, Z.J. and Pikaard, C.S. 1997a. Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev. 11: 2124–2136.

    PubMed  Google Scholar 

  • Chen, Z.J. and Pikaard, C.S. 1997b. Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/ silencing of progenitor rRNA genes is developmentally regulated in Brassica. Proc. Natl. Acad. Sci. USA 94: 3442–2447.

    PubMed  Google Scholar 

  • Cluster, P.D., Calderini, O., Puppilli, F., Crea, F., Damiani, F. and Arcioni, S. 1996. The fate of ribosomal genes in three interspecific somatic hybrids of Medicago sativa; three different outcomes including the rapid amplification of new spacer-length variants. Theor. Appl. Genet. 93: 801–808.

    Google Scholar 

  • Csink, A.K. and Henikoff, S. 1996. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381: 529–531.

    PubMed  Google Scholar 

  • Da Rocha, P.S. C.F. and Bertrand, H. 1995. Structure and comparative analysis of the rDNA intergenic spacer of Brassica rapa: implications for the function and evolution of the Cruciferae spacer. Eur. J. Biochem. 229: 550–557.

    PubMed  Google Scholar 

  • Doelling, J.H., Gaudino, R.J. and Pikaard, C.S. 1993. Functional analysis of Arabidopsis thaliana rRNA gene and spacer promoters in vivo and by transient expression. Proc. Natl. Acad. Sci. USA 90: 7528–7532.

    PubMed  Google Scholar 

  • Doelling, J.H. and Pikaard, C.S. 1995. The minimal ribosomal RNA gene promoter of Arabidopsis thaliana includes acritical element at the transcription initiation site.Plant J. 8:683–692.

    PubMed  Google Scholar 

  • Doelling, J.H. and Pikaard, C.S. 1996. Species-specificity of rRNA gene transcription in plants manifested as a switch in polymerase-specificity.Nucleic Acids Res. 24: 4725–4732.

    PubMed  Google Scholar 

  • Dover, G.A. and Flavell, R.V. 1984. Molecular co-evolution: rDNA divergence and the maintenance of function. Cell 38: 622–623.

    PubMed  Google Scholar 

  • Engel, J. 1997. Signifikante Schule der schlichten Statistik. Filander Verlag GmbH, Fu¨ rth, Germany.

    Google Scholar 

  • Fan, H., Kimitaka, Y., Miyanishi, M., Sugita, M. and Sugiura, M. 1995. In vitro transcription of plant RNA polymerase I-dependent rRNA genes is species-specific. Plant J 8: 295–298.

    PubMed  Google Scholar 

  • Flavell, R.B. 1986. The structure and control of expression of ribosomal RNA genes. Ox. Surv. Plant Mol. Cell Biol. 3: 252–274.

    Google Scholar 

  • Flavell, R.B., O'Dell, M. and Thompson, W.F. 1988. Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J. Mol. Biol. 204: 523–534.

    PubMed  Google Scholar 

  • Frieman, M., Chen, Z.J., Saez-Vasquez, J., Shen, L.A. and Pikaard, C.S. 1999. RNA polymerase I transcription in a Brassica interspecific hybrid and its progenitors: tests of transcription factor involvement in nucleolar dominance. Genetics 152: 451–460.

    PubMed  Google Scholar 

  • Ganal, M.W., Lapitan, N.L.V. and Tanksley, S.D. 1988. A molecular and cytogenetic survey of major repeated DNA sequences in tomato (Lycopersicon esculentum). Mol. Gen. Genet. 213: 262–268.

    Google Scholar 

  • Garriga-Caldere´, F., Huigen, D.J., Angrisano, A., Jacobsen, E. and Ramanna, M.S. 1998. Transmission of alien tomato chromosomes from BC1 to BC2 progenies derived from backcrossing potato(+)tomato fusion hybrids to potato: the selection of single additions for seven different tomato chromosomes. Theor. Appl. Genet. 96: 155–163.

    Google Scholar 

  • Garriga-Caldere´, F., Huigen, D.J., Filotico, F., Jacobsen, E. and Ramanna, M.S. 1997. Identification of alien chromosomes through GISH and RLFP analysis and the potential for the establishment of potato lines with monosomic additions of tomato chromosomes. Genome 40: 666–673.

    Google Scholar 

  • Gebhardt, C., Ritter, E., Barone, A., Debener, T., Walkemeier, B., Schachtschabel, U., Kaufmann, H., Thomson, R.D., Bonierbale, M.W., Ganal, M.W., Tanksley, S.D. and Salamini, F. 1991. RFLP maps of potato and their alignment with the homologous tomato genome. Theor. Appl. Genet. 83: 49–57.

    Google Scholar 

  • Georgiev, S., Papazova, N. and Gecheff, K. 2001. Transcriptional activity of an inversion split NOR in barley (Hordeum vulgare L.). Chromosome Res. 9: 507–514.

    PubMed  Google Scholar 

  • Grant, V. 1981. Plant Speciation, 2nd edn. Columbia University Press, New York.

    Google Scholar 

  • Gruenbaum, Y., Naveh-Many, T., Cedar, H. and Razin, A. 1981. Sequence specificity of methylation in higher plant DNA. Nature 292: 860–862.

    PubMed  Google Scholar 

  • Grummt, I. and Pikaard, C.S. 2003. Epigenetic mechanisms controlling RNA polymerase I transcription. Nat. Rev. Mol. Cell Biol. 4: 641–649.

    PubMed  Google Scholar 

  • Grummt, I., Roth, E. and Paule, M.R. 1982. rRNA transcription in vitro is species-specific. Nature 296: 173–174.

    PubMed  Google Scholar 

  • Gustafson, J.P., Dera, A.R. and Petrovic, S. 1988. Expression of modified rye ribosomal RNA genes in wheat. Proc. Natl. Acad. Sci. USA 85: 3943–3945.

    Google Scholar 

  • Heitz, E. 1931. Nucleolen und Chromosomen in der Gattung Vicia. Planta 15: 495–505.

    Google Scholar 

  • Hemleben, V., Ganal, M., Gerstner, J., Schiebel, K., Torres, R.A. 1988. Organization and length heterogeneity of plant ribosomal RNA genes. In: G. Kahl (Ed.), The Architecture of Eukaryotic Gene. VHC. Weinheim, pp. 371–384.

  • Honjo, T. and Reeder, R.H. 1973. Preferential transcription of Xenopus laevis ribosomal RNA in interspecific hybrids between Xenopus laevis and Xenopus mulleri. J. Mol. Biol. 80: 217–228.

    PubMed  Google Scholar 

  • Houchins, K., O'Dell, M., Flavell, R.B. and Gustafson, J.P. 1997. Cytosine methylation and nucleolar dominance in cereal hybrids. Mol. Gen. Genet. 55: 294–301.

    Google Scholar 

  • Izawa, T., Foster, R. and Chue, N.-H. 1993. Plant bZIP protein DNA binding specificity. J. Mol. Biol. 230: 1131–1144.

    PubMed  Google Scholar 

  • Jacobsen, E., De Jong, J.H., Kamstra; S.A., Van Den Berg, P.M. M.M. and Ramanna, M.S. 1995. Genomic in situ hybridization (GISH) and RFLP analysis for the identifi-cation of alien chromosomes in the backcross progeny of potato(+)tomato fusion hybrids. Heredity 74: 250–257.

    Google Scholar 

  • Kiss, T., Kis, M. and Solymosy, F. 1989a. Nucleotide sequence of a 25S rRNA gene from tomato. Nucleic Acids Res. 17: 796.

    PubMed  Google Scholar 

  • Kiss, T., Szkukalek, A. and Solymosy, F. 1989b. Nucleotide sequence of a 17S (18S) rRNA gene from tomato. Nucleic Acids Res. 17: 2127.

    PubMed  Google Scholar 

  • Labhart, P. and Reeder, R.H. 1984. Enhancer-like properties of the 60/81 bp elements in the ribosomal gene spacer of Xenopus laevis. Cell 37: 285–289.

    PubMed  Google Scholar 

  • Lawrence, R.J., Earley, K., Pontes, O., Silva, M., Chen, Z.J., Neves, N., Viegas, W. and Pikaard, C.S. 2004. A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol. Cell 13: 599–609.

    PubMed  Google Scholar 

  • Lee, H.S. and Chen, Z.J. 2001. Protein-coding genes are epigenetically regulated in Arabidopsis allopolyploids. Proc. Natl. Acad. Sci. 98: 6753–6758.

    PubMed  Google Scholar 

  • Levin, D.A. 2002. The Role of Chromosomal Change in Plant Evolution. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Lim, K.Y., Skalicka, K., Koukalova, B., Volkov, R.A., Matyasek, R., Hemleben, V., Leitch, A.R. and Kovarik, A. 2004. Dynamic changes in the distribution of a satellite homologous to intergenic 26–18S rDNA spacer in the evolution of Nicotiana. Genetics 166: 1935–1946.

    PubMed  Google Scholar 

  • Macleod, D. and Bird, A. 1982. DNAase I sensitivity and methylation of active versus inactive rRNA genes in xenopus species hybrids. Cell 29: 211–218.

    PubMed  Google Scholar 

  • McClintock, B. 1934. The relationship of a particular chromosomal element to the development of the nucleoli in Zea mays.Z. Zellforsch. Mikrosk. Anat. 21: 294–328.

    Google Scholar 

  • Mishima, Y., Financsek, I., Kominami, R. and Muramatsu, M. 1982. Fractionation and reconstitution of factors required for accurate transcription of mammalian ribosomal genes: identification of species-dependent initiation factor. Nucleic Acids Res. 10: 6659–6670.

    PubMed  Google Scholar 

  • Moss, T. 1983. A transcription function for the repetitive ribosomal spacer in Xenopus laevis. Nature 302: 223–228.

    PubMed  Google Scholar 

  • Mougey, E.B., Pape, L.K. and Sollner-Webb, B. 1996. J. Virtually the entire Xenopus laevis rDNA multikilobase intergenic spacer serves to stimulate polymerase I transcription. Biol. Chem. 271: 27138–27145.

    Google Scholar 

  • Murashige, T. and Skoog, F. 1962. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15: 437–497.

    Google Scholar 

  • Navashin, M. 1927. Changes in number and form of chromosomes as a result of hybridization. Z. Zellforsch. Mikrosk. Anat. 6: 195–223.

    Google Scholar 

  • Navashin, M. 1934. Chromosomal alterations caused by hybridization and their bearing upon certain general genetic problems. Cytologia 5: 169–203.

    Google Scholar 

  • Neves, N., Silva, M., Heslop-Harrison, J.S. and Viegas, W. 1997. Nucleolar dominance in triticales: control by unlinked genes. Chromosome Res. 5: 125–131.

    PubMed  Google Scholar 

  • Nicoloff, H. 1979. Nucleolar dominance is observed in barley translocation lines with specifically reconstructed SAT chromosomes. Theor. Appl. Genet. 55: 247–251.

    Google Scholar 

  • Niu, X.P., Renshaw-Gegg, L., Miller, L. and Guiltinan, M.J. 1999. Bipartite determinants of DNA-binding specificity of plant basic leucine zipper proteins. Plant Mol. Biol. 41: 1–13.

    PubMed  Google Scholar 

  • Oberwalder, B., Rouss, B., Schilde-Rentschler, L., Hemleben, V. and Ninnemann, H. 1997. Asymmetric fusion between wild and cultivated species of potato (Solanum spp.) – detection of asymmetric hybrids and genome elimination. Theor. Appl. Genet. 94: 1104–1112.

    Google Scholar 

  • Osborn, T.C., Pires, J.C., Birchler, J.A., Auger, D.L., Chen, Z.J., Lee, H.S., Comai, L., Madlung, A., Doerge, R.W., Colot, V. and Martienssen, R.A. 2003. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19: 141–147.

    PubMed  Google Scholar 

  • Papazova, N., Hvarleva, T., Atanassov, A. and Gecheff, K. 2001. The role of cytosine methylation for rRNA gene expression in reconstructed karyotypes of barley. Biotechnol. Equipment 15: 35–44.

    Google Scholar 

  • Pape, L.K., Windile, J.J., Mougey, E.B. and Sollner-Webb, B. 1989. The Xenopus ribosomal DNA 60-and 81-base-pair repeats are position-dependent enhancers that function at the establishment of the preinitiation complex: analysis in vivo and in an enhancer-responsive in vitro system. Mol. Cell Biol. 9: 5093–5104.

    PubMed  Google Scholar 

  • Perry, K.L. and Palukaitis, P. 1990. Transcription of tomato ribosomal DNA and the organization of the intergenic spacer. Mol. Gen. Genet. 221: 102–112.

    Google Scholar 

  • Pikaard, C.S. 2000. Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. Plant Mol. Biol. 43: 163–177.

    PubMed  Google Scholar 

  • Pikaard, C.S. and Reeder, R.H. 1988. Sequence elements essential for function of the Xenopus laevis ribosomal DNA enhancers. Mol. Cell Biol. 8: 4282–4288.

    PubMed  Google Scholar 

  • Reeder, R.H. 1985. Mechanisms of nucleolar dominance in animals and plants. J. Cell Biol. 101: 2013–2016.

    PubMed  Google Scholar 

  • Riddle, N.C. and Birchler, J.A. 2003. Effects of reunited diverged regulatory hierarchies in allopolyploids and species hybrids. Trends Genet. 19: 597–600.

    PubMed  Google Scholar 

  • Saez-Vasquez, J., Caparros-Ruiz, D., Barneche, F. and Echeverria, M. 2004. A plant snoRNP complex containing snoRNAs, fibrillarin, and nucleolin-like proteins is competent for both rRNA gene binding and pre-rRNA processing in vitro. Mol. Cell. Biol. 24: 7284–7297.

    PubMed  Google Scholar 

  • Saez-Vasquez, J. and Pikaard, C.S. 1997. Extensive purification of a putative RNA polymerase I holoenzyme from plants that accurately initiates rRNA gene transcription in vitro. Proc. Natl. Acad. Sci. USA 94: 11869–11874.

    PubMed  Google Scholar 

  • Sambrook, J., Fritsch, E. and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Santoro, R., Li, J. and Grummt, I. 2002. The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nature Genet. 32: 393–396.

    PubMed  Google Scholar 

  • Sardana, R., O'Dell, A. and Flavell, R. 1993. Correlation between the size of the intergenic regulatory region, the status of cytosine methylation of rRNA genes and nucleolar expression in wheat. Mol. Gen. Genet. 236: 155–162.

    PubMed  Google Scholar 

  • Schilde-Rentschler, L., Ruoss, B. and Ninnemann, H. 1993. Availability of new genetic resources from wild species for potato breeding. In: EAPR 12th Conference Trienniale, Paris, pp. 195–196.

  • Schlo¨ gelhofer, P., Nizhynska, V., Feik, N., Chambon, C., Potuschak, T., Wanzenbock, E.M., Schweizer, D. and Bachmair, A. 2002. The upstream Sal repeat-containing segment of Arabidopsis thaliana ribosomal DNA intergenic region (IGR) enhances the activity of adjacent proteincoding genes. Plant Mol. Biol. 49: 655–667.

    PubMed  Google Scholar 

  • Schmidt-Puchta, W., Gunther, I. and Sanger, H.L. 1989. Nucleotide sequence of the intergenic spacer (IGS) of the tomato ribosomal DNA. Plant Mol. Biol. 13: 251–253.

    PubMed  Google Scholar 

  • Schubert, I. and Kunzel, C. 1990. Position-dependent NOR activity in barley. Chromosoma 99: 352–359.

    Google Scholar 

  • Schwarzacher, T. and Heslop-Harrison, P. 2000. Practical In Situ Hybridization. The Bath Press, Bath, UK.

    Google Scholar 

  • Schweizer, G., Borisjuk, N., Borisjuk, L., Stadler, M., Stelzer, T., Schilde, L. and Hemleben, V. 1993. Molecular analysis of highly repeated genome fractions in Solanum and their use as markers for the characterization of species and cultivar. Theor. Appl. Genet. 85: 801–808.

    Google Scholar 

  • Stelzer, T. 1996. Vorkommen repetitiver DNA-Elemente und detaillierte Genomanalyse von somatischen Hybriden aus intra-und interspezifischen, symmetrischen Fusionen der Gattung Solanum. Ph.D. Dissertation, Verlag Ulrich E. Grauer, Sturttgart, Germany.

    Google Scholar 

  • Song, K., Lu, P., Tang, K. and Osborn, T.C. 1995. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. Proc. Natl. Acad. Sci. 92: 7719–7723.

    PubMed  Google Scholar 

  • Spooner, D.M., Anderson, G.J. and Jansen, R.K. 1993. Chloroplast DNA evidence for the interrelationships of tomatoes, potatoes, and pepinos (Solanaceae).Am. J. Bot. 80: 676–688.

    Google Scholar 

  • Stupar, R.M., Song, J., Tek, A.L., Cheng, Z., Dong, F. and Jiang, J. 2002. Highly condensed potato pericentromeric heterochromatin contains rDNA-related tandem repeats. Genetics 162: 1435–1444.

    PubMed  Google Scholar 

  • Tanksley, S.D., Ganal, M.W., Prince, J.P., De Vicente, M.C., Bonierbale, M.W., Broun, P., Fulton, T.M., Giovannoni, J.J., Grandillo, S., Martin, G.B., Messeguer, R., Miller, J.C., Miller, L., Paterson, A.H., Pineda, O., Ro¨ der, M.S., Wing, R.A., Wu, W. and Young, N.D. 1992. High density molecular linkage maps of the tomato and potato genomes. Genetics 132: 1141–1160.

    PubMed  Google Scholar 

  • Torres-Ruiz, R.A. and Hemleben, V. 1994. Pattern and degree of methylation in ribosomal RNA genes of Cucurbita pepo L. Plant Mol. Biol. 26: 1167–1179.

    PubMed  Google Scholar 

  • Tremousaygue, D., Laudie, M., Grellet, F. and Delseny, M. 1992. The Brassica oleracea rDNA spacer revisited. Plant Mol. Biol. 18: 1013–1018.

    PubMed  Google Scholar 

  • Vallejos, C.E., Tanksley, S.D. and Bernatzky, R. 1986. Localization in the tomato genome of DNA restriction fragments containing sequences homologous to the rRNA (45S), he major chlorophyll a/b binging polypeptide and the ribulosobisphosphate carboxylase genes. Genetics 112: 93–105.

    Google Scholar 

  • Viera, A., Mello-Sampayo, T. and Viegas, W.S. 1990a. Genetic control of 1R nucleolus organizer region in the presence of wheat genome. Genome 33: 713–718.

    Google Scholar 

  • Viera, A., Morais, L., Barao, A., Mello-Sampayo, T. and Viegas, W.S. 1990b. 1R chromosome nucleolus organizer region activation by 5-azacytidine in wheat · rye hybrids. Genome 33: 707–712.

    Google Scholar 

  • Visser, R., Hoekstra, R., Van der Leji, F., Witholt, B. and Feenstra, W. 1988. In situ hybridization to somatic metaphase chromosomes of potato. Theor. Appl. Genet. 76: 420–424.

    Google Scholar 

  • Volkov, R.A., Borisjuk, N.V., Panchuk, I.I., Schweizer, D. and Hemleben, V. 1999. Elimination and rearrangement of parental rDNA in allotetraploid Nicotiana tabacum. Mol. Biol. Evol. 16: 311–320.

    PubMed  Google Scholar 

  • Volkov, R.A., Zanke, C., Panchuk, I.I. and Hemleben, V. 2001. Molecular evolution of 5S rDNA of Solanum species (sect. Petota): application for molecular phylogeny and breeding. Theor. Appl. Genet. 103: 1273–1282.

    Google Scholar 

  • Volkov. R.A., Komarova, N.Y., Panchuk, I.I. and Hemleben, V. 2003a. Molecular evolution of rDNA external transcribed spacer and phylogeny of sect. Petota (genus Solanum) Mol. Phylogenet. Evol. 29: 187–202.

    PubMed  Google Scholar 

  • Volkov, R.A., Panchuk, I.I. and Scho¨ ffl, F. 2003b. Heat-stressdependency and developmental modulation of gene expression: the potential of house-keeping genes as internal standards in mRNA expression profiling using real-time RT-PCR. J. Exp. Bot. 391: 2343–2349.

    Google Scholar 

  • Volkov, R.A., Medina, F.J., Zentgraf, U. and Hemleben V. 2004. Molecular cell biology: Organization and molecular evolution of rDNA, nucleolar dominance, and nucleolus structure. In: Progress in Botany 65. Springer-Verlag, Berlin–Heidelberg, pp. 106–146.

    Google Scholar 

  • Wallace, H. and Langbridge, W.H.R. 1971. Differential amphiplasty and the control of ribosomal RNA synthesis.Heredity 27: 1–13.

    Google Scholar 

  • Wanzenbock, E.M., Schofer, C, Schweizer, D. and Bachmair, A. 1997. Ribosomal transcription units integrated via T-DNA transformation associate with the nucleolus and do not require upstream repeat sequences for activity in Arabidopsis thaliana. Plant J. 11: 1007–1016.

    PubMed  Google Scholar 

  • Wendel, J.F., Schnabel, A. and Seelanan, T. 1995. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium).Proc. Natl. Acad. Sci. 92: 280–284.

    PubMed  Google Scholar 

  • Xu, J. and Earle, E.D. 1996. High resolution physical mapping of 45S (5.8S, 18S and 25S) rDNA gene loci in the tomato genome using a combination of karyotyping and FISH of pachytene chromosomes. Chromosoma 104: 545–550.

    PubMed  Google Scholar 

  • Yeh, B.P. and Peloquin, S.J. 1965. The nucleolus associated chromosome of Solanum species and hybrids. Am. J. Bot. 52: 626.

    Google Scholar 

  • Zentgraf, U. and Hemleben, V. 1992. Complex formation of nuclear proteins with the spacer of Cucumis sativus ribosomal DNA. Nucl. Acids Res. 20: 3685–3691.

    PubMed  Google Scholar 

  • Zentgraf, U. and Hemleben, V. 1994. Structural organization and regulation of transcription by RNA polymerase I of plant nuclear ribosomal RNA genes. In: L. Nover (Ed.), Plant Promoters and Transcription Factors. Results and Problems in Cell Differentiation 20, Springer-Verlag, Berlin– Heidelberg, pp. 3–24.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Komarova, N.Y., Grabe, T., Huigen, D.J. et al. Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol Biol 56, 439–463 (2004). https://doi.org/10.1007/s11103-004-4678-x

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-004-4678-x

Navigation