To study the relationship between uniparental rDNA (encoding 18S, 5.8S and 26S ribosomal RNA) silencing (nucleolar dominance) and rRNA gene dosage, we studied a recently emerged (within the last 80 years) allotetraploid Tragopogon mirus (2n=24), formed from the diploid progenitors T. dubius (2n=12, D-genome donor) and T. porrifolius (2n=12, P-genome donor). Here, we used molecular, cytogenetic and genomic approaches to analyse rRNA gene activity in two sibling T. mirus plants (33A and 33B) with widely different rRNA gene dosages. Plant 33B had ~400 rRNA genes at the D-genome locus, which is typical for T. mirus, accounting for ~25% of total rDNA. We observed characteristic expression dominance of T. dubius-origin genes in all organs. Its sister plant 33A harboured a homozygous macrodeletion that reduced the number of T. dubius-origin genes to about 70 copies (~4% of total rDNA). It showed biparental rDNA expression in root, flower and callus, but not in leaf where D-genome rDNA dominance was maintained. There was upregulation of minor rDNA variants in some tissues. The RNA polymerase I promoters of reactivated T. porrifolius-origin rRNA genes showed reduced DNA methylation, mainly at symmetrical CG and CHG nucleotide motifs. We hypothesise that active, decondensed rDNA units are most likely to be deleted via recombination. The silenced homeologs could be used as a 'first reserve' to ameliorate mutational damage and contribute to evolutionary success of polyploids. Deletion and reactivation cycles may lead to bidirectional homogenisation of rRNA arrays in the long term.

Laboratory of Molecular Epigenetics Academy of Sciences of the Czech Republic v v i Institute of Biophysics Brno Czech Republic

Laboratory of Molecular Systematics and Evolutionary Genetics Department of Biology University of Florida Gainesville FL USA

Laboratory of Molecular Systematics and Evolutionary Genetics Florida Museum of Natural History University of Florida Gainesville FL USA

School of Biological and Chemical Sciences Queen Mary University of London London UK

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Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N et al. (2013). Hybridization and speciation. J Evol Biol 26: 229–246. PubMed

Adams KL, Wendel JF. (2005). Novel patterns of gene expression in polyploid plants. Trends Genet 21: 539–543. PubMed

Bao Y, Wendel JF, Ge S. (2010). Multiple patterns of rDNA evolution following polyploidy in Oryza. Mol Phylogenet Evol 55: 136–142. PubMed

Caperta AD, Neves N, Morais-Cecilio L, Malho R, Viegas W. (2002). Genome restructuring in rye affects the expression, organization and disposition of homologous rDNA loci. J Cell Sci 115: 2839–2846. PubMed

Chen ZJ, Pikaard CS. (1997). 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: 3442–3447. PubMed PMC

Costa-Nunes P, Pontes O, Preuss SB, Pikaard CS. (2010). Extra views on RNA-dependent DNA methylation and MBD6-dependent heterochromatin formation in nucleolar dominance. Nucleus 1: 254–259. PubMed PMC

Doelling JH, Pikaard CS. (1995). The minimal ribosomal-RNA gene promoter of Arabidopsis-Thaliana includes a critical element at the transcription initiation site. Plant J 8: 683–692. PubMed

Flavell RB, Odell M. (1976). Ribosomal RNA genes on homoeologous chromosomes of groups 5 and 6 in hexaploid wheat. Heredity 37: 377–385.

Flavell RB, Odell M. (1979). Genetic-control of nucleolus formation in wheat. Chromosoma 71: 135–152.

Fojtová M, Kovařík A, Matyášek R. (2001). Cytosine methylation of plastid genome in higher plants. Fact of artefact? Plant Sci 160: 585–593. PubMed

Garcia S, Kovarik A. (2013). Dancing together and separate again: gymnosperms exhibit frequent changes of fundamental 5S and 35S rRNA gene (rDNA) organisation. Heredity 111: 23–33. PubMed PMC

Ge XH, Ding L, Li ZY. (2013). Nucleolar dominance and different genome behaviors in hybrids and allopolyploids. Plant Cell Rep 32: 1661–1673. PubMed

Grandont L, Jenczewski E, Lloyd A. (2013). Meiosis and its deviations in polyploid plants. Cytogenet Genome Res 140: 171–184. PubMed

Grummt I, Pikaard CS. (2003). Epigenetic silencing of RNA polymerase I transcription. Nat Rev Mol Cell Biol 4: 641–649. PubMed

Hasterok R, Maluszynska J. (2000). Nucleolar dominance does not occur in root tip cells of allotetraploid Brassica species. Genome 43: 574–579. PubMed

Hetzl J, Foerster AM, Raidl G, Mittelsten Scheid O. (2007). CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. Plant J 51: 526–536. PubMed

Ingle J, Timmis JN, Sinclair J. (1975). The relationship between satellite deoxyribonucleic acid, ribosomal ribonucleic acid gene redundancy, and genome size in plants. Plant Physiol 55: 496–501. PubMed PMC

Kobayashi T, Ganley AR. (2005). Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309: 1581–1584. PubMed

Kobyashi T. (2011). Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptiblity in yeast. Cell Mol Life Sci 68: 1395–1403. PubMed PMC

Komarova NY, Grabe T, Huigen TJ, Hemleben V, Volkov RA. (2004). Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol Biol 56: 439–463. PubMed

Koukalova B, Fojtova M, Lim KY, Fulnecek J, Leitch AR, Kovarik A. (2005). Dedifferentiation of tobacco cells is associated with ribosomal RNA gene hypomethylation, increased transcription, and chromatin alterations. Plant Physiol 139: 275–286. PubMed PMC

Kovarik A, Dadejova M, Lim YK, Chase MW, Clarkson JJ, Knapp S, Leitch AR. (2008). Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann Bot (Lond) 101: 815–823. PubMed PMC

Kovarik A, Pires JC, Leitch AR, Lim KY, Sherwood AM, Matyasek R et al. (2005). Rapid concerted evolution of nuclear ribosomal DNA in two Tragopogon allopolyploids of recent and recurrent origin. Genetics 169: 931–944. PubMed PMC

Leitch AR, Leitch IJ. (2008). Genomic plasticity and the diversity of polyploid plants. Science 320: 481–483. PubMed

Lim KY, Soltis DE, Soltis PS, Tate J, Matyasek R, Srubarova H et al. (2008). Rapid chromosome evolution in recently formed polyploids in Tragopogon (Asteraceae). PLoS ONE 3: e3353. PubMed PMC

Matyasek R, Renny-Byfield S, Fulnecek J, Macas J, Grandbastien MA, Nichols R et al. (2012). Next generation sequencing analysis reveals a relationship between rDNA unit diversity and locus number in Nicotiana diploids. BMC Genomics 13: 722. PubMed PMC

Matyasek R, Tate JA, Lim YK, Srubarova H, Koh J, Leitch AR et al. (2007). Concerted evolution of rDNA in recently formed Tragopogon allotetraploids is typically associated with an inverse correlation between gene copy number and expression. Genetics 176: 2509–2519. PubMed PMC

Mavrodiev EV, Soltis PS, Soltis DE. (2008). Putative parentage of six Old World polyploids in Tragopogon L. (Asteraceae: Scorzonerinae) based on ITS, ETS, and plastid sequence data. Taxon 57: 1215–1232.

Mohan J, Ritossa FM. (1970). Regulation of ribosomal RNA synthesis and its bearing on the bobbed phenotype in Drosophila melanogaster. Dev Biol 22: 495–512. PubMed

Navashin M. (1934). Chromosomal alterations caused by hybridzation and their bearing upon certain general genetic problems. Cytologia 5: 169–203.

Neves N, Heslopharrison JS, Viegas W. (1995). Ribosomal RNA gene activity and control of expression mediated by methylation and imprinting during embryo development in wheat X rye hybrids. Theor Appl Genet 91: 529–533. PubMed

Nieto Feliner G, Rossello JA. (2012). Concerted evolution of multigene families and homeologous recombination. In: Wendel JF (ed) Plant Genome Diversity Vol. 1, Springer-Verlag: Wien. pp 171–194.

Paredes S, Branco AT, Hartl DL, Maggert KA, Lemos B. (2011). Ribosomal DNA deletions modulate genome-wide gene expression: ‘rDNA-sensitive' genes and natural variation. PLoS Genet 7: e1001376. PubMed PMC

Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C et al. (2010). Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol 186: 37–45. PubMed

Peng JC, Karpen GH. (2007). H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat Cell Biol 9: 25–35. PubMed PMC

Pires JC, Lim KY, Kovarik A, Matyasek R, Boyd A, Leitch AR et al. (2004). Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveal a karyotype that is additive of the diploid progenitors. Am J Bot 91: 1022–1035. PubMed

Pontvianne F, Blevins T, Chandrasekhara C, Mozgova I, Hassel C, Pontes OMF et al. (2013). Subnuclear partitioning of rRNA genes between the nucleolus and nucleoplasm reflects alternative epiallelic states. Gene Dev 27: 1545–1550. PubMed PMC

Raskina O, Belyayev A, Nevo E. (2004). Activity of the En/Spm-like transposons in meiosis as a base for chromosome repatterning in a small, isolated, peripheral population of Aegilops speltoides Tausch. Chromosome Res 12: 153–161. PubMed

Renny-Byfield S, Wendel JF. (2014). Doubling down on genome: polyploidy and crop plants. Am J Bot 101: 1711–1725. PubMed

Ritossa FM, Atwood KC, Spiegelman S. (1966). A molecular explanation of the bobbed mutants of Drosophila as partial deficiencies of ‘ribosomal' DNA. Genetics 54: 819–834. PubMed PMC

Soltis DE, Mavrodiev EV, Meyers SC, Severns PM, Zhang LJ, Gitzendanner MA et al. (2012). Additional origins of Ownbey's Tragopogon mirus. Bot J Linn Soc 169: 297–311.

Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate J. (2004). Recent and recurrent polyploidy in Tragopogon (Asteraceae): genetics, genomic, and cytogenetic comparisons. Biol J Linn Soc 82: 485–501.

Tate JA, Ni Z, Scheen AC, Koh J, Gilbert CA, Lefkowitz D et al. (2006). Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173: 1599–1611. PubMed PMC

Volkov RA, Komarova NY, Hemleben V. (2007). Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Syst Biodivers (NHM London) 5: 261–276.

Wendel JF, Schnabel A, Seelanan T. (1995). Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92: 280–284. PubMed PMC

Transcriptional Silencing of 35S rDNA in Tragopogon porrifolius Correlates with Cytosine Methylation in Sequence-Specific Manner

Uniparental expression of ribosomal RNA in ×Festulolium grasses: a link between the genome and nucleolar dominance

The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum

Competition of Parental Genomes in Plant Hybrids

Unique Epigenetic Features of Ribosomal RNA Genes (rDNA) in Early Diverging Plants (Bryophytes)

Intragenomic heterogeneity of intergenic ribosomal DNA spacers in Cucurbita moschata is determined by DNA minisatellites with variable potential to form non-canonical DNA conformations

Unstable Inheritance of 45S rRNA Genes in Arabidopsis thaliana

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Dryad
10.5061/dryad.BB249

GENBANK
HG915911