Differential amplification of satellite PaB6 in chromosomally hypervariable Prospero autumnale complex (Hyacinthaceae)

. 2014 Dec ; 114 (8) : 1597-608. [epub] 20140828

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25169019

Grantová podpora
P 21440 Austrian Science Fund FWF - Austria

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.

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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

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