Silenced rRNA genes are activated and substitute for partially eliminated active homeologs in the recently formed allotetraploid, Tragopogon mirus (Asteraceae)

Heredity

Volumn 114, Issue 3, 2015, Pages 356-365

  Dobesova E ^a   Malinska H ^a   Matyasek R ^a   Leitch, A R ^b   Soltis, D E ^c   Soltis, P S ^d   Kovarik A ^a  

^a INSTITUTE OF BIOPHYSICS   (Czech Republic)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARRAY; GENE EXPRESSION; GENOME; HERB; METHYLATION; POLYPLOIDY; RECOMBINATION; RNA;

ASTERACEAE; TRAGOPOGON MIRUS;

RIBOSOME RNA; RNA 18S; RNA 5.8S; RNA, RIBOSOMAL, 26S;

CHROMOSOME NOR; DNA METHYLATION; DNA SEQUENCE; GENE DELETION; GENE DOSAGE; GENE SILENCING; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PLANT GENE; POLYPLOIDY; PROMOTER REGION; RNA GENE; TRAGOPOGON;

DNA METHYLATION; EVOLUTION, MOLECULAR; GENE DOSAGE; GENE SILENCING; GENES, PLANT; GENES, RRNA; MOLECULAR SEQUENCE DATA; NUCLEOLUS ORGANIZER REGION; POLYPLOIDY; PROMOTER REGIONS, GENETIC; RNA, RIBOSOMAL; RNA, RIBOSOMAL, 18S; RNA, RIBOSOMAL, 5.8S; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; TRAGOPOGON;

EID: 84922620224     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2014.111     Document Type: Article

References (45)

1. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N et al. (2013). Hybridization and speciation. J Evol Biol 26: 229-246
2. Adams KL, Wendel JF (2005). Novel patterns of gene expression in polyploid plants. Trends Genet 21: 539-543
3. Bao Y, Wendel JF, Ge S (2010). Multiple patterns of rDNA evolution following polyploidy in Oryza. Mol Phylogenet Evol 55: 136-142
4. 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
5. 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
6. 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
7. 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
8. Flavell RB, Odell M (1976). Ribosomal RNA genes on homoeologous chromosomes of groups 5 and 6 in hexaploid wheat. Heredity 37: 377-385
9. Flavell RB, Odell M (1979). Genetic-control of nucleolus formation in wheat. Chromosoma 71: 135-152
10. Fojtová M, Kovarík A, Matyášek R (2001). Cytosine methylation of plastid genome in higher plants. Fact of artefact? Plant Sci 160: 585-593
11. 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
12. Ge XH, Ding L, Li ZY (2013). Nucleolar dominance and different genome behaviors in hybrids and allopolyploids. Plant Cell Rep 32: 1661-1673
13. Grandont L, Jenczewski E, Lloyd A (2013). Meiosis and its deviations in polyploid plants. Cytogenet Genome Res 140: 171-184
14. Grummt I, Pikaard CS (2003). Epigenetic silencing of RNA polymerase I transcription. Nat Rev Mol Cell Biol 4: 641-649
15. Hasterok R, Maluszynska J (2000). Nucleolar dominance does not occur in root tip cells of allotetraploid Brassica species. Genome 43: 574-579
16. 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
17. 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
18. Kobayashi T, Ganley AR (2005). Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309: 1581-1584
19. 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
20. 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
21. 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
22. 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
23. 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
24. Leitch AR, Leitch IJ (2008). Genomic plasticity and the diversity of polyploid plants. Science 320: 481-483
25. 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
26. 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
27. 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
28. 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
29. 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
30. Navashin M (1934). Chromosomal alterations caused by hybridzation and their bearing upon certain general genetic problems. Cytologia 5: 169-203
31. 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
32. 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
33. 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
34. 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
35. Peng JC, Karpen GH (2007). H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nat Cell Biol 9: 25-35
36. 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
37. 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
38. 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
39. Renny-Byfield S, Wendel JF (2014). Doubling down on genome: polyploidy and crop plants. Am J Bot 101: 1711-1725
40. 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
41. 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
42. 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
43. 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.
44. Volkov RA, Komarova NY, Hemleben V (2007). Ribosomal DNA in plant hybrids: inheritance, rearrangement, expression. Syst Biodivers (NHM London) 5: 261-276
45. 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