Differential amplification of satellite PaB6 in chromosomally hypervariable Prospero autumnale complex (Hyacinthaceae)
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
P 21440
Austrian Science Fund FWF - Austria
PubMed
25169019
PubMed Central
PMC4273535
DOI
10.1093/aob/mcu178
PII: mcu178
Knihovny.cz E-zdroje
- Klíčová slova
- Hyacinthaceae, PaB6, Prospero autumnale, chromosomal evolution, copy number, differential amplification, fluorescence in situ hybridization (FISH), genome size, next-generation sequencing, pericentric satellite DNA,
- MeSH
- chromozomy rostlin genetika MeSH
- diploidie MeSH
- DNA rostlinná genetika MeSH
- fylogeneze MeSH
- genom rostlinný MeSH
- liliovité genetika MeSH
- modely genetické MeSH
- molekulární evoluce MeSH
- molekulární sekvence - údaje MeSH
- polymerázová řetězová reakce * MeSH
- repetitivní sekvence nukleových kyselin genetika MeSH
- satelitní DNA genetika MeSH
- sekvence nukleotidů MeSH
- sekvenční analýza DNA MeSH
- telomery metabolismus MeSH
- variabilita počtu kopií segmentů DNA MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA rostlinná MeSH
- satelitní DNA MeSH
BACKGROUND AND AIMS: Chromosomal evolution, including numerical and structural changes, is a major force in plant diversification and speciation. This study addresses genomic changes associated with the extensive chromosomal variation of the Mediterranean Prospero autumnale complex (Hyacinthaceae), which includes four diploid cytotypes each with a unique combination of chromosome number (x = 5, 6, 7), rDNA loci and genome size. METHODS: A new satellite repeat PaB6 has previously been identified, and monomers were reconstructed from next-generation sequencing (NGS) data of P. autumnale cytotype B(6)B(6) (2n = 12). Monomers of all other Prospero cytotypes and species were sequenced to check for lineage-specific mutations. Copy number, restriction patterns and methylation levels of PaB6 were analysed using Southern blotting. PaB6 was localized on chromosomes using fluorescence in situ hybridization (FISH). KEY RESULTS: The monomer of PaB6 is 249 bp long, contains several intact and truncated vertebrate-type telomeric repeats and is highly methylated. PaB6 is exceptional because of its high copy number and unprecedented variation among diploid cytotypes, ranging from 10(4) to 10(6) copies per 1C. PaB6 is always located in pericentromeric regions of several to all chromosomes. Additionally, two lineages of cytotype B(7)B(7) (x = 7), possessing either a single or duplicated 5S rDNA locus, differ in PaB6 copy number; the ancestral condition of a single locus is associated with higher PaB6 copy numbers. CONCLUSIONS: Although present in all Prospero species, PaB6 has undergone differential amplification only in chromosomally variable P. autumnale, particularly in cytotypes B(6)B(6) and B(5)B(5). These arose via independent chromosomal fusions from x = 7 to x = 6 and 5, respectively, accompanied by genome size increases. The copy numbers of satellite DNA PaB6 are among the highest in angiosperms, and changes of PaB6 are exceptionally dynamic in this group of closely related cytotypes of a single species. The evolution of the PaB6 copy numbers is discussed, and it is suggested that PaB6 represents a recent and highly dynamic system originating from a small pool of ancestral repeats.
Cambridge University Botanic Garden Cambridge CB2 1JF UK
Czech Academy of Sciences Institute of Biophysics Brno Czech Republic
Czech Academy of Sciences Institute of Plant Molecular Biology Ceske Budejovice Czech Republic
Department of Botany and Biodiversity Research University of Vienna Rennweg 14 A 1030 Vienna Austria
Zobrazit více v PubMed
Ainsworth CC, Parker JS, Horton DM. Chromosome variation and evolution in Scilla autumnalis. In: Brandham PE, Bennett MD, editors. Kew Chromosome Conference II. London: Allen and Unwin; 1983. pp. 261–268.
Ali SS, Yu Y, Pfosser M, Wetschnig W. Inferences of biogeographical histories within subfamily Hyacinthoideae using S-DIVA and Bayesian binary MCMC analysis implemented in RASP (Reconstruct Ancestral State in Phylogenies) Annals of Botany. 2012;109:95–107. PubMed PMC
Almeida C, Fonseca A, dos Santos KGB, Pedrosa-Harand A. Contrasting evolution of a satellite DNA and its ancestral IGS rDNA in Phaseolus (Fabaceae) Genome. 2012;55:683–689. PubMed
Altschul S, Gish W, Miller W, Myers E, Lipman D. Basic local alignment search tool. Journal of Molecular Biology. 1990;215:403–410. PubMed
Ambrožová K, Mandáková T, Bures P, et al. Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Annals of Botany. 2011;107:255–268. PubMed PMC
Belyayev A, Raskina O. Chromosome evolution in marginal populations of Aegilops speltoides: causes and consequences. Annals of Botany. 2013;111:531–538. PubMed PMC
Charlesworth B, Sniegowski P, Stephan W. The evolutionary dynamics of repetitive DNA in eukaryotes. Nature. 1994;371:215–220. PubMed
Cohen S, Houben A, Segal D. Extrachromosomal circular DNA derived from tandemly repeated genomic sequences in plants. The Plant Journal. 2008;53:1027–1034. PubMed
Cohen S, Agmon N, Sobol O, Segal D. Extrachromosomal chromosomal circles of satellite repeats and 5S ribosomal DNA in human cells. Mobile DNA. 2010;1:11. PubMed PMC
Csink AK, Henikoff S. Something from nothing: the evolution and utility of satellite repeats. Trends in Genetics. 1998;14:200–204. PubMed
Cuadrado A, Jouve N. Evolutionary trends of different repetitive DNA sequences during speciation in the genus Secale. Journal of Heredity. 2002;93:339–345. PubMed
Deschamps S, Campbell MA. Utilization of next-generation sequencing platforms in plant genomics and genetic variant discovery. Molecular Breeding. 2010;25:553–570.
Dover GA. Molecular drive: a cohesive mode of species evolution. Nature. 1982;299:111–117. PubMed
Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin. 1987;19:11–15.
Ebert I, Greilhuber J, Speta F. Chromosome banding and genome size differentiation in Prospero (Hyacinthaceae): diploids. Plant Systematics and Evolution. 1996;203:143–177.
Eickbush TH, Eickbush DG. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics. 2007;175:477–485. PubMed PMC
Elder JF, Turner BJ. Concerted evolution of repetitive DNA sequences in eukaryotes. Quarterly Review of Biology. 1995;70:297–323. PubMed
Ferree PM, Prasad S. How can satellite DNA divergence cause reproductive isolation? Let us count the chromosomal ways. 2012. Genetics Research International Article ID 430136. PubMed PMC
Garrido-Ramos MA, de la Herran R, Ruiz Rejón C, Ruiz Rejón M. A satellite DNA of the Sparidae family (Pisces, Perciformes) associated with telomeric sequences. Cytogenetics and Cell Genetics. 1998;83:3–9. PubMed
Gong Z, Wu Y, Koblízková A, et al. Repeatless and repeat-based centromeres in potato: implications for centromere evolution. The Plant Cell. 2012;24:3559–3574. PubMed PMC
Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 1999;41:95–98.
He L, Jiang J, Liu J, et al. Interstitial telomeric repeats are enriched in the centromeres of chromosomes in Solanum species. Chromosome Research. 2013;21:5–13. PubMed
Heckmann S, Macas J, Kumke K, et al. The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. The Plant Journal. 2013;73:555–565. PubMed
Hemleben V, Kovařík A, Torres-Ruiz RA, Volkov RA, Beridze T. Plant highly repeated satellite DNA: molecular evolution, distribution and use for identification of hybrids. Systematics and Biodiversity. 2007;5:277–289.
de la Herrán R, Robles F, Cuñado N, et al. A heterochromatic satellite DNA is highly amplified in a single chromosome of Muscari (Hyacinthaceae) Chromosoma. 2001;110:197–202. PubMed
Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution. 2006;23:254–267. PubMed
Jang T-S, Emadzade K, Parker J, et al. Chromosomal diversification and karyotype evolution of diploids in the cytologically diverse genus Prospero (Hyacinthaceae) BMC Evolutionary Biology. 2013;13:136. PubMed PMC
Kato A, Yakura K, Tanifuji S. Sequence analysis of Vicia faba repeated DNA, the FokI repeat element. Nucleic Acids Research. 1984;12:6415–6426. PubMed PMC
Koukalova B, Moraes AP, Renny-Byfield S, Matyášek R, Leitch AR, Kovařík A. Fall and rise of satellite repeats in allopolyploids of Nicotiana over c. 5 million years. New Phytologist. 2010;186:148–160. PubMed
Kuhn GCS, Schwarzacher T, Heslop-Harrison JS. The non-regular orbit: three satellite DNAs in Drosophila martensis (buzzatii complex, repleta group) followed three different evolutionary pathways. Molecular Genetics and Genomics. 2010;284:251–262. PubMed
Liao D. Concerted evolution: molecular mechanism and biological implications. American Journal of Human Genetics. 1999;64:24–30. PubMed PMC
Lim KY, Skalicka K, Koukalova B. Dynamic changes in the distribution of a satellite homologous to intergenic 26–18S rDNA spacer in the evolution of Nicotiana. Genetics. 2004;166:1935–1946. PubMed PMC
Macas J, Pozárková D, Navrátilová A, Nouzová M, Neumann P. Two new families of tandem repeats isolated from genus Vicia using genomic self-priming PCR. Molecular and General Genetics. 2000;263:741–751. PubMed
Macas J, Mészáros T, Nouzová M. PlantSat: a specialized database for plant satellite repeats. Bioinformatics. 2002;18:28–35. PubMed
Macas J, Neumann P, Navrátilová A. Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics. 2007;8:427. PubMed PMC
Macas J, Neumann P, Novák P, Jiang J. Global sequence characterization of rice centromeric satellite based on oligomer frequency analysis in large-scale sequencing data. Bioinformatics. 2010;26:2101–2108. PubMed
Macas J, Kejnovský E, Neumann P, Novák P, Koblížková A, Vyskot B. Next generation sequencing-based analysis of repetitive DNA in the model dioecious plant Silene latifolia. PLoS One. 2011;6:e27335. PubMed PMC
Margulies M, Egholm M, Altman WE, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 2005;437:376–380. PubMed PMC
Martins C, Baptista CS, Ienne S, Cerqueira GC, Bartholomeu DC, Zingales B. Genomic organization and transcription analysis of the 195-bp satellite DNA in Trypanosoma cruzi. Molecular and Biochemical Parasitology. 2008;160:60–64. PubMed
Matyášek R, Fulnecek J, Leitch AR, Kovařík A. Analysis of two abundant, highly related satellites in the allotetraploid Nicotiana arentsii using double-strand conformation polymorphism analysis and sequencing. New Phytologist. 2011;192:747–759. PubMed
Meštrovič N, Plohl M, Mravinac B, Ugarković D. Evolution of satellite DNAs from the genus Palorus – experimental evidence for the ‘library’ hypothesis. Molecular Biology and Evolution. 1998;15:1062–1068. PubMed
Metcalfe CJ, Eldridge MDB, Johnston PG. Mapping the distribution of the telomeric sequence (T2AG3)n in the 2n = 14 ancestral marsupial complement and in the macropodines (Marsupialia: Macropodidae) by fluorescence in situ hybridization. Chromosome Research. 2004;12:405–414. PubMed
Meyne J, Baker RJ, Hobart HH, et al. Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma. 1990;99:3–10. PubMed
Mlinarec J, Chester M, Siljak-Yakovlev S, Papeš D, Leitch A, Besendorfer V. Molecular structure and chromosome distribution of three repetitive DNA families in Anemone hortensis L. (Ranunculaceae) Chromosome Research. 2009;17:331–346. PubMed
Mravinac B, Plohl M, Ugarković D. Preservation and high sequence conservation of satellite DNAs suggest functional constraints. Journal of Molecular Evolution. 2005;61:542–550. PubMed
Navajas-Pérez R, Quesada del Bosque ME, Garrido-Ramos MA. Effect of location, organization, and repeat-copy number in satellite-DNA evolution. Molecular Genetics and Genomics. 2009;282:395–406. PubMed
Navrátilová A, Koblízková A, Macas J. Survey of extrachromosomal circular DNA derived from plant satellite repeats. BMC Plant Biology. 2008;8:90. PubMed PMC
Nergadze SG, Rocchi M, Azzalin CM, Mondello C, Giulotto E. Insertion of telomeric repeats at intrachromosomal break sites during primate evolution. Genome Research. 2004;14:1704–1710. PubMed PMC
Nergadze SG, Santagostino M, Salzano A, Mondello C, Giulotto E. Contribution of telomerase RNA retrotranscription to DNA double-strand break repair during mammalian genome evolution. Genome Biology. 2007;8:R260. PubMed PMC
Nijman IJ, Lenstra JA. Mutation and recombination in cattle satellite DNA: a feedback model for the evolution of satellite DNA repeats. Journal of Molecular Evolution. 2001;52:361–371. PubMed
Novák P, Neumann P, Macas J. Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics. 2010;11:378. PubMed PMC
Novák P, Neumann P, Pech J, Steinhaisl J, Macas J. RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next generation sequence reads. Bioinformatics. 2013;29:792–793. PubMed
Park JM, Schneeweiss GM, Weiss-Schneeweiss H. Diversity and evolution of Ty1-copia and Ty3-gypsy retroelements in the non-photosynthetic flowering plants Orobanche and Phelipanche (Orobanchaceae) Gene. 2007;387:75–86. PubMed
Peacock WJ, Dennis ES, Rhoades MM, Pryor AJ. Highly repeated DNA sequence limited to knob heterochromatin in maize. Proceedings of the National Academy of Sciences, USA. 1981;78:4490–4494. PubMed PMC
Pezer Z, Brajković J, Feliciello I, Ugarkovć D. Satellite DNA-mediated effects on genome regulation. Genome Dynamics. 2012;7:153–169. PubMed
Pfosser M, Speta F. Phylogenetics of Hyacinthaceae based on plastid DNA sequences. Annals of the Missouri Botanical Garden. 1999;86:852–875.
Plohl M, Luchetti A, Meštrovič N, Mantovani B. Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero) chromatin. Gene. 2008;409:72–82. PubMed
Plohl M. Those mysterious sequences of satellite DNAs. Periodicum Biologorum. 2010;112:403–410.
Plohl M, Petrović V, Luchetti A, et al. Long-term conservation vs. high sequence divergence: the case of an extraordinarily old satellite DNA in bivalve mollusks. Heredity. 2010;104:543–551. PubMed
Pons J, Bruvo B, Petitpierre E, Plohl M, Ugarković D, Juan C. Complex structural features of satellite DNA sequences in the genus Pimelia (Coleoptera: Tenebrionidae): random differential amplification from a common ‘satellite DNA library. Heredity. 2004;92:418–427. PubMed
Presting GG, Frary A, Pillen K, Tanksley SD. Telomere-homologous sequences occur near the centromeres of many tomato chromosomes. Molecular and General Genetics. 1996;251:526–531. PubMed
Raskina O, Brodsky L, Belyayev A. Tandem repeats on an eco-geographical scale: outcomes from the genome of Aegilops speltoides. Chromosome Research. 2011;19:607–623. PubMed
Ribeiro T, dos Santos KGB, Fonsêca A, Pedrosa-Harand A. Isolation and characterization of a new repetitive DNA family recently amplified in the Mesoamerican gene pool of the common bean (Phaseolus vulgaris L., Fabaceae) Genetica. 2011;139:1135–1142. PubMed
Richard GF, Kerrest A, Dujon B. Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiology and Molecular Biology Reviews. 2008;72:686–727. PubMed PMC
Rosato M, Galián JA, Rosselló JA. Amplification, contraction and genomic spread of a satellite DNA family (E180) in Medicago (Fabaceae) and allied genera. Annals of Botany. 2012;109:773–782. PubMed PMC
Ruiz-Herra A, Nergadze SG, Santagostino M, Giulotto E. Telomeric repeats far from the ends: mechanisms of origin and role in evolution. Cytogenetics and Genome Research. 2008;122:219–228. PubMed
Sarri V, Minelli S, Panara F, et al. Characterization and chromosomal organization of satellite DNA sequences in Picea abies. Genome. 2008;51:705–713. PubMed
Schmidt T, Heslop-Harrison JS. Genomes, genes and junk: the large-scale organization of plant chromosomes. Trends in Plant Sciences. 1998;3:195–199.
Schneider TD, Stephens R. Sequence logos: a new way to display consensus sequences. Nucleic Acids Research. 1990;18:6097–6100. PubMed PMC
Sharma A, Wolfgruber TK, Presting GG. Tandem repeats derived from centromeric retrotransposons. BMC Genomics. 2013;14:142. PubMed PMC
Slijepcevic P, Xiao Y, Dominguez I, Natarajan AT. Spontaneous and radiation-induced chromosomal breakage at interstitial telomeric sites. Chromosoma. 1996;104:596–604. PubMed
Smith GP. Evolution of repeated DNA sequences by unequal crossover. Science. 1976;191:528–535. PubMed
Sonnhammer EL, Durbin R. A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene. 1995;167:GC1–10. PubMed
Speta F. Systematische Analyze der Gattung Scilla L. s. l. (Hyacinthaceae) Phyton. 1998;38:1–141.
Stephan W, Cho S. Possible role of natural selection in the formation of tandem-repetitive noncoding DNA. Genetics. 1994;136:333–341. PubMed PMC
Torres GA, Gong Z, Iovene M, et al. Organization and evolution of subtelomeric satellite repeats in the potato genome. G3 (Bethesda)s. 2011;1:85–92. PubMed PMC
Uchida W, Matsunaga S, Sugiyama R, Kawano S. Interstitial telomere-like repeats in the Arabidopsis thaliana genome. Genes and Genetic Systems. 2002;77:63–67. PubMed
Ugarković D. Functional elements residing within satellite DNAs. EMBO Reports. 2005;6:1035–1039. PubMed PMC
Ugarković D, Plohl M. Variation in satellite DNA profiles – causes and effects. EMBO Journal. 2002;21:5955–5959. PubMed PMC
Vaughan HE, Taylor S, Parker JS. The ten cytological races of the Scilla autumnalis species complex. Heredity. 1997;79:371–379.
Vittorazzi SE, Lourenço LB, Del-Grande ML, Recco-Pimentel SM. Satellite DNA derived from 5S rDNA in Physalaemus cuvieri (Anura, Leiuperidae) Cytogenetic and Genome Research. 2011;134:101–107. PubMed
Volkov RA, Komarova NY, Zentgraf U, Hemleben V. Molecular cell biology: epigenetic gene silencing in plants. Progress in Botany. 2006;67:101–133.
Walsh JB. Persistence of tandem arrays: implications for satellite and simple-sequence DNAs. Genetics. 1987;115:553–567. PubMed PMC
Weiss-Schneeweiss H, Riha K, Jang CG, Puizina J, Scherthan H, Schweizer D. Chromosome termini of the monocot plant Othocallis siberica are maintained by telomerase, which specifically synthesises vertebrate-type telomere sequences. The Plant Journal. 2004;37:484–493. PubMed
Weiss-Schneeweiss H, Schneeweiss GM. Karyotype diversity and evolutionary trends in angiosperms. In: Leitch IJ, Greilhuber J, Doležel J, Wendel JF, editors. Plant genome diversity, Vol 2. Physical structure, behavior and evolution of plant genomes. Wien: Springer-Verlag; 2013. pp. 209–230.
Wicker T, Taudien S, Houben A, et al. A whole genome snapshot of 454 sequences exposes the composition of the barley genome and provides evidence for parallel evolution of genome size in wheat and barley. The Plant Journal. 2009;59:712–722. PubMed
Willard HF. Centromeres: the missing link in the development of human artificial chromosomes. Current Opinion in Genetics and Development. 1998;8:219–225. PubMed
The Evolution of Chromosome Numbers: Mechanistic Models and Experimental Approaches
Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb
GENBANK
KF897587, KF897588, KF897589, KF897590, KF897591, KF897592, KF897593, KF897594, KF897595, KF897596, KF897597, KF897598, KF897599, KF897600, KF897601, KF897602, KF897603, KF897604, KF897605, KF897606, KF897607, KF897608, KF897609, KF897610, KF897611, KF897612, KF897613, KF897614, KF897615, KF897616, KF897617, KF897618, KF897619, KF897620, KF897621, KF897622, KF897623, KF897624, KF897625, KF897626, KF897627, KF897628, KF897629, KF897630, KF897631, KF897632, KF897633, KF897634, KF897635, KF897636, KF897637, KF897638, KF897639, KF897640, KF897641, KF897642, KF897643, KF897644, KF897645, KF897646, KF897647, KF897648, KF897649, KF897650, KF897651, KF897652