When fathers are instant losers: homogenization of rDNA loci in recently formed Cardamine × schulzii trigenomic allopolyploid
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
24916080
DOI
10.1111/nph.12873
Knihovny.cz E-zdroje
- Klíčová slova
- Brassicaceae, concerted evolution, hybridization, hybrids, polyploidy, rDNA,
- MeSH
- Cardamine genetika MeSH
- chromozomy rostlin genetika MeSH
- druhová specificita MeSH
- fylogeneze MeSH
- genetická variace MeSH
- genetické lokusy * MeSH
- genom rostlinný MeSH
- klonování DNA MeSH
- křížení genetické * MeSH
- mezerníky ribozomální DNA genetika MeSH
- polyploidie * MeSH
- regulace genové exprese u rostlin MeSH
- ribozomální DNA genetika MeSH
- sekvence nukleotidů MeSH
- vysoce účinné nukleotidové sekvenování MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- mezerníky ribozomální DNA MeSH
- ribozomální DNA MeSH
Recently formed allopolyploids represent an excellent system to study the impacts of hybridization and genomic duplication on genome structure and evolution. Here we explored the 35SrRNA genes (rDNA) in the Cardamine × schulzii allohexaploid that was formed by two subsequent hybridization events within the past c. 150 yr. The rDNA loci were analyzed by cloning, next generation sequencing (NGS), RT-PCR and FISH methods. The primary C. × insueta triploid hybrid derived from C. rivularis (♀) and C. amara (♂) had gene ratios highly skewed towards maternal sequences. Similarly, C. × schulzii, originating from the secondary hybridization event involving C. × insueta (♀) and C. pratensis (♂), showed a reduction in paternal rDNA homeologs despite an excess of chromosomes inherited from C. pratensis. We also identified novel rDNA loci in C. × schulzii, suggesting that lost loci might be slowly reinstalled by translocation (but not recombination) of genes from partner genomes. Prevalent clonal propagation of allopolyploids, C. × insueta and C. × schulzii, indicates that concerted evolution of rDNA may occur in the absence of extensive meiotic cycles. Adoption of NGS in rDNA variant analysis is highly informative for deciphering the evolutionary histories of allopolyploid species with ongoing homogenization processes.
Department of Biology University Osnabrueck Osnabrueck Germany
Institute of Botany Slovak Academy of Sciences Bratislava Slovakia
RG Plant Cytogenomics CEITEC Masaryk University Brno Czech Republic
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Abbott RJ, Lowe AJ. 2004. Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles. Biological Journal of the Linnean Society 82: 467-474.
Ainouche ML, Baumel A, Salmon A. 2004. Spartina anglica Schreb.: a natural model system for analysing early evolutionary changes that affect allopolyploid genomes. Biological Journal of the Linnean Society 82: 475-484.
Álvarez I, Wendel JW. 2003. Ribosomal ITS sequences and plant phylogenetic inference. Molecular Phylogenetics and Evolution 29: 417-434.
Bao Y, Wendel JF, Ge S. 2010. Multiple patterns of rDNA evolution following polyploidy in Oryza. Molecular Phylogenetics and Evolution 55: 136-142.
Birchler JA. 2012. Genetic consequences of polyploidy in plants. In: Soltis PE, Soltis DE, eds. Polyploidy and genome evolution. Berlin/Heidelberg, Germany: Springer, 21-32.
Brown DD, Wensink PC, Jordan E. 1972. Comparison of ribosomal DNAs of Xenopus laevis and Xenopus mulleri - evolution of tandem genes. Journal of Molecular Biology 63: 57-73.
Carlsen T, Bleeker W, Hurka H, Elven R, Brochmann C. 2009. Biogeography and phylogeny of Cardamine (Brassicaceae). Annals of the Missouri Botanical Garden 96: 215-236.
Cronn R, Cedroni M, Haselkorn T, Grover C, Wendel JF. 2002. PCR-mediated recombination in amplification products derived from polyploid cotton. Theoretical and Applied Genetics 104: 482-489.
Dover GA. 1982. Molecular drive: a cohesive mode of species evolution. Nature 299: 111-117.
Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF. 2008. Evolutionary genetics of genome merger and doubling in plants. Annual Review of Genetics 42: 443-461.
Eickbush TH, Eickbush DG. 2007. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175: 477-485.
Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
Franzke A, Hurka H. 2000. Molecular systematics and biogeography of the Cardamine pratensis complex (Brassicaceae). Plant Systematics and Evolution 224: 213-234.
Franzke A, Mummenhoff K. 1999. Recent hybrid speciation in Cardamine (Brassicaceae) - conversion of nuclear ribosomal ITS sequences in statu nascendi. Theoretical and Applied Genetics 98: 831-834.
Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27: 221-224.
Hemleben V, Ganal M, Gersnter J, Schiebel K, Torres RA. 1988. Organization and length heterogeneity of plant ribosomal RNA genes. In: Kahl G, ed. The architecture of Eukaryotic Gene. Weinheim, Germany: VHC, 371-384.
Hillis DM, Moritz C, Porter CA, Baker RJ. 1991. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science 251: 308-310.
Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254-267.
Jones RN, Hegarty M. 2009. Order out of chaos in the hybrid plant nucleus. Cytogenetic and Genome Research 126: 376-389.
Kircher M, Kelso J. 2010. High-throughput DNA sequencing - concepts and limitations. BioEssays 32: 524-536.
Kolano B, Tomczak H, Molewska R, Jellen EN, Maluszynska J. 2012. Distribution of 5S and 35S rRNA gene sites in 34 Chenopodium species (Amaranthaceae). Botanical Journal of the Linnean Society 170: 220-231.
Kotseruba V, Gernand D, Meister A, Houben A. 2003. Uniparental loss of ribosomal DNA in the allotetraploid grass Zingeria trichopoda (2n = 8). Genome 46: 156-163.
Kovarik A, Lim KY, Dadejová M, Matyasek R, Chase M, Knapp S, Clarkson J, Leitch AR. 2008. Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Annals of Botany 101: 815-823.
Kovarik A, Matyasek R, Lim KY, Skalicka K, Koukalova B, Knapp S, Chase M, Leitch AR. 2004. Concerted evolution of 18-5.8-26S rDNA repeats in Nicotiana allotetraploids. Biological Journal of the Linnean Society 82: 615-625.
Kovarik 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.
Ksiazczyk T, Kovarik A, Eber F, Huteau V, Khaitova L, Tesarikova Z, Coriton O, Chevre AM. 2011. Immediate unidirectional epigenetic reprogramming of NORs occurs independently of rDNA rearrangements in synthetic and natural forms of a polyploid species Brassica napus. Chromosoma 120: 557-571.
Leitch AR, Leitch IJ. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481-483.
Lepen I, Puizina J. 2011. FISH mapping of 18S-5.8S-26S rRNA genes and fluorochrome banding in the triploid viviparous onion Allium x cornutum Clementi ex Visiani, 1842. Acta Biologica Cracoviensia. Series: Botanica 53: 111-116.
Lim KY, Matyasek R, Kovarik A, Leitch A. 2007. Parental origin and genome evolution in the allopolyploid Iris versicolor. Annals of Botany 100: 219-224.
Liu B, Davis TM. 2011. Conservation and loss of ribosomal RNA gene sites in diploid and polyploid Fragaria (Rosaceae). BMC Plant Biology 11: 157.
Lowe AJ, Abbott RJ. 1996. Origins of the new allopolyploid species Senecio cambrensis (Asteraceae) and its relationship to the Canary Islands endemic Senecio teneriffae. American Journal of Botany 83: 1365-1372.
Lysak MA, Mandáková T. 2013. Analysis of plant meiotic chromosomes by chromosome painting. Methods in Molecular Biology 990: 13-24.
Malinska H, Tate JA, Matyasek R, Leitch AR, Soltis DE, Soltis PS, Kovarik A. 2010. Similar patterns of rDNA evolution in synthetic and recently formed natural populations of Tragopogon (Asteraceae) allotetraploids. BMC Evolutionary Biology 10: 291.
Mandáková T, Kovarik A, Zozomová-Lihová J, Shimizu-Inatsugi R, Shimizu KK, Mummenhoff K, Marhold K, Lysak MA. 2013. The more the merrier: recent hybridization and polyploidy in Cardamine. Plant Cell 25: 3280-3389.
Marhold K, Lihová J, Perný M, Bleeker W. 2004. Comparative ITS and AFLP analysis of diploid Cardamine (Brassicaceae) taxa from closely related polyploid complexes. Annals of Botany 93: 507-520.
Matyasek R, Renny-Byfield S, Fulnecek J, Macas J, Grandbastien MA, Nichols R, Leitch A, Kovarik A. 2012. Next generation sequencing analysis reveals a relationship between rDNA unit diversity and locus number in Nicotiana diploids. BMC Genomics 13: 722.
Matyasek R, Tate JA, Lim YK, Srubarova H, Koh J, Leitch AR, Soltis DE, Soltis PS, Kovarik A. 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.
McClintock B. 1984. The significance of responses of the genome to challenge. Science 226: 792-801.
Mlinarec J, Šatović Z, Malenica N, Ivančić-Baće I, Besendorfer V. 2012. Evolution of the tetraploid Anemone multifida (2n = 32) and hexaploid A. baldensis (2n = 48) (Ranunculaceae) was accompanied by rDNA loci loss and intergenomic translocation: evidence for their common genome origin. Annals of Botany 110: 703-712.
Mummenhoff K, Franzke A, Koch M. 1997. Molecular phylogenetics of Thlaspi s.l. (Brassicaceae) based on chloroplast DNA restriction site variation and sequences of the internal transcribed spacers of nuclear ribosomal DNA. Canadian Journal of Botany 75: 469-482.
Nieto Feliner G, Rosselló JA. 2007. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molecular Phylogenetics and Evolution 44: 911-919.
Nieto Feliner G, Rosselló JA. 2012. Concerted evolution of multigene families and homeologous recombination. In: Wendel JF, ed. Plant genome diversity. Wien, Germany: Springer, 171-194.
Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B, Grandbastien MA. 2010. Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytologist 186: 37-45.
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: 18 240-18 245.
Raskina O, Belyayev A, Nevo E. 2004. Quantum speciation in Aegilops: molecular cytogenetic evidence from rDNA cluster variability in natural populations. Proceedings of the National Academy of Sciences, USA 101: 14 818-14 823.
Rauscher JT, Doyle JJ, Brown AH. 2004. Multiple origins and nrDNA internal transcribed spacer homeologue evolution in the Glycine tomentella (Leguminosae) allopolyploid complex. Genetics 166: 987-998.
Schönswetter P, Stehlik I, Holderegger R, Tribsch A. 2005. Molecular evidence for glacial refugia of mountain plants in the European Alps. Molecular Ecology 14: 3547-3555.
Skalicka K, Lim KY, Matyasek R, Koukalova B, Leitch AR, Kovarik A. 2003. Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line. American Journal of Botany 90: 988-996.
Skalicka K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik 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.
Soltis DE, Soltis PS, Pires JC, Kovarik A, Tate JA, Mavrodiev E. 2004. Recent and recurrent polyploidy in Tragopogon (Asteraceae): cytogenetic, genomic and genetic comparisons. Biological Journal of the Linnean Society 82: 485-501.
Soltis PS, Soltis DE. 2009. The role of hybridization in plant speciation. Annual Review of Plant Biology 60: 561-588.
Straub SC, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A. 2012. Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. American Journal of Botany 99: 349-364.
Urbanska KM, Hurka H, Landolt E, Neuffer B, Mummenhoff K. 1997. Hybridization and evolution in Cardamine (Brassicaceae) at Urnerboden, central Switzerland: Biosystematic and molecular evidence. Plant Systematics and Evolution 204: 233-256.
Urbanska KM, Landolt E. 1999. Patterns and processes of man-influenced hybridisation in Cardamine L. In: van Raamsdonk LWD, den Nijs HCM, eds. Plant evolution in man-made habitats. Amsterdam, the Netherlands: Hugo de Vries Laboratory, 29-47.
Urbanska-Worytkiewicz KM. 1977. Reproduction in natural triploid hybrids (2n = 24) between Cardamine rivularis Schur and C. amara L. Berichte des Geobotanischen Institutes der ETH, Stiftung Rübel 44: 42-85.
Vallejo-Marin M, Lye GC. 2013. Hybridisation and genetic diversity in introduced Mimulus (Phrymaceae). Heredity 110: 111-122.
Veitia RA, Bottani S, Birchler JA. 2013. Gene dosage effects: nonlinearities, genetic interactions, and dosage compensation. Trends in Genetics 29: 385-393.
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.
Weiss-Schneeweiss H, Bloch C, Turner B, Villasenor JL, Stuessy TF, Schneeweiss GM. 2012. The promiscuous and the chaste: frequent allopolyploid speciation and its genomic consequences in american daisies (Melampodium sect. Melampodium; Asteraceae). Evolution 6: 211-228.
Weiss-Schneeweiss H, Emadzade K, Jang T-S, Schneeweiss GM. 2013. Evolutionary consequences, constraints and potential of polyploidy in plants. Cytogenetic and Genome Research 140: 137-150.
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.
Xiong ZY, Gaeta RT, Pires JC. 2011. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid Brassica napus. Proceedings of the National Academy of Sciences, USA 108: 7908-7913.
Zimmerli S. 1986. Einfluss der Bewirtschaftung auf die Entstehung und Struktur der Cardamine Populationen auf dem Urnerboden. Veröffentlichungen des Geobotanischen Institutes der ETH, Stiftung Rübel 87: 141-154.
Zozomová-Lihová J, Krak K, Mandáková T, Shimizu KK, Španiel S, Vít P, Lysak MA. 2014. Multiple hybridization events in Cardamine (Brassicaceae) during the last 150 years: revisiting a textbook example of neoallopolyploidy. Annals of Botany 113: 817-830.
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