Differential Genome Size and Repetitive DNA Evolution in Diploid Species of Melampodium sect. Melampodium (Asteraceae)
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
Grantová podpora
P 25131
Austrian Science Fund FWF - Austria
PubMed
32296454
PubMed Central
PMC7136903
DOI
10.3389/fpls.2020.00362
Knihovny.cz E-zdroje
- Klíčová slova
- Bayesian analysis, Melampodium, ancestral state reconstruction, genome size, phylogenetics, repetitive DNA, tandem repeats, transposable elements,
- Publikační typ
- časopisecké články MeSH
Plant genomes vary greatly in composition and size mainly due to the diversity of repetitive DNAs and the inherent propensity for their amplification and removal from the host genome. Most studies addressing repeatome dynamics focus on model organisms, whereas few provide comprehensive investigations across the genomes of related taxa. Herein, we analyze the evolution of repeats of the 13 species in Melampodium sect. Melampodium, representing all but two of its diploid taxa, in a phylogenetic context. The investigated genomes range in size from 0.49 to 2.27 pg/1C (ca. 4.5-fold variation), despite having the same base chromosome number (x = 10) and very strong phylogenetic affinities. Phylogenetic analysis performed in BEAST and ancestral genome size reconstruction revealed mixed patterns of genome size increases and decreases across the group. High-throughput genome skimming and the RepeatExplorer pipeline were utilized to determine the repeat families responsible for the differences in observed genome sizes. Patterns of repeat evolution were found to be highly correlated with phylogenetic position, namely taxonomic series circumscription. Major differences found were in the abundances of the SIRE (Ty1-copia), Athila (Ty3-gypsy), and CACTA (DNA transposon) lineages. Additionally, several satellite DNA families were found to be highly group-specific, although their overall contribution to genome size variation was relatively small. Evolutionary changes in repetitive DNA composition and genome size were complex, with independent patterns of genome up- and downsizing throughout the evolution of the analyzed diploids. A model-based analysis of genome size and repetitive DNA composition revealed evidence for strong phylogenetic signal and differential evolutionary rates of major lineages of repeats in the diploid genomes.
Department of Botany and Biodiversity Research University of Vienna Vienna Austria
Department of Botany National Autonomous University of Mexico Mexico City Mexico
Zobrazit více v PubMed
Albach D. C., Greilhuber J. (2004). Genome size variation and evolution in Veronica. Ann. Bot. 94 897–911. 10.1093/aob/mch219 PubMed DOI PMC
Barghini E., Natali L., Cossu R. M., Giordani T., Pindo M., Cattonaro F., et al. (2014). The peculiar landscape of repetitive sequences in the olive (Olea europaea L.) genome. Genome Biol. Evol. 6 776–791. 10.1093/gbe/evu058 PubMed DOI PMC
Belyayev A. (2014). Bursts of transposable elements as an evolutionary driving force. J. Evol. Biol. 27 2573–2584. 10.1111/jeb.12513 PubMed DOI
Bennetzen J. L. (2005). Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95 127–132. 10.1093/aob/mci008 PubMed DOI PMC
Bennetzen J. L., Wang H. (2014). The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu. Rev. Plant Biol. 65 505–530. 10.1146/annurev-arplant-050213-035811 PubMed DOI
Blöch C., Weiss-Schneeweiss H., Schneeweiss G. M., Barfuss M. H., Rebernig C. A., Villaseñor J. L., et al. (2009). Molecular phylogenetic analyses of nuclear and plastid DNA sequences support dysploid and polyploid chromosome number changes and reticulate evolution in the diversification of Melampodium (Millerieae, Asteraceae). Mol. Phyl. Evol. 53 220–233. 10.1016/j.ympev.2009.02.021 PubMed DOI PMC
Bloomberg S. P., Garland J. T., Ives A. R., Crespi B. (2003). Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57 717–745. 10.1111/j.0014-3820.2003.tb00285.x PubMed DOI
Bouckaert R., Heled J., Kühnert D., Vaughan T., Wu C.-H., Xie D., et al. (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10:e1003537. 10.1371/journal.pcbi.1003537 PubMed DOI PMC
Cusimano N., Renner S. S. (2014). Ultrametric trees or phylograms for ancestral state reconstruction: does it matter? Taxon 63 721–726. 10.12705/634.14 DOI
Dodsworth S., Chase M. W., Kelly L. J., Leitch I. J., Macas J., Novak P., et al. (2015). Genomic repeat abundances contain phylogenetic signal. Syst. Biol. 64 112–126. 10.1093/sysbio/syu080 PubMed DOI PMC
Dodsworth S., Jang T.-S., Struebig M., Chase M. W., Weiss-Schneeweiss H., Leitch A. R. (2016). Genome-wide repeat dynamics reflect phylogenetic distance in closely related allotetraploid Nicotiana (Solanaceae). Plant Syst. Evol. 303 1013–1020. 10.1007/s00606-016-1356-9 PubMed DOI PMC
Edgar R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 1792–1797. 10.1093/nar/gkh340 PubMed DOI PMC
Felsenstein J. (1985). Phylogenies and the comparative method. Am. Nat. 125 1–15. 10.1086/286013 DOI
Felsenstein J. (1993). PHYLIP: Phylogenetic Inference Package, Version 3.5. Available online at: http://evolution.genetics.washington.edu/phylip.html (accessed July 14, 2015).
Fleischmann A., Michael T. P., Rivadavia F., Sousa A., Wang W., Temsch E. M., et al. (2014). Evolution of genome size and chromosome number in the carnivorous plant genus Genlisea (Lentibulariaceae), with a new estimate of the minimum genome size in angiosperms. Ann. Bot. 114 1651–1663. 10.1093/aob/mcu189 PubMed DOI PMC
Garrido-Ramos M. A. (2015). Satellite DNA in plants: more than just rubbish. Cytogenet. Genome Res. 146 153–170. 10.1159/000437008 PubMed DOI
Harmon L. J., Losos J. B., Davies J. T., Gillespie R. G., Gittleman J. L., Bryan Jennings W., et al. (2010). Early bursts of body size and shape evolution are rare in comparative data. Evolution 64 2385–2396. 10.1111/j.1558-5646.2010.01025.x PubMed DOI
Hawkins J. S., Proulx S. R., Rapp R. A., Wendel J. F. (2009). Rapid DNA loss as a counterbalance to genome expansion through retrotransposon proliferation in plants. Proc. Natl. Acad. Sci. U.S.A. 106 17811–17816. 10.1073/pnas.0904339106 PubMed DOI PMC
Heslop-Harrison J. S., Murata M., Ogura Y., Schwarzacher T., Motoyoshi F. (1999). Polymorphisms and genomic organization of repetitive DNA from centromeric regions of Arabidopsis chromosomes. Plant Cell 11 31–42. 10.1105/tpc.11.1.31 PubMed DOI PMC
Höhna S., Landis M. J., Heath T. A., Boussau B., Lartillot N., Moore B. R., et al. (2016). RevBayes: bayesian phylogenetic inference using graphical models and an interactive model-specification language. Syst. Biol. 65 726–736. 10.1093/sysbio/syw021 PubMed DOI PMC
Horvilleur B., Lartillot N. (2014). Monte Carlo algorithms for Brownian phylogenetic models. Bioinform. 30 3020–3028. 10.1093/bioinformatics/btu485 PubMed DOI PMC
Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., et al. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinform. 28 1647–1649. 10.1093/bioinformatics/bts199 PubMed DOI PMC
Kelly L. J., Renny-Byfield S., Pellicer J., Macas J., Novák P., Neumann P., et al. (2015). Analysis of the giant genomes of Fritillaria (Liliaceae) indicates that a lack of DNA removal characterizes extreme expansions in genome size. New Phytol. 208 596–607. 10.1111/nph.13471 PubMed DOI PMC
Kovařík A., Dadejova M., Lim Y. K., Chase M. W., Clarkson J. J., Knapp S., et al. (2008). Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann. Bot. 101 815–823. 10.1093/aob/mcn019 PubMed DOI PMC
Lysak M. A., Koch M. A., Beaulieu J. M., Meister A., Leitch I. J. (2009). The dynamic ups and downs of genome size evolution in Brassicaceae. Mol. Biol. Evol. 26 85–98. 10.1093/molbev/msn223 PubMed DOI
Macas J., Meszaros T., Nouzova M. (2002). PlantSat: a specialized database for plant satellite repeats. Bioinform 18 28–35. 10.1093/bioinformatics/18.1.28 PubMed DOI
Macas J., Neumann P., Novák P., Jiang J. (2010). Global sequence characterization of rice centromeric satellite based on oligomer frequency analysis in large-scale sequencing data. Bioinform. 26 2101–2108. 10.1093/bioinformatics/btq343 PubMed DOI
Macas J., Novák P., Pellicer J., Čížková J., Koblížková A., Neumann P., et al. (2015). In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe Fabeae. PLoS One 10:e0143424. 10.1371/journal.pone.0143424 PubMed DOI PMC
McCann J., Jang T.-S., Macas J., Schneeweiss G. M., Matzke N. J., Novák P., et al. (2018). Dating the species network: allopolyploidy and repetitive DNA evolution in American daisies (Melampodium sect. Melampodium, Asteraceae). Syst. Biol. 67 1010–1024. 10.1093/sysbio/syy024 PubMed DOI PMC
McCann J., Schneeweiss G. M., Stuessy T. F., Villaseñor J. L., Weiss-Schneeweiss H. (2016). The impact of reconstruction methods, phylogenetic uncertainty and branch lengths on inference of chromosome number evolution in American daisies (Melampodium. Asteraceae). PLoS One 11:e0162299. 10.1371/journal.pone.0162299 PubMed DOI PMC
Melters D. P., Bradnam K. R., Young H. A., Telis N., May M. R., Ruby J. G., et al. (2013). Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution. Genome Biol. 14:R10. 10.1186/gb-2013-14-1-r10 PubMed DOI PMC
Natali L., Cossu R. M., Barghini E., Giordani T., Buti M., Mascagni F., et al. (2013). The repetitive component of the sunflower genome as shown by different procedures for assembling next generation sequencing reads. BMC Genom. 14:686. 10.1186/1471-2164-14-686 PubMed DOI PMC
Novák P., Hřibová E., Neumann P., Koblížková A., Doležel J., Macas J. (2014). Genome-wide analysis of repeat diversity across the family Musaceae. PLoS One 9:e98918. 10.1371/journal.pone.0098918 PubMed DOI PMC
Novák P., Neumann P., Macas J. (2010). Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinform 11:378. 10.1186/1471-2105-11-378 PubMed DOI PMC
Novák P., Neumann P., Pech J., Steinhaisl J., Macas J. (2013). RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinform 29 792–793. 10.1093/bioinformatics/btt054 PubMed DOI
Ogilvie H. A., Drummond A. J. (2016). StarBEAST2 brings faster species tree inference and accurate estimates of substitution rates. BioRxiv [preprint]. 10.1093/molbev/msx126 PubMed DOI PMC
Pagel M., Meade A. (2004). BayesTraits Manual. Available online at: www.evolution.rdg.ac.uk/BayesTraits.html (accessed December 12, 2015).
Pellicer J., Fay M. F., Leitch I. J. (2010). The largest eukaryotic genome of them all? Bot. J. Linn. Soc. 164 10–15. 10.1111/j.1095-8339.2010.01072.x DOI
Plummer M., Best N., Cowles K., Vines K. (2006). CODA: convergence diagnosis and output analysis for MCMC. R News 6 7–11.
Rambaut A. (2007). Tracer Version 1.6. Available online at: http://beast.bio.ed.ac.uk/Tracer (accessed February 22, 2016).
Rebernig C. A., Weiss-Schneeweiss H., Blöch C., Turner B., Stuessy T. F., Obermayer R., et al. (2012). The evolutionary history of the white-rayed species of Melampodium (Asteraceae) involved multiple cycles of hybridization and polyploidization. Am. J. Bot. 99 1043–1057. 10.3732/ajb.1100539 PubMed DOI PMC
Renny-Byfield S., Chester M., Nichols R. A., Macas J. (2012). Independent, rapid and targeted loss of highly repetitive DNA in natural and synthetic allopolyploids of Nicotiana tabacum. PLoS One 7:e36963. 10.1371/journal.pone.0036963 PubMed DOI PMC
Renny-Byfield S., Kovařík A., Kelly L. J., Macas J., Novak P., Chase M. W., et al. (2013). Diploidization and genome size change in allopolyploids is associated with differential dynamics of low-and high-copy sequences. Plant J. 74 829–839. 10.1111/tpj.12168 PubMed DOI
Rudd M. K., Wray G. A., Willard H. F. (2006). The evolutionary dynamics of α-satellite. Genome Res. 16 88–96. 10.1101/gr.3810906 PubMed DOI PMC
Sonnhammer E. L. L., Durbin R. (1995). A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. Gene 167 1–10. 10.1016/0378-1119(95)00714-8 PubMed DOI
Stuessy T. F., Blöch C., Villaseñor J. L., Rebernig C. A., Weiss-Schneeweiss H. (2011). Phylogenetic analyses of DNA sequences with chromosomal and morphological data confirm and refine sectional and series classification within Melampodium (Asteraceae. Millerieae). Taxon 60 436–449. 10.1002/tax.602013 DOI
Tek A. L., Song J., Macas J., Jiang J. (2005). Sobo, a recently amplified satellite repeat of potato, and its implications for the origin of tandemly repeated sequences. Genetics 170 1231–1238. 10.1534/genetics.105.041087 PubMed DOI PMC
Ugarković Ð. (2008). Satellite DNA libraries and centromere evolution. Open Evol. J. 2 1–6. 10.2174/1874404400802010001 DOI
Ugarković Ð, Plohl M. (2002). Variation in satellite DNA profiles—causes and effects. EMBO J. 21 5955–5959. 10.1093/emboj/cdf612 PubMed DOI PMC
Vallès, Canela M. Á, Garcia S., Hidalgo O., Pellicer J., Sánchez-Jiménez I., et al. (2013). Genome size variation and evolution in the family Asteraceae. Caryologia 66 221–235. 10.1080/00087114.2013.829690 DOI
Vu G. T. H., Schmutzer T., Bull F., Cao H. X., Fuchs J., Tran T. D., et al. (2015). Comparative genome analysis reveals divergent genome size evolution in a carnivorous plant genus. Plant Genome 8 1–14. 10.3835/plantgenome2015.04.0021 PubMed DOI
Weiss-Schneeweiss H., Blöch C., Turner B., Villaseñor J. L., Stuessy T. F., Schneeweiss G. M. (2012). The promiscuous and the chaste: frequent allopolyploid speciation and its genomic consequences in American daisies (Melampodium sect. Melampodium; Asteraceae). Evolution 66 211–228. 10.1111/j.1558-5646.2011.01424.x PubMed DOI
Weiss-Schneeweiss H., Leitch A. R., McCann J., Jang T.-S., Macas J. (2015). “Employing next generation sequencing to explore the repeat landscape of the plant genome,” in Next Generation Sequencing in Plant Systematics, Regnum Vegetabile 157, eds Hörandl E., Appelhans M. (Königstein: Koeltz Scientific Books; ), 155–180.
Weiss-Schneeweiss H., Stuessy T. F., Villaseñor J. L. (2009). Chromosome numbers, karyotypes, and evolution in Melampodium (Asteraceae). Int. J. Plant Sci. 170 1168–1182. 10.1086/605876 DOI
Wicker T., Sabot F., Hua-Van A., Bennetzen J. L., Capy P., Chalhoub B., et al. (2007). A unified classification system for eukaryotic transposable elements. Nature Rev. Genet. 8 973–982. 10.1038/nrg2165 PubMed DOI
Zozomová-Lihová J., Mandáková T., Kovaříková A., Mühlhausen A., Mummenhoff K., Lysak M. A., et al. (2014). When fathers are instant losers: homogenization of rDNA loci in recently formed Cardamine schulzii trigenomic allopolyploid. New Phytol. 203 1096–1108. 10.1111/nph.12873 PubMed DOI
Cytomolecular diversity among Vigna Savi (Leguminosae) subgenera
Evolution of Tandem Repeats Is Mirroring Post-polyploid Cladogenesis in Heliophila (Brassicaceae)