Concerted evolution of rDNA in recently formed Tragopogon allotetraploids is typically associated with an inverse correlation between gene copy number and expression
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.
PubMed
17603114
PubMed Central
PMC1950650
DOI
10.1534/genetics.107.072751
PII: genetics.107.072751
Knihovny.cz E-zdroje
- MeSH
- chromatin genetika MeSH
- diploidie MeSH
- DNA primery genetika MeSH
- DNA rostlinná genetika MeSH
- exprese genu MeSH
- genová dávka MeSH
- molekulární evoluce MeSH
- molekulární sekvence - údaje MeSH
- organizátor jadérka genetika MeSH
- polymorfismus konformace jednovláknové DNA MeSH
- polyploidie MeSH
- populační genetika MeSH
- ribozomální DNA genetika MeSH
- rostlinné geny MeSH
- sekvence nukleotidů MeSH
- Tragopogon genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Geografické názvy
- Idaho MeSH
- Washington MeSH
- Názvy látek
- chromatin MeSH
- DNA primery MeSH
- DNA rostlinná MeSH
- ribozomální DNA MeSH
We analyzed nuclear ribosomal DNA (rDNA) transcription and chromatin condensation in individuals from several populations of Tragopogon mirus and T. miscellus, allotetraploids that have formed repeatedly within only the last 80 years from T. dubius and T. porrifolius and T. dubius and T. pratensis, respectively. We identified populations with no (2), partial (2), and complete (4) nucleolar dominance. It is probable that epigenetic regulation following allopolyploidization varies between populations, with a tendency toward nucleolar dominance by one parental homeologue. Dominant rDNA loci are largely decondensed at interphase while silent loci formed condensed heterochromatic regions excluded from nucleoli. Those populations where nucleolar dominance is fixed are epigenetically more stable than those with partial or incomplete dominance. Previous studies indicated that concerted evolution has partially homogenized thousands of parental rDNA units typically reducing the copy numbers of those derived from the T. dubius diploid parent. Paradoxically, despite their low copy number, repeats of T. dubius origin dominate rDNA transcription in most populations studied, i.e., rDNA units that are genetic losers (copy numbers) are epigenetic winners (high expression).
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Abbott, R. J., and A. J. Lowe, 2004. Origins, establishment and evolution of two new polyploid species of Senecio in the British Isles. Biol. J. Linn. Soc. 82: 467–474.
Adams, K. L., and J. F. Wendel, 2005. Novel patterns of gene expression in polyploid plants. Trends Genet. 21: 539–543. PubMed
Ainouche, M. L., A. Baumel and A. Salmon, 2004. Spartina anglica Schreb.: a natural model system for analysing evolutionary changes that affect allopolyploid genomes. Biol. J. Linn. Soc. 82: 475–484.
Alvarez, I., and J. W. Wendel, 2003. Ribosomal ITS sequences and plant phylogenetic inference. Mol. Phylogenet. Evol. 29: 417–434. PubMed
Bennett, R. I., and A. G. Smith, 1991. Use of a genomic clone for ribosomal RNA from Brassica oleracea in RFLP analysis of Brassica species. Plant. Mol. Biol. 16: 685–688. PubMed
Birchler, J.A., N. C. Riddle, D. L. Auger and R. A. Veitia, 2005. Dosage balance in gene regulation: biological implications. Trends Genet. 21: 219–226. PubMed
Chen, Z. J., and C. S. Pikaard, 1997. a Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev. 11: 2124–2136. PubMed PMC
Chen, Z. J., and C. S. Pikaard, 1997. b 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
Chen, Z. J., L. Comai and C. S. Pikaard, 1998. Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proc. Natl. Acad. Sci. USA 95: 14891–14896. PubMed PMC
Cluster, P. D., O. Calderini, F. Pupilli, F. Crea, F. Damiani et al., 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. PubMed
Cook, L. M., P. S. Soltis, S. J. Brunsfeld and D. E. Soltis, 1998. Multiple independent formations of Tragopogon tetraploids (Asteraceae): evidence from RAPD markers. Mol. Ecol. 7: 1293–1302.
Dadejová, M., K. Y. Lim, K. Součková-Skalická, R. Matyášek, M.-A. Grandbastien et al., 2007. Transcription activity of rRNA genes correlates with a tendency towards intergenomic homogenization in Nicotiana allotetraploids. New Phytol. 166: 291–303. PubMed
Durica, D. S., and H. M. Krider, 1978. Studies on the ribosomal RNA cistrons in interpsecific Drosophila hybrids. II. Heterochromatic regions mediating nucleolar dominance. Genetics 89: 37–64. PubMed PMC
Earley, K., R. J. Lawrence, O. Pontes, R. Reuther, A. J. Enciso et al., 2006. Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev. 20: 1283–1293. PubMed PMC
Flavell, R. B., and M. O'Dell, 1976. Ribosomal RNA genes in homeologous chromosomes of groups 5 and 6 in hexaploid wheat. Heredity 37: 377–385.
Flavell, R. B., M. O'Dell, M. Vincentz, R. Sardana and R. F. Barker, 1986. The differential expression of ribosomal RNA genes. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 314: 295–298.
Fulnecek, J., R. Matyášek, A. Kovarik and M. Bezdek, 1998. Mapping of 5-methylcytosine residues in Nicotiana tabacum 5S rRNA genes by genomic sequencing. Mol. Gen. Genet. 259: 133–141. PubMed
Gerlach, W. L., and J. R. Bedbrook, 1979. Cloning and characterization of ribosomal RNA genes in wheat. Nucleic Acids Res. 7: 1869–1885. PubMed PMC
Gonzalez-Melendi, P., B. Wells, A. F. Beven and P. J. Shaw, 2001. Single ribosomal transcription units are linear, compacted Christmas trees in plant nucleoli. Plant J. 27: 223–233. PubMed
Goodrich-Young, C., and H. M. Krider, 1989. Nucleolar dominance and replicative dominance in Drosophila interspecific hybrids. Genetics 133: 349–358. PubMed PMC
Joly, S., J. T. Rauscher, S. L. Sherman-Broyles, A. H. Brown and J. J. Doyle, 2004. Evolutionary dynamics and preferential expression of homeologous 18S–5.8S–26S nuclear ribosomal genes in natural and artificial glycine allopolyploids. Mol. Biol. Evol. 21: 1409–1421. PubMed
Komarova, N. Y., T. Grabe, D. J. Huigen, V. Hemleben and R. A. Volkov, 2004. Organization, differential expression and methylation of rDNA in artificial Solanum allopolyploids. Plant Mol. Biol. 56: 439–463. PubMed
Kovarik, A., R. Matyášek, K. Y. Lim, K. Skalicka, B. Koukalova et al., 2004. Concerted evolution of 18–5.8–26S rDNA repeats in Nicotiana allotetraploids. Biol. J. Linn. Soc. 82: 615–625.
Kovarik, A., J. C. Pires, A. R. Leitch, K. Y. Lim, A. M. Sherwood 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
Lawrence, R. J., K. Early, O. Pontes, M. Silva, Z. J. Chen et al., 2004. A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol. Cell 13: 599–609. PubMed
Leach, C. R., A. Houben, B. Field, K. Pistrick, D. Demidov et al., 2005. Molecular evidence for transcription of genes on a B chromosome in Crepis capillaris. Genetics 171: 269–278. PubMed PMC
Leitch, A. R., K. Y. Lim, D. R. Webb and G. I. McFadden, 2001. In situ hybridisation, pp. 267–203 in Plant Cell Biology, a Practical Approach, edited by C. Hawes and B. Satiat-Jeunemaitre Oxford University Press, Oxford.
Lewis, M. S., J. M. Cheverud and C. S. Pikaard, 2004. Evidence for nucleolus organizer regions as the units of regulation in nucleolar dominance in Arabidopsis thaliana interecotype hybrids. Genetics 167: 931–939. PubMed PMC
Lim, K. Y., A. Kovarik, R. Matyášek, M. Bezdek, C. P. Lichtenstein et al., 2000. Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109: 161–172. PubMed
Lim, K.Y., K. Souckova-Skalicka, V. Sarasan, J. J. Clarkson, M. W. Chase et al., 2006. A genetic appraisal of a new synthetic Nicotiana tabacum (Solanaceae) and the Kostoff synthetic tobacco. Am. J. Bot. 93: 875–883. PubMed
Lin, L.-S., T. D. Ho and J. R. Harlan, 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. Develop. Genet. 6: 101–112.
Martini, G., M. O'Dell and R. B. Flavell, 1982. Partial inactivation of wheat nucleolus chromosomes from Aegilopos umbellulata. Chromosoma 84: 867–700.
Mavrodiev, E. V., C. E. Edwards, D. C. Albach, M. A. Gitzendanner, P. S. Soltis et al., 2004. Phylogenetic relationships in subtribe Scorzonerinae (Asteraceae: Cichorioideae: Cichorieae) based on ITS sequence data. Taxon 53: 699–712.
Mayer, C., K. M. Schmitz, J. Li, I. Grummt and R. Santoro, 2006. Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol. Cell 22: 351–361. PubMed
Michel, A. H., B. Kornmann, K. Dubrana and D. Shore, 2005. Spontaneous rDNA copy number variation modulates Sir2 levels and epigenetic gene silencing. Genes Dev. 19: 1199–1210. PubMed PMC
Navashin, M., 1934. Chromosomal alterations caused by hybridization and their bearing upon certain general genetic problems. Cytologia 5: 169–203.
Neves, N., M. Delgado, M. Silva, A. Caperta, L. Morais-Cecilio et al., 2005. Ribosomal DNA heterochromatin in plants. Cytogenet. Genome Res. 109: 104–111. PubMed
Novak, S. J., D. E. Soltis and P. S. Soltis, 1991. Ownbey's Tragopogons: forty years later. Am. J. Bot. 37: 788–796.
O'Kane, S. L., B. A. Schaal and I. A. Al-Shehbaz, 1996. The origins of Arabidopsis suecica as indicated by nuclear rDNA sequences. Syst. Bot. 21: 559–566.
Ownbey, M., 1950. Natural hybridization and amphiploidy in the genus Tragopogon. Am. J. Bot. 37: 487–499.
Pikaard, C. S., 2000. The epigenetics of nucleolar dominance. Trends Genet. 16: 495–500. PubMed
Pires, J. C., K. Y. Lim, A. Kovarík, R. Matyášek, A. Boyd et al., 2004. Molecular cytogenetic analysis of recently evolved Tragopogon (Asteracea) allopolyploids reveal a karyotype that is additive of the diploid progenitors. Am. J. Bot. 91: 1022–1035. PubMed
Pontes, O., R. J. Lawrence, N. Neves, M. Silva, J. H. Lee et al., 2003. Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in Arabidopsis. Proc. Natl. Acad. Sci. USA 100: 11418–11423. PubMed PMC
Pontes, O., N. Neves, M. Silva, M. S. Lewis, A. Madlung et al., 2004. Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc. Natl. Acad. Sci. USA 101: 18240–18245. PubMed PMC
Preuss, S., and C. S. Pikaard, 2007. rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochem. Biophys. Acta 1769: 383–392. PubMed PMC
Probst, A. V., M. Fagard, F. Proux, P. Mourrain, S. Boutet et al., 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. PubMed PMC
Riddle, N. C., and E. J. Richards, 2002. The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162: 355–363. PubMed PMC
Saghai-Maroof, M. A., K. M. Soliman, R. A. Jorgensen and R. W. Allard, 1984. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc. Natl. Acad. Sci. USA 81: 8014–8018. PubMed PMC
Sambrook, J., and D. W. Russel, 2001. Detection of mutations by single-strand conformation polymorphism and heteroduplex analysis, pp. 1349–1356 in Molecular Cloning: A Laboratory Manual, edited by J. Sambrook and D. W. Russel. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Schubert, I., and C. Kunzel, 1990. Position-dependent NOR activity in barley. Chromosoma 99: 352–359.
Shaw, P. J., and E. G. Jordan, 1995. The nucleolus. Ann. Rev. Cell. Develop. Biol. 11: 93–121. PubMed
Skalická, K., K. Y. Lim, R. Matyášek, B. Koukalová, A. Leitch et al., 2003. Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. Am. J. Bot. 90: 291–303. PubMed
Soltis, D. E., and P. S. Soltis, 1989. Allopolyploid speciation in Tragopogon: insights from chloroplast DNA. Am. J. Bot. 76: 1119–1124.
Soltis, D. E., P. S. Soltis, J. C. Pires, A. Kovarik and J. Tate, 2004. Recent and recurrent polyploidy in Tragopogon (Asteraceae): Genetics, Genomic, and Cytogenetic Comparisons. Biol. J. Linn. Soc. 82: 485–501.
Soltis, P. E., G. M. Plunkett, S. J. Novak and D. E. Soltis, 1995. Genetic variation in Tragopogon species: additional origins of the allotetraploids T. mirus and T. miscellus (Compositae). Am. J. Bot. 82: 1329–1341.
Tate, J. A., Z. Ni, A.-C. Scheen, J. Koh, C. A. Gilbert et al., 2006. Transcriptome diversity and rapid elimination of homeologous loci in Tragopogon miscellus (Asteracea), a recent and reciprocally formed allopolyploid. Genetics 173: 1599–1611. PubMed PMC
van Vugt, J. J., S. de Nooijer, R. Stouthamer and H. de Jong, 2005. NOR activity and repeat sequences of the paternal sex ratio chromosome of the parasitoid wasp Trichogramma kaykai. Chromosoma 114: 410–419. PubMed
Viegas, W., N. Neves, M. Silva, A. Caperta and L. Morais-Cecilio, 2002. Nucleolar dominance: a “David and Goliath” imprinting process. Curr. Genomics 3: 563–576.
Volkov, R. A., N. Y. Komarova and V. Hemleben, 2007. Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Syst. Biodiv. (in press).
Weiss, H., and J. Maluszynska, 2000. Chromosomal rearrangement in autotetraploid plants of Arabidopsis thaliana. Hereditas 133: 255–261. PubMed
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