Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids
Language English Country Great Britain, England Media print
Document type Journal Article, Research Support, Non-U.S. Gov't
- MeSH
- Transcription, Genetic MeSH
- Genome, Plant MeSH
- Genes, rRNA * MeSH
- Polyploidy * MeSH
- DNA, Ribosomal genetics MeSH
- RNA, Plant genetics MeSH
- Nicotiana genetics MeSH
- Gene Silencing MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Ribosomal MeSH
- RNA, Plant MeSH
This paper establishes relationships between two aspects of ribosomal DNA (rDNA) biology: epigenetic silencing of rDNA loci; and homogenization leading to concerted evolution. Here, we examined rDNA inheritance and expression patterns in three natural Nicotiana allopolyploids (closest living descendants of diploid parents are given), N. rustica (N. paniculata x N. undulata), N. tabacum (N. sylvestris x N. tomentosiformis) and N. arentsii (N. undulata x N. wigandioides), and synthetic F(1) hybrids and allopolyploids. The extent of interlocus rDNA homogenization decreased in the direction N. arentsii > N. tabacum > N. rustica. The persistence of parental rDNA units in one of the subgenomes was associated with their transcription inactivity and likely heterochromatization. Of synthetic hybrids and polyploids only N. paniculata x N. undulata showed strong uniparental transcriptional silencing of rDNA triggered already in F(1). Epigenetic patterns of expression established early in allopolyploid nucleus formation may render units susceptible or resistant to homogenization over longer time-frames. We propose that nucleolus-associated transcription leaves rDNA units vulnerable to homogenization, while epigenetically inactivated units, well-separated from the nucleolus, remain unconverted.
Institute of Biophysics Academy of Sciences of the Czech Republic Brno CZ 61265 Czech Republic
School of Biological and Chemical Sciences Queen Mary University of London London E1 4NS UK
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Adams KL, Wendel JF. 2005. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology 8: 135-141.
Aguilera A. 2002. The connection between transcription and genomic instability. EMBO Journal 21: 195-201.
Alvarez I, Wendel JF. 2003. Ribosomal ITS sequences and plant phlyogenetic inference. Molecular Phylogenetics and Evolution 29: 417-434.
Bennett RI, Smith AG. 1991. Use of a genomic clone for ribosomal RNA from Brassica oleracea. RFLP analysis of Brassica species. Plant Molecular Biology 16: 685-688.
Borisjuk NV, Davidjuk YM, Kostishin SS, Miroshnichenco GP, Velasco R, Hemleben V, Volkov RA. 1997. Structural analysis of rDNA in the genus Nicotiana. Plant Molecular Biology 35: 655-660.
Burk LG. 1973. Partial self-fertility in a theoretical amphiploid progenitor of N. tabacum. Journal of Heredity 64: 348-350.
Chase MW, Knapp S, Cox AV, Clarkson JJ, Butsko Y, Joseph J, Savolainen V, Parokonny AS. 2003. Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). Annals of Botany (London) 92: 107-127.
Chen ZJ, Ni Z. 2006. Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. Bioessays 28: 240-252.
Chen ZJ, Pikaard CS. 1997a. Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica. Proceedings of the National Academy of Sciences, USA 94: 3442-3447.
Chen ZJ, Pikaard CS. 1997b. Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes and Development 11: 2124-2136.
Chen ZJ, Comai L, Pikaard CS. 1998. Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proceedings of the National Academy of Sciences, USA 95: 14891-14896.
Clarkson JJ, Lim KY, Kovarík A, Chase MW, Knapp S, Leitch AR. 2005. Long-term genome diploidization in allopolyploid Nicotiana section Repandae (Solanaceae). New Phytologist 168: 241-252.
Cluster PD, Calderini O, Pupilli F, Crea F, Damiani F, 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. Theoretical and Applied Genetics 93: 801-808.
Earley K, Lawrence RJ, Pontes O, Reuther R, Enciso AJ, Silva M, Neves N, Gross M, Viegas W, Pikaard CS. 2006. Erasure of histone acetylation by Arabidopsis HDAC6 mediates large-scale gene silencing in nucleolar dominance. Genes and Development 20: 1283-1293.
Fan H, Yakura K, Miyanishi M, Sugita M, Sugiura M. 1995. In vitro transcription of plant RNA polymerase I-dependent rRNA genes is species-specific. Plant Journal 8: 295-298.
Flavell RB. 1989. Variation in structure and expression of ribosomal DNA loci in wheat. Genome 31: 963-968.
Flowers JM, Burton RS. 2006. Ribosomal RNA gene silencing in interpopulation hybrids of Tigriopus californicus: nucleolar dominance in the absence of intergenic spacer subrepeats. Genetics 173: 1479-1486.
Fulnecek J, Matyasek R, Kovarík A, Bezdek M. 1998. Mapping of 5-methylcytosine residues in Nicotiana tabacum 5S rRNA genes by genomic sequencing. Molecular and General Genetics 259: 133-141.
Gerlach WL, Bedbrook JR. 1979. Cloning and characterization of ribosomal RNA genes in wheat. Nucleic Acids Research 7: 1869-1885.
Hemleben V, Zentgraf U. 1994. Structural organisation and regulation of transcription by RNA polymerase I of plant nuclear ribosomal genes. In: L. Nover ed. Results and problems in cell differentiation 20: plant promoters and transcription factors. Berlin, Germany: Springer-Verlag, 3-24.
Jellen EN, Gill BS, Cox TS. 1994. Genomic in situ hybridization differentiates between A/D- and C-genome chromatin and detects intergenomic translocations in polyploid oat species (genus Avena). Genome 37: 613-618.
Jiang J, Gill BS. 1994. Different species-specific chromosome translocations in Triticum timopheevii and T. turgidum support the diphyletic origin of polyploid wheats. Chromosome Research 2: 59-64.
Joly S, Rauscher JT, Sherman-Broyles SL, Brown AH, Doyle JJ. 2004. Evolutionary dynamics and preferential expression of homeologous 18S-5.8S−26S nuclear ribosomal genes in natural and artificial glycine allopolyploids. Molecular Biology and Evolution 21: 1409-1421.
Kenton A, Parokonny AS, Gleba YY, Bennett MD. 1993. Characterization of the Nicotiana tabacum L. genome by molecular cytogenetics. Molecular and General Genetics 240: 159-169.
Kobayashi T, Ganley AR. 2005. Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309: 1581-1584.
Komarova NY, Grabe T, Huigen DJ, Hemleben V, Volkov RA. 2004. Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Molecular Biology 56: 439-463.
Koukalova B, Fojtova M, Lim KY, Fulnecek J, Leitch AR, Kovarík A. 2005. Dedifferentiation of tobacco cells is associated with rRNA genes hypomethylation, their increased transcription and chromatin alterations. Plant Physiology 139: 275-286.
Kovarík A, Koukalova B, Lim KY, Matyasek R, Lichtenstein CP, Leitch AR, Bezdek M. 2000. Comparative analysis of DNA methylation in tobacco heterochromatic sequences. Chromosome Research 8: 527-541.
Kovarík A, Matyasek R, Lim KY, Skalicka K, Koukalova B, Knapp S, Chase M, Leitch A. 2004. Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biological Journal of the Linnean Society 82: 615-625.
Kovarík A, Pires JC, Leitch AR, Lim KY, Sherwood AM, Matyasek R, Rocca J, Soltis DE, Soltis PS. 2005. Rapid concerted evolution of nuclear ribosomal DNA in two Tragopogon allopolyploids of recent and recurrent origin. Genetics 169: 931-944.
Leitch AR. 2000. Higher levels of organization in the interphase nucleus of cycling and differentiated cells. Microbiology and Molecular Biology Reviews 64: 138-152.
Leitch AR, Lim KY, Webb DR, McFadden GI. 2001. In situ hybridisation. In: Hawes C, Satiat-Jeunemaitre B, eds. Plant Cell Biology, a Practical Approach. Oxford, UK: Oxford University Press, 267-293.
Lewis MS, Cheverud JM, Pikaard CS. 2004. Evidence for nucleolus organizer regions as the units of regulation in nucleolar dominance in Arabidopsis thaliana interecotype hybrids. Genetics 167: 931-939.
Lim KY, Kovarík A, Matyasek R, Bezdek M, Lichtenstein CP, Leitch AR. 2000. Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109: 161-172.
Lim KY, Kovarík A, Matyasek R, Chase M, Knapp S, Clarkson J, Leitch AR. 2006a. Comparative genomics and repetitive sequence divergence in the diploid Nicotiana section Alatae. Plant Journal 48: 907-919.
Lim KY, Matyasek R, Kovarík A, Leitch A. 2004. Genome evolution in allotetraploid Nicotiana. Biological Journal of the Linnean Society 82: 599-606.
Lim KY, Souckova-Skalicka K, Sarasan V, Clarkson JJ, Chase MW, Kovarík A, Leitch A. 2006b. A genetic appraisal of a new synthetic Nicotiana tabacum (Solanaceae) and the Kostoff synthetic tobacco. American Journal of Botany 93: 875-883.
Lin L-S, Ho TD, Harlan JR. 1985. Rapid amplification and fixation of new restriction sites in the ribosomal DNA repeats in the derivatives of a cross between maize and Tripsacum dactyloides. Developmental Genetics 6: 101-112.
Maloisel L, Rossignol JL. 1998. Suppression of crossing-over by DNA methylation in Ascobolus. Genes and Development 12: 1381-1389.
Martini G, O'Dell M, Flavell RB. 1982. Partial inactivation of wheat nucleolus chromosomes from Aegilops umbellulata. Chromosoma 84: 867-700.
Matyasek R, Lim KY, Kovarík A, Leitch AR. 2003. Ribosomal DNA evolution and gene conversion in Nicotiana rustica. Heredity 91: 268-275.
Murad L, Lim KY, Christopodulou V, Matyasek R, Lichtenstein C, Kovarík A, Leitch A. 2002. The origin of tobacco's T genome is tracted to a particular lineage within Nicotiana tomentosiformis (Solanaceae). American Journal of Botany 89: 921-928.
Navashin M. 1934. Chromosomal alterations caused by hybridization and their bearing upon certain general genetic problems. Cytologia 5: 169-203.
Neves N, Delgado M, Silva M, Caperta A, Morais-Cecilio L, Viegas W. 2005. Ribosomal DNA heterochromatin in plants. Cytogenetic and Genome Research 109: 104-111.
O’Kane SL, Schaal BA, Al-Shehbaz IA. 1996. The origins of Arabidopsis suecica as indicated by nuclear rDNA sequences. Systematic Botany 21: 559-566.
Pecinka A, Schubert V, Meister A, Kreth G, Klatte M, Lysak MA, Fuchs J, Schubert I. 2004. Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random except for NOR-bearing chromosomes. Chromosoma 113: 258-269.
Pikaard CS. 2000. The epigenetics of nucleolar dominance. Trends in Genetics 16: 495-500.
Pontes O, Neves N, Silva M, Lewis MS, Madlung A, Comai L, Viegas W, Pikaard CS. 2004. Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proceedings of the National Academy of Sciences, USA 101: 18240-18245.
Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I, Vaucheret H, Mittelsten Scheid O. 2004. Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16: 1021-1034.
Ren N, Timko MP. 2001. AFLP analysis of genetic polymorphism and evolutionary relationships among cultivated and wild Nicotiana species. Genome 44: 559-571.
Riddle NC, Richards EJ. 2005. Genetic variation in epigenetic inheritance of ribosomal RNA gene methylation in Arabidopsis. Plant Journal 41: 524-532.
Sang T, Crawford DJ, Stuessy TF. 1995. Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proceedings of the National Academy of Sciences, USA 92: 6813-6817.
Shaw PJ, Jordan EG. 1995. The nucleolus. Annual Review of Cell and Developmental Biology 11: 93-121.
Skalická K, Lim KY, Matyásek R, Koukalová B, Leitch A, Kovarík A. 2003. Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. American Journal of Botany 90: 291-303.
Skalicka K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarík A. 2005. Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytologist 166: 291-303.
Storchova H, Hrdlickova R, Chrtek J, Tetera M, Fitze D, Fehrer J. 2000. An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon 49: 79-84.
Viegas W, Neves N, Silva M, Caperta A, Morais-Cecilio L. 2002. Nucleolar dominance: a ‘David and Goliath’ imprinting process. Current Genomics 3: 563-576.
Volkov RA, Borisjuk NV, Panchuk II, Schweizer D, Hemleben V. 1999. Elimination and rearrangement of parental rDNA in the allotetraploid Nicotiana tabacum. Molecular Biology and Evolution 16: 311-320.
Weiss H, Maluszynska. J. 2000. Chromosomal rearrangement in autotetraploid plants of Arabidopsis thaliana. Hereditas 133: 255-261.
Wendel JF, Schnabel A, Seelanan T. 1995. Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proceedings of the National Academy of Sciences, USA 92: 280-284.
Yukawa M, Tsudzuki T, Sugiura M. 2006. The chloroplast genome of Nicotiana sylvestris and Nicotiana tomentosiformis: complete sequencing confirms that the Nicotiana sylvestris progenitor is the maternal genome donor of Nicotiana tabacum. Molecular Genetics and Genomics 275: 367-373.
Zhao XP, Si Y, Hanson RE, Crane CF, Price HJ, Stelly DM, Wendel JF, Paterson AH. 1998. Dispersed repetitive DNA has spread to new genomes since polyploid formation in cotton. Genome Research 8: 479-492.
Variation in Ribosomal DNA in the Genus Trifolium (Fabaceae)
The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum
Evolution of Plant B Chromosome Enriched Sequences
Low abundant spacer 5S rRNA transcripts are frequently polyadenylated in Nicotiana
