Plant genomes are highly diverse in size and repetitive DNA composition. In the absence of polyploidy, the dynamics of repetitive elements, which make up the bulk of the genome in many species, are the main drivers underpinning changes in genome size and the overall evolution of the genomic landscape. The advent of high-throughput sequencing technologies has enabled investigation of genome evolutionary dynamics beyond model plants to provide exciting new insights in species across the biodiversity of life. Here we analyze the evolution of repetitive DNA in two closely related species of Heloniopsis (Melanthiaceae), which despite having the same chromosome number differ nearly twofold in genome size [i.e., H. umbellata (1C = 4,680 Mb), and H. koreana (1C = 2,480 Mb)]. Low-coverage genome skimming and the RepeatExplorer2 pipeline were used to identify the main repeat families responsible for the significant differences in genome sizes. Patterns of repeat evolution were found to correlate with genome size with the main classes of transposable elements identified being twice as abundant in the larger genome of H. umbellata compared with H. koreana. In addition, among the satellite DNA families recovered, a single shared satellite (HeloSAT) was shown to have contributed significantly to the genome expansion of H. umbellata. Evolutionary changes in repetitive DNA composition and genome size indicate that the differences in genome size between these species have been underpinned by the activity of several distinct repeat lineages.

Faculty of Sciences University of Masaryk Brno Czechia

Institut Botànic de Barcelona Barcelona Spain

Royal Botanic Gardens Kew Richmond United Kingdom

School of Plant Biology University of Western Australia Crawley WA Australia

Front Genet. 2021 Nov 03;12:799661. doi: 10.3389/fgene.2021.799661. PubMed

Zobrazit více v PubMed

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 (N. Y.) 69 1053–1062. 10.1111/evo.12627 PubMed DOI

Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., et al. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 3389–3402. 10.1093/nar/25.17.3389 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

Cossu R. M., Casola C., Giacomello S., Vidalis A., Scofield D. G., Zuccolo A. (2017). LTR retrotransposons show low levels of unequal recombination and high rates of intraelement gene conversion in large plant genomes. Genome Biol. Evol. 9 3449–3462. 10.1093/gbe/evx260 PubMed DOI PMC

Cuadrado Á, Golczyk H., Jouve N. (2009). A novel, simple and rapid nondenaturing FISH (ND-FISH) technique for the detection of plant telomeres. Potential used and possible target structures detected. Chromosom. Res. 17:755. 10.1007/s10577-009-9060-z PubMed DOI

de Assis R., Baba V. Y., Cintra L. A., Gonçalves L. S. A., Rodrigues R., Vanzela A. L. L. (2020). Genome relationships and LTR-retrotransposon diversity in three cultivated Capsicum L. (Solanaceae) species. BMC Genomics 21:237. 10.1186/s12864-020-6618-9 PubMed DOI PMC

Devos K. M., Brown J. K. M., Bennetzen J. (2002). Genome size seduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12 1075–1079. 10.1101/gr.132102 PubMed DOI PMC

Divashuk M. G., Karlov G. I., Kroupin P. Y. (2020). Copy number variation of transposable elements in Thinopyrum intermedium and its diploid relative species. Plants 9:15. 10.3390/plants9010015 PubMed DOI PMC

Doyle J. J., Doyle J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19 11–15.

Garrido-Ramos M. A. (2015). Satellite DNA in plants: more than just rubbish. Cytogenet. Genome Res. 146 153–170. 10.1159/000437008 PubMed DOI

Hawkins J. S., Kim H., Nason J. D., Wing R. A., Wendel J. F. (2006). Differential lineage-specific amplification of transposable elements is responsible for genome size variation in Gossypium. Genome Res. 16 1251–1261. 10.1101/gr.5282906 PubMed DOI PMC

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

Heckmann S., Macas J., Kumke K., Fuchs J., Schubert V., Ma L., et al. (2013). The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. Plant J. 73 555–565. 10.1111/tpj.12054 PubMed DOI

Hloušková P., Mandáková T., Pouch M., Trávníček P., Lysak M. A. (2019). The large genome size variation in the Hesperis clade was shaped by the prevalent proliferation of DNA repeats and rarer genome downsizing. Ann. Bot. 124 103–120. 10.1093/aob/mcz036 PubMed DOI PMC

Kato A., Lamb J. C., Albert P. S., Danilova T., Han F., Gao Z., et al. (2011). “Chromosome Painting for Plant Biotechnology,” in Plant Chromosome Engineering: Methods and Protocols, ed. Birchler J. A. (New York, NY: Springer; ), 67–96. 10.1007/978-1-61737-957-4_4 PubMed DOI

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

Kim C., Kim S.-C., Kim J.-H. (2019). Historical biogeography of Melanthiaceae: a case of out-of-North America through the Bering land bridge. Front. Plant Sci. 10:396. 10.3389/fpls.2019.00396 PubMed DOI PMC

Kim S.-C., Kim J. S., Chase M. W., Fay M. F., Kim J.-H. (2016). Molecular phylogenetic relationships of Melanthiaceae (Liliales) based on plastid DNA sequences. Bot. J. Linn. Soc. 181 567–584. 10.1111/boj.12405 DOI

Kokubugata G., Peng C. I., Yokota M. (2004). Comparison of karyotypes among three Heloniopsis species from Ryuku Archipelago and Taiwan. Ann. Tsukuba Bot. Gard. 23 13–16.

Lee Y.-I., Yap J. W., Izan S., Leitch I. J., Fay M. F., Lee Y.-C., et al. (2018). Satellite DNA in Paphiopedilum subgenus Parvisepalum as revealed by high-throughput sequencing and fluorescent in situ hybridization. BMC Genomics 19:578. 10.1186/s12864-018-4956-7 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., 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

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. Bioinformatics 26 2101–2108. PubMed

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

Mata-Sucre Y., Sader M., Van-Lume B., Gagnon E., Pedrosa-Harand A., Leitch I. J., et al. (2020). How diverse is heterochromatin in the Caesalpinia group? Cytogenomic characterization of Erythrostemon hughesii Gagnon & G.P. Lewis (Leguminosae: Caesalpinioideae). Planta 252:49. 10.1007/s00425-020-03453-8 PubMed DOI

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 saisies (Melampodium sect. Melampodium, Asteraceae). Syst. Biol. 67 1010–1024. 10.1093/sysbio/syy024 PubMed DOI PMC

McCann J., Macas J., Novák P., Stuessy T. F., Villaseñor J. L., Weiss-Schneeweiss H. (2020). Differential genome size and repetitive DNA evolution in diploid species of Melampodium sect. Melampodium (Asteraceae). Front. Plant Sci. 11:362. 10.3389/fpls.2020.00362 PubMed DOI PMC

Mian S. (2019). The Impact of Genomic Structural Variation on Meiotic Pairing and Segregation in Beta vulgaris subsp. maritima. Ph. D. thesis. London: Queen Mary University of London, 10.34885/61 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. Mob. DNA 10:1. 10.1186/s13100-018-0144-1 PubMed DOI PMC

Neumann P., Oliveira L., Čížková J., Jang T.-S., Klemme S., Novák P., et al. (2021). Impact of parasitic lifestyle and different types of centromere organization on chromosome and genome evolution in the plant genus Cuscuta. New Phytol. 229 2365–2377. 10.1111/nph.17003 PubMed DOI

Novák P., Guignard M. S., Neumann P., Kelly L. J., Mlinarec J., Koblížková A., et al. (2020a). Repeat-sequence turnover shifts fundamentally in species with large genomes. Nat. Plants. 6 1325–1329. 10.1038/s41477-020-00785-x PubMed DOI

Novák P., Neumann P., Macas J. (2020b). Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat. Protoc. 15 3745–3776. 10.1038/s41596-020-0400-y PubMed DOI

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

Nystedt B., Street N. R., Wetterbom A., Zuccolo A., Lin Y.-C., Scofield D. G., et al. (2013). The Norway spruce genome sequence and conifer genome evolution. Nature 497 579–584. 10.1038/nature12211 PubMed DOI

Pellicer J., Hidalgo O., Dodsworth S., Leitch I. J. (2018). Genome size diversity and its impact on the evolution of land plants. Genes (Basel). 9:88. 10.3390/genes9020088 PubMed DOI PMC

Pellicer J., Kelly L. J., Leitch I. J., Zomlefer W. B., Fay M. F. (2014). A universe of dwarfs and giants: genome size and chromosome evolution in the monocot family Melanthiaceae. New Phytol. 201 1484–1497. 10.1111/nph.12617 PubMed DOI

Pellicer J., Kelly L. J., Magdalena C., Leitch I. J. (2013). Insights into the dynamics of genome size and chromosome evolution in the early diverging angiosperm lineage Nymphaeales (water lilies). Genome 56 437–449. 10.1139/gen-2013-0039 PubMed DOI

Piegu B., Guyot R., Picault N., Roulin A., Sanyal A., Kim H., et al. (2006). Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res. 16 1262–1269. 10.1101/gr.5290206 PubMed DOI PMC

R Core Team (2019). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Revell L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3 217–223. 10.1111/j.2041-210X.2011.00169.x DOI

Sader M., Vaio M., Cauz-Santos L. A., Dornelas M. C., Vieira M. L. C., Melo N., et al. (2021). Large vs small genomes in Passiflora: the influence of the mobilome and the satellitome. Planta 253:86. 10.1007/s00425-021-03598-0 PubMed DOI

Schubert I., Vu G. T. H. (2016). Genome stability and evolution: attempting a holistic view. Trends Plant Sci. 21 749–757. 10.1016/j.tplants.2016.06.003 PubMed DOI

Vallès J., 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

Vitales D., Álvarez I., Garcia S., Hidalgo O., Nieto Feliner G., Pellicer J., et al. (2020). 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

Vu G. T. H., Cao H. X., Reiss B., Schubert I. (2017). Deletion-bias in DNA double-strand break repair differentially contributes to plant genome shrinkage. New Phytol. 214 1712–1721. 10.1111/nph.14490 PubMed DOI

Wang D., Zheng Z., Li Y., Hu H., Wang Z., Du X., et al. (2021). Which factors contribute most to genome size variation within angiosperms? Ecol. Evol. 11 2660–2668. 10.1002/ece3.7222 PubMed DOI PMC

Wang X., Morton J., Pellicer J., Leitch I. J., Leitch A. R. (2021). Genome downsizing after polyploidy: mechanisms, rates and selection pressures. Plant J. 10.1111/tpj.15363 [Epub ahead of print]. PubMed 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. Nat. Rev. Genet. 8 973–982. 10.1038/nrg2165 PubMed DOI

Wickham H. (2016). ggplot2: Elegant Graphics for Data Analysis, 2nd Edn. New York, NY: Springer-Verlag.

Cytomolecular diversity among Vigna Savi (Leguminosae) subgenera

Ancient hybridization and repetitive element proliferation in the evolutionary history of the monocot genus Amomum (Zingiberaceae)

The ecology of palm genomes: repeat-associated genome size expansion is constrained by aridity