The repetitive content of the plant genome (repeatome) often represents its largest fraction and is frequently correlated with its size. Transposable elements (TEs), the main component of the repeatome, are an important driver in the genome diversification due to their fast-evolving nature. Hybridization and polyploidization events are hypothesized to induce massive bursts of TEs resulting, among other effects, in an increase of copy number and genome size. Little is known about the repeatome dynamics following hybridization and polyploidization in plants that reproduce by apomixis (asexual reproduction via seeds). To address this, we analyzed the repeatomes of two diploid parental species, Hieracium intybaceum and H. prenanthoides (sexual), their diploid F1 synthetic and their natural triploid hybrids (H. pallidiflorum and H. picroides, apomictic). Using low-coverage next-generation sequencing (NGS) and a graph-based clustering approach, we detected high overall similarity across all major repeatome categories between the parental species, despite their large phylogenetic distance. Medium and highly abundant repetitive elements comprise ∼70% of Hieracium genomes; most prevalent were Ty3/Gypsy chromovirus Tekay and Ty1/Copia Maximus-SIRE elements. No TE bursts were detected, neither in synthetic nor in natural hybrids, as TE abundance generally followed theoretical expectations based on parental genome dosage. Slight over- and under-representation of TE cluster abundances reflected individual differences in genome size. However, in comparative analyses, apomicts displayed an overabundance of pararetrovirus clusters not observed in synthetic hybrids. Substantial deviations were detected in rDNAs and satellite repeats, but these patterns were sample specific. rDNA and satellite repeats (three of them were newly developed as cytogenetic markers) were localized on chromosomes by fluorescence in situ hybridization (FISH). In a few cases, low-abundant repeats (5S rDNA and certain satellites) showed some discrepancy between NGS data and FISH results, which is due partly to the bias of low-coverage sequencing and partly to low amounts of the satellite repeats or their sequence divergence. Overall, satellite DNA (including rDNA) was markedly affected by hybridization, but independent of the ploidy or reproductive mode of the progeny, whereas bursts of TEs did not play an important role in the evolutionary history of Hieracium.

Institute of Botany Czech Academy of Sciences Průhonice Czechia

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Ågren J. A., Greiner S., Johnson M. T. J., Wright S. I. (2015). No evidence that sex and transposable elements drive genome size variation in evening primroses. Evolution 69 1053–1062. 10.1111/evo.12627 PubMed DOI

Akiyama Y., Hanna W. W., Ozias-Akins P. (2005). High-resolution physical mapping reveals that the apospory-specific genomic region (ASGR) in Cenchrus ciliaris is located on a heterochromatic and hemizygous region of a single chromosome. Theor. Appl. Genet. 111 1042–1051. 10.1007/s00122-005-0020-5 PubMed DOI

Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215 403–410. 10.1016/S0022-2836(05)80360-2 PubMed DOI

An Z., Tang Z., Ma B., Mason A. S., Guo Y., Yin J., et al. (2014). Transposon variation by order during allopolyploidisation between Brassica oleracea and Brassica rapa. Plant Biol. 16 825–835. 10.1111/plb.12121 PubMed DOI

Ávila Robledillo L., Koblížková A., Novák P., Böttinger K., Vrbová I., Neumann P., et al. (2018). Satellite DNA in Vicia faba is characterized by remarkable diversity in its sequence composition, association with centromeres, and replication timing. Sci. Rep. 8:5838. 10.1038/s41598-018-24196-3 PubMed DOI PMC

Beaulieu J., Jean M., Belzile F. (2009). The allotetraploid Arabidopsis thaliana–Arabidopsis lyrata subsp. petraea as an alternative model system for the study of polyploidy in plants. Mol. Genet. Genomics 281 421–435. 10.1007/s00438-008-0421-7 PubMed DOI

Belyayev A. (2014). Bursts of transposable elements as an evolutionary driving force. J. Evol. Biol. 27 2573–2584. 10.1111/jeb.12513 PubMed DOI

Belyayev A., Paštová L., Fehrer J., Josefiová J., Chrtek J., Mráz P. (2018). Mapping of Hieracium (Asteraceae) chromosomes with genus-specific satDNA elements derived from next-generation sequencing data. Plant Syst. Evol. 304 387–396. 10.1007/s00606-017-1483-y DOI

Ben-David S., Yaakov B., Kashkush K. (2013). Genome-wide analysis of short interspersed nuclear elements SINES revealed high sequence conservation, gene association and retrotranspositional activity in wheat. Plant J. 76 201–210. 10.1111/tpj.12285 PubMed DOI PMC

Bennetzen J. L., Ma J., Devos K. M. (2005). Mechanisms of recent genome size variation in flowering plants. Ann. Bot. 95 127–132. 10.1093/aob/mci008 PubMed DOI PMC

Benson G. (1999). Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27 573–580. 10.1093/nar/27.2.573 PubMed DOI PMC

Bräutigam S., Greuter W. (2007). A new treatment of Pilosella for the Euro-Mediterranean flora [Notulae ad floram euro-mediterraneam pertinentes 24]. Willdenowia 37 123–137. 10.3372/wi.37.37106 DOI

Casacuberta E., González J. (2013). The impact of transposable elements in environmental adaptation. Mol. Ecol. 22 1503–1517. 10.1111/mec.12170 PubMed DOI

Charlesworth B., Langley C. H. (1986). The evolution of self-regulated transposition of transposable elements. Genetics 112:359. PubMed PMC

Chrtek J., Jr., Zahradníček J., Krak K., Fehrer J. (2009). Genome size in Hieracium subgenus Hieracium (Asteraceae) is strongly correlated with major phylogenetic groups. Ann. Bot. 104 161–178. 10.1093/aob/mcp107 PubMed DOI PMC

Chrtek J., Mráz P., Belyayev A., Paštová L., Mrázová V., Caklová P., et al. (2020). Evolutionary history and genetic diversity of apomictic allopolyploids in Hieracium s.str.: morphological versus genomic features. Am. J. Bot. 107 66–90. 10.1002/ajb2.1413 PubMed DOI

Comai L. (2000). “Genetic and epigenetic interactions in allopolyploid plants,” in Plant Gene Silencing, eds Matzke M. A., Matzke A. J. M. (Dordrecht: Springer Netherlands; ), 267–279. 10.1007/978-94-011-4183-3_19 PubMed DOI

Docking T. R., Saadé F. E., Elliott M. C., Schoen D. J. (2006). Retrotransposon sequence variation in four asexual plant species. J. Mol. Evol. 62 375–387. 10.1007/s00239-004-0350-y PubMed DOI

Dodsworth S., Jang T.-S., Struebig M., Chase M. W., Weiss-Schneeweiss H., Leitch A. R. (2017). 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

Dolgin E. S., Charlesworth B. (2006). The fate of transposable elements in asexual populations. Genetics 174:817. 10.1534/genetics.106.060434 PubMed DOI PMC

Dubin M. J., Mittelsten Scheid O., Becker C. (2018). Transposons: a blessing curse. Curr. Opin. Plant Biol. 42 23–29. 10.1016/j.pbi.2018.01.003 PubMed DOI

Fehrer J., Gemeinholzer B., Chrtek J., Bräutigam S. (2007). Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae). Mol. Phylogenet. Evol. 42 347–361. 10.1016/j.ympev.2006.07.004 PubMed DOI

Fehrer J., Krak K., Chrtek J. (2009). Intra-individual polymorphism in diploid and apomictic polyploid hawkweeds (Hieracium, Lactuceae, Asteraceae): disentangling phylogenetic signal, reticulation, and noise. BMC Evol. Biol. 9:239. 10.1186/1471-2148-9-239 PubMed DOI PMC

Ferreira de Carvalho J., de Jager V., van Gurp T. P., Wagemaker N. C. A. M., Verhoeven K. J. F. (2016). Recent and dynamic transposable elements contribute to genomic divergence under asexuality. BMC Genomics 17:884. 10.1186/s12864-016-3234-9 PubMed DOI PMC

Galindo-González L., Mhiri C., Deyholos M. K., Grandbastien M.-A. (2017). LTR-retrotransposons in plants: engines of evolution. Gene 626 14–25. 10.1016/j.gene.2017.04.051 PubMed DOI

Glémin S., Galtier N. (2012). “Genome evolution in outcrossing versus selfing versus asexual species,” in Evolutionary Genomics: Statistical and Computational Methods, Vol. 1 ed. Anisimova M. (Totowa, NJ: Humana Press; ), 311–335. 10.1007/978-1-61779-582-4_11 PubMed DOI

Hake A. A., Shirasawa K., Yadawad A., Nadaf H. L., Gowda M. V. C., Bhat R. S. (2018). Genome-wide structural mutations among the lines resulting from genetic instability in peanut (Arachis hypogaea L.). Plant Gene 13 1–7. 10.1016/j.plgene.2017.11.001 DOI

Hall T. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 95–98.

Hemleben V., Kovarik A., Torres-Ruiz R. A., Volkov R. A., Beridze T. (2007). Plant highly repeated satellite DNA: molecular evolution, distribution and use for identification of hybrids. Syst. Biodiv. 5 277–289. 10.1017/S147720000700240X DOI

Hickey D. A. (1982). Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101:519. PubMed PMC

Jurka J., Kapitonov V. V., Pavlicek A., Klonowski P., Kohany O., Walichiewicz J. (2005). Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110 462–467. 10.1159/000084979 PubMed DOI

Kaplan Z., Jarolímová V., Fehrer J. (2013). Revision of chromosome numbers of Potamogetonaceae: a new basis for taxonomic and evolutionary implications. Preslia 85 421–482.

Kashkush K., Feldman M., Levy A. A. (2002). Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651. PubMed PMC

Kejnovsky E., Hawkins J. S., Feschotte C. (2012). “Plant transposable elements: biology and evolution,” in Plant Genome Diversity Volume 1: Plant Genomes, their Residents, and their Evolutionary Dynamics, eds Wendel J. F., Greilhuber J., Dolezel J., Leitch I. J. (Vienna: Springer Vienna; ), 17–34. 10.1007/978-3-7091-1130-7_2 DOI

Kraitshtein Z., Yaakov B., Khasdan V., Kashkush K. (2010). Genetic and epigenetic dynamics of a retrotransposon after allopolyploidization of wheat. Genetics 186:801. 10.1534/genetics.110.120790 PubMed DOI PMC

Krak K., Caklová P., Chrtek J., Fehrer J. (2013). Reconstruction of phylogenetic relationships in a highly reticulate group with deep coalescence and recent speciation (Hieracium, Asteraceae). Heredity 110 138–151. 10.1038/hdy.2012.100 PubMed DOI PMC

Krishnan P., Sapra V. T., Soliman K. M., Zipf A. (2001). FISH mapping of the 5S and 18S-28S rDNA loci in different species of Glycine. J. Heredity 92 295–300. 10.1093/jhered/92.3.295 PubMed DOI

Macas J., Kejnovský E., Neumann P., Novák P., Koblížková A., Vyskot B. (2011). Next generation sequencing-based analysis of repetitive DNA in the model dioceous plant Silene latifolia. PLoS One 6:e27335. 10.1371/journal.pone.0027335 PubMed DOI PMC

Madlung A., Tyagi A. P., Watson B., Jiang H., Kagochi T., Doerge R. W., et al. (2005). Genomic changes in synthetic Arabidopsis polyploids. Plant J. 41 221–230. 10.1111/j.1365-313X.2004.02297.x PubMed DOI

Majeský L’, Krahulec F., Vašut R. J. (2017). How apomictic taxa are treated in current taxonomy: a review. TAXON 66 1017–1040. 10.12705/665.3 DOI

Mascagni F., Giordani T., Ceccarelli M., Cavallini A., Natali L. (2017). Genome-wide analysis of LTR-retrotransposon diversity and its impact on the evolution of the genus Helianthus (L.). BMC Genomics 18:634. 10.1186/s12864-017-4050-6 PubMed DOI PMC

Matzke M., Gregor W., Mette M. F., Aufsatz W., Kanno T., Jakowitsch J., et al. (2004). Endogenous pararetroviruses of allotetraploid Nicotiana tabacum and its diploid progenitors, N. sylvestris and N. tomentosiformis. Biol. J. Linnean Soc. 82 627–638. 10.1111/j.1095-8312.2004.00347.x DOI

Maumus F., Quesneville H. (2014). Deep investigation of Arabidopsis thaliana junk DNA reveals a continuum between repetitive elements and genomic dark matter. PLoS One 9:e94101. 10.1371/journal.pone.0094101 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

McClintock B. (1984). The significance of responses of the genome to challenge. Science 226 792–801. 10.1126/science.15739260 PubMed DOI

Mestiri I., Chagué V., Tanguy A.-M., Huneau C., Huteau V., Belcram H., et al. (2010). Newly synthesized wheat allohexaploids display progenitor-dependent meiotic stability and aneuploidy but structural genomic additivity. New Phytol. 186 86–101. 10.1111/j.1469-8137.2010.03186.x PubMed DOI

Mlinarec J., Skuhala A., Jurković A., Malenica N., McCann J., Weiss-Schneeweiss H., et al. (2019). The repetitive DNA composition in the natural pesticide producer Tanacetum cinerariifolium: interindividual variation of subtelomeric tandem repeats. Front. Plant Sci. 10:613. 10.3389/fpls.2019.00613 PubMed DOI PMC

Mráz P., Zdvořák P. (2019). Reproductive pathways in Hieracium s.s. (Asteraceae): strict sexuality in diploids and apomixis in polyploids. Ann. Bot. 123 391–403. 10.1093/aob/mcy137 PubMed DOI PMC

Myburg A. A., Griffin A. R., Sederoff R. R., Whetten R. W. (2003). Comparative genetic linkage maps of Eucalyptus grandis, Eucalyptus globulus and their F1 hybrid based on a double pseudo-backcross mapping approach. Theor. Appl. Genet. 107 1028–1042. 10.1007/s00122-003-1347-4 PubMed DOI

Neumann P., Novák P., Hoštáková N., Macas J. (2019). Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mobile DNA 10:1. 10.1186/s13100-018-0144-1 PubMed DOI PMC

Noé L., Kucherov G. (2005). YASS: enhancing the sensitivity of DNA similarity search. Nucleic Acids Res. 33(suppl_2) W540–W543. 10.1093/nar/gki478 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. Bioinformatics 29 792–793. 10.1093/bioinformatics/btt054 PubMed DOI

Okada T., Ito K., Johnson S. D., Oelkers K., Suzuki G., Houben A., et al. (2011). Chromosomes carrying meiotic avoidance loci in three apomictic eudicot Hieracium subgenus Pilosella species share structural features with two monocot apomicts. Plant Physiol. 157:1327. 10.1104/pp.111.181164 PubMed DOI PMC

Okamoto H., Hirochika H. (2001). Silencing of transposable elements in plants. Trends Plant Sci. 6 527–534. 10.1016/S1360-1385(01)02105-7 PubMed DOI

Parisod C., Salmon A., Zerjal T., Tenaillon M., Grandbastien M.-A., Ainouche M. (2009). Rapid structural and epigenetic reorganization near transposable elements in hybrid and allopolyploid genomes in Spartina. New Phytol. 184 1003–1015. 10.1111/j.1469-8137.2009.03029.x PubMed DOI

Parisod C., Senerchia N. (2012). “Responses of Transposable Elements to Polyploidy,” in Plant Transposable Elements: Impact on Genome Structure and Function, eds Grandbastien M.-A., Casacuberta J. M. (Berlin: Springer Berlin; ), 147–168. 10.1007/978-3-642-31842-9_9 DOI

Petit M., Guidat C., Daniel J., Denis E., Montoriol E., Bui Q. T., et al. (2010). Mobilization of retrotransposons in synthetic allotetraploid tobacco. New Phytol. 186 135–147. 10.1111/j.1469-8137.2009.03140.x PubMed DOI

Piednoël M., Sousa A., Renner S. S. (2015). Transposable elements in a clade of three tetraploids and a diploid relative, focusing on Gypsy amplification. Mobile DNA 6:5. 10.1186/s13100-015-0034-8 PubMed DOI PMC

R Core Development Team (2018). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Renny-Byfield S., Kovarik 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

Rosato M., Kovařík A., Garilleti R., Rosselló J. A. (2016). Conserved organisation of 45S rDNA sites and rDNA gene copy number among major clades of early land plants. PLoS One 11:e0162544. 10.1371/journal.pone.0162544 PubMed DOI PMC

Sarilar V., Marmagne A., Brabant P., Joets J., Alix K. (2011). BraSto, a Stowaway MITE from Brassica: recently active copies preferentially accumulate in the gene space. Plant Mol. Biol. 77 59–75. 10.1007/s11103-011-9794-9 PubMed DOI

Sarilar V., Palacios P. M., Rousselet A., Ridel C., Falque M., Eber F., et al. (2013). Allopolyploidy has a moderate impact on restructuring at three contrasting transposable element insertion sites in resynthesized Brassica napus allotetraploids. New Phytol. 198 593–604. 10.1111/nph.12156 PubMed DOI

Shan X., Liu Z., Dong Z., Wang Y., Chen Y., Lin X., et al. (2005). Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Mol. Biol. Evol. 22 976–990. 10.1093/molbev/msi082 PubMed DOI

Staginnus C., Gregor W., Mette M. F., Teo C. H., Borroto-Fernández E. G., Machado M. L. D. C., et al. (2007). Endogenous pararetroviral sequences in tomato (Solanum lycopersicum) and related species. BMC Plant Biol. 7:24. 10.1186/1471-2229-7-24 PubMed DOI PMC

Staton S. E., Burke J. M. (2015). Evolutionary transitions in the Asteraceae coincide with marked shifts in transposable element abundance. BMC Genomics 16:623. 10.1186/s12864-015-1830-8 PubMed DOI PMC

Stupar R. M., Song J., Tek A. L., Cheng Z., Dong F., Jiang J. (2002). Highly condensed potato pericentromeric heterochromatin contains rDNA-related tandem repeats. Genetics 162 1435. PubMed PMC

Valárik M., Bartoš J., Kovááová P., Kubaláková M., De Jong J. H., Doležel J. (2004). High-resolution FISH on super-stretched flow-sorted plant chromosomes. Plant J. 37 940–950. 10.1111/j.1365-313X.2003.02010.x PubMed DOI

van Dijk E. L., Jaszczyszyn Y., Thermes C. (2014). Library preparation methods for next-generation sequencing: tone down the bias. Exp. Cell Res. 322 12–20. 10.1016/j.yexcr.2014.01.008 PubMed DOI

Van Dijk P. J., Vijverberg K. (2005). “The significance of apomixis in the evolution of the angiosperms: a reappraisal,” in Plant Species−Level Systematics: New Perspectives on Pattern and Process, eds Bakker L. C. F., Gravendeel B., Pelser P. B. (Ruggell: Gantner Verlag; ), 101–116.

Vicient C. M., Casacuberta J. M. (2017). Impact of transposable elements on polyploid plant genomes. Ann. Bot. 120 195–207. 10.1093/aob/mcx078 PubMed DOI PMC

Vitales D., Álvarez I., Garcia S., Hidalgo O., Nieto Feliner G., Pellicer J., et al. (2019). Genome size variation at constant chromosome number is not correlated with repetitive DNA dynamism in Anacyclus (Asteraceae). Ann. Bot. 125 611–623. 10.1093/aob/mcz183 PubMed DOI PMC

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. Nat. Rev. Genet. 8 973–982. 10.1038/nrg2165 PubMed DOI

Xu Y., Zhong L., Wu X., Fang X., Wang J. (2009). Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229 471–483. 10.1007/s00425-008-0844-8 PubMed DOI

Yaakov B., Kashkush K. (2010). Massive alterations of the methylation patterns around DNA transposons in the first four generations of a newly formed wheat allohexaploid. Genome 54 42–49. 10.1139/G10-091 PubMed DOI

Analysis of pericentromere composition and structure elucidated the history of the Hieracium alpinum L. genome, revealing waves of transposable elements insertions

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Molecular Evolution and Organization of Ribosomal DNA in the Hawkweed Tribe Hieraciinae (Cichorieae, Asteraceae)