LTR retrotransposons constitute a significant part of plant genomes and their evolutionary dynamics play an important role in genome size changes. Current methods of LTR retrotransposon age estimation are based only on LTR (long terminal repeat) divergence. This has prompted us to analyze sequence similarity of LTRs in 25,144 LTR retrotransposons from fifteen plant species as well as formation of solo LTRs. We found that approximately one fourth of nested retrotransposons showed a higher LTR divergence than the pre-existing retrotransposons into which they had been inserted. Moreover, LTR similarity was correlated with LTR length. We propose that gene conversion can contribute to this phenomenon. Gene conversion prediction in LTRs showed potential converted regions in 25% of LTR pairs. Gene conversion was higher in species with smaller genomes while the proportion of solo LTRs did not change with genome size in analyzed species. The negative correlation between the extent of gene conversion and the abundance of solo LTRs suggests interference between gene conversion and ectopic recombination. Since such phenomena limit the traditional methods of LTR retrotransposon age estimation, we recommend an improved approach based on the exclusion of regions affected by gene conversion.

Department of Plant Developmental Genetics Institute of Biophysics of the Czech Academy of Sciences Brno Czechia

Faculty of Informatics Masaryk University Brno Czechia

Zobrazit více v PubMed

Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. (1990). Basic local alignment search tool. PubMed DOI

Banks J. A., Nishiyama T., Hasebe M., Bowman J. L., Gribskov M., dePamphilis C., et al. (2011). The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. PubMed DOI PMC

Bennetzen J. L., Ma J., Devos K. M. (2005). Mechanisms of recent genome size variation in flowering plants. PubMed DOI PMC

Benovoy D., Drouin G. (2009). Ectopic gene conversions in the human genome. PubMed DOI

Bowen N. J., McDonald J. F. (2001). Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. PubMed DOI PMC

Charles M., Belcram H., Just J., Huneau C., Viollet A., Couloux A., et al. (2008). Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. PubMed DOI PMC

Choulet F., Wicker T., Rustenholz C., Paux E., Salse J., Leroy P., et al. (2010). Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. PubMed DOI PMC

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. PubMed DOI PMC

Cummings W. J., Yabuki M., Ordinario E. C., Bednarski D. W., Quay S., Maizels N. (2007). Chromatin structure regulates gene conversion. PubMed DOI PMC

Derr L. K. (1998). The involvement of cellular recombination and repair genes in RNA-mediated recombination in Saccharomyces cerevisiae. PubMed PMC

Derr L. K., Strathern J. N. (1993). A role of reverse transcription in gene conversion. PubMed DOI

Derr L. K., Strathern J. N., Garfinkel D. J. (1991). RNA-mediated recombination in PubMed DOI

Devos K. M., Brown J. K. M., Bennetzen J. L. (2002). Genome size reduction through illegitimate recombination counteracts genome expansion in PubMed DOI PMC

D’Hont A., Denoeud F., Aury J. (2012). The banana ( PubMed DOI

Doolittle W. F. (1985). RNA-mediated gene conversion? DOI

Du J., Tian Z., Hans C. S., Laten H. M., Cannon S. B., Jackson S. A., et al. (2012). Evolutionary conservation, diversity and specificity of LTR-retrotransposons in flowering plants: insight from genome-wide analysis and multi-specific comparison. PubMed DOI

Ezawa K., OOta S., Saitou N. (2006). Genome-wide search of gene conversions in duplicated genes of mouse and rat. PubMed DOI

Fedoroff N. V. (2012). Transposable elements, epigenetics, and genome evolution. PubMed DOI

Feschotte C., Jiang N., Wessler S. R. (2002). Plant transposable elements: where genetics meets genomics. PubMed DOI

Gaut B., Morton B. R., McCaig B. C., Clegg M. T. (1996). Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. PubMed DOI PMC

Giordano J., Ge Y., Gelfand Y., Abrusan G., Benson G., Warburton P. E. (2007). Evolutionary history of mammalian transposons determined by genome-wide defragmentation. PubMed DOI PMC

Goodstein D. M., Shu S., Howson R., Neupane R., Hayes R. D., Fazo J., et al. (2012). Phytozome: a comparative platform for green plant genomics. PubMed DOI PMC

Grandbastien M.-A. (1998). Activation of plant retrotransposons under stress conditions. DOI

Guindon S., Gascuel O. (2003). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. PubMed DOI

Hirochika H. (1997). Retrotransposons of rice: their regulation and use for genome analysis. PubMed DOI

Hosmani P. S., Flores-Gonzalez M., van de Geest H., Maumus F., Bakker L. V., Schijlen E., et al. (2019). An improved de novo assembly and annotation of the tomato reference genome using single-molecule sequencing, Hi-C proximity ligation and optical maps. DOI

International Brachypodium Initiative. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. PubMed DOI

Jurka J. (1998). Repeats in genomic DNA: mining and meaning. PubMed DOI

Kass D. H., Batzer M. A., Deininger P. L. (1995). Gene conversion as a secondary mechanism of short interspersed element (SINE) evolution. PubMed DOI PMC

Kejnovsky E., Hawkins J. S., Feschotte C. (2012). “Plant transposable elements: biology and evolution,” in DOI

Kejnovsky E., Hobza R., Kubat Z., Widmer A., Marais G. A. B., Vyskot B. (2007). High intrachromosomal similarity of retrotransposon long terminal repeats: evidence for homogenization by gene conversion on plant sex chromosomes? PubMed DOI

Kejnovsky E., Leitch I., Leitch A. (2009). Contrasting evolutionary dynamics between angiosperm and mammalian genomes. PubMed DOI

Kijima T. E., Innan H. (2009). On the estimation of the insertion time of LTR retrotransposable elements. PubMed DOI

Kim T.-M., Hong S.-J., Rhyu M.-G. (2004). Periodic explosive expansion of human retroelements associated with the evolution of the hominoid primate. PubMed DOI PMC

Koch M. A., Haubold B., Mitchell-Olds T. (2000). Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in PubMed DOI

Krzywinski J., Sangare D., Besansky N. J. (2005). Satellite DNA from the Y chromosome of the malarial vector Anopheles gambiae. PubMed DOI PMC

Lamesch P., Berardini T. Z., Li D., Swarbreck D., Wilks C., Sasidharan R., et al. (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. PubMed DOI PMC

Lang D., Ullrich K. K., Murat F., Fuchs J., Jenkins J., Haas F. B., et al. (2018). The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. PubMed DOI

Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., et al. (2007). Clustal W and Clustal X version 2.0. PubMed DOI

Lexa M., Lapar R., Jedlicka P., Vanat I., Cervenansky M., Kejnovsky E. (2018). “TE-nester: a recursive software tool for structure-based discovery of nested transposable elements,” in DOI

Li W. (1997).

Lim K. Y., Kovarik A., Matyasek R., Bezdek M., Lichtenstein C. P., Leitch A. R. (2000). Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. PubMed DOI

Llorens C., Futami R., Covelli L., Dominguez-Escriba L., Viu J. M., Tamarit D., et al. (2011). The gypsy database (GyDB) of mobile genetic elements: release 2.0. PubMed DOI PMC

Ma J., Bennetzen J. L. (2004). Rapid recent growth and divergence of rice nuclear genomes. PubMed DOI PMC

Ma J., Devos K. M., Bennetzen J. L. (2004). Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. PubMed DOI PMC

Macas J., Novak P., Pellicer J., Cizkova J., Koblizkova 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. PubMed DOI PMC

Mansai S. P., Innan H. (2010). The power of the methods for detecting interlocus gene conversion. PubMed DOI PMC

Mansai S. P., Kado T., Innan H. (2011). The rate and tract length of gene conversion between duplicated genes. PubMed DOI PMC

Martins H., Villesen P. (2011). Improved integration time estimation of endogenous retroviruses with phylogenetic data. PubMed DOI PMC

Maumus F., Quesneville H. (2014). Ancestral repeats have shaped epigenome and genome composition for millions of years in Arabidopsis thaliana. PubMed DOI PMC

McCormick R. F., Truong S. K., Sreedasyam A., Jenkins J., Shu S., Sims D., et al. (2017). The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization. PubMed DOI

Merchant S. S., Prochnik S. E., Vallon O., Harris E. H., Karpowicz S. J., Witman G. B., et al. (2007). The Chlamydomonas genome reveals the evolution of key animal and plant functions. PubMed DOI PMC

Neumann P., Novak P., Hostakova N., Macas J. (2019). Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. PubMed DOI PMC

Ou S., Jiang N. (2018). LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. PubMed DOI PMC

Ouyang S., Zhu W., Hamilton J., Lin H., Campbell M., Childs K., et al. (2007). The TIGR rice genome annotation resource: improvements and new features. PubMed DOI PMC

Pereira V. (2004). Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. PubMed DOI PMC

Pereira V. (2008). Automated paleontology of repetitive DNA with REANNOTATE. PubMed DOI PMC

Quinlan A. R., Hall I. M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. PubMed DOI PMC

Rawat V., Abdelsamad A., Pietzenuk B., Seymour D. K., Koenig D., Weigel D., et al. (2015). Improving the annotation of PubMed DOI PMC

Rice P., Longden I., Bleasby A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. PubMed DOI

Roeder G. S., Fink G. R. (1982). Movement of yeast transposable elements by gene conversion. PubMed DOI PMC

Roy A. M., Carrol M. L., Nguyen S. V., Salem A.-H., Oldridge M., Wilkie A. O. M., et al. (2000). Potential gene conversion and source genes for recently integrated Alu elements. PubMed DOI

SanMiguel P., Gaut B., Tikhonov A., Nakajima Y., Bennetzen J. L. (1998). The paleontology of intergene retrotransposons of maize. PubMed DOI

SanMiguel P. J., Ramakrishna W., Bennetzen J. L., Busso C., Dubcovsky J. (2002). Transposable elements, genes and recombination in a 215-kb contig from wheat chromosome 5Am. PubMed DOI

Sato S., Nakamura Y., Kaneko T., Asamizu E., Kato T., Nakao M., et al. (2008). Genome structure of the legume, PubMed DOI PMC

Sawyer S. A. (1999).

Schmutz J., Cannon S. B., Schlueter J., Ma J., Mitros T., Nelson W., et al. (2010). Genome sequence of the palaeopolyploid soybean. PubMed DOI

Schnable P. S., Ware D., Fulton R. S., Stein J. C., Wei F., Pasternak S., et al. (2009). The B73 maize genome: complexity, diversity, and dynamics. PubMed DOI

Sharma S. K., Bolser D., de Boer J., Sønderkær M., Amoros W., Carboni M. F., et al. (2013). Construction of reference chromosome-scale pseudomolecules for potato: integrating the potato genome with genetic and physical maps. PubMed DOI PMC

Shirazu K., Schulman A. H., Lahaye T., Schulze-Lefert P. (2000). A contiguous 66-kb barley DNA sequence provides evidence for reversible genome expansion. PubMed DOI PMC

Tang H., Krishnakumar V., Bidwell S., Rosen B., Chan A., Zhou S., et al. (2014). An improved genome release (version Mt4.0) for the model legume PubMed DOI PMC

Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution. PubMed DOI PMC

Trombetta B., Fantini G., D’Atanasio E., Sellitto D., Cruciani F. (2016). Evidence of extensive non-allelic gene conversion among LTR elements in the human genome. PubMed DOI PMC

Tuskan G. A., Difazio S., Jansson S., Bohlmann J., Grigoriev I., Hellsten U., et al. (2006). The genome of black cottonwood, PubMed DOI

Vitte C., Panaud O. (2003). Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice PubMed DOI

Vitte C., Panaud O. (2005). LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. PubMed DOI

Wicker T., Grundlach H., Spannagl M., Uauy C., Borrill P., Ramirez-Gonzales R. H., et al. (2018). Impact of transposable elements on genome structure and evolution in bread wheat. PubMed DOI PMC

Wicker T., Keller B. (2007). Genome-wide comparative analysis of PubMed DOI PMC

Wicker T., Yahiaoui N., Guyot R., Schlagenhauf E., Liu Z.-D., Dubcovsky J., et al. (2003). Rapid genome divergence at orthologous low molecular weight glutenin loci of the A and Am genomes of wheat. PubMed DOI PMC

Xu Y., Du J. (2014). Young but not relatively old retrotransposons are preferentially located in gene-rich euchromatic regions in tomato ( PubMed DOI

Xu Z., Wang H. (2007). LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. PubMed DOI PMC

Zhang Q. J., Gao L. Z. (2017). Rapid and recent evolution of LTR retrotransposons drives rice genome evolution during the speciation of AA-genome PubMed DOI PMC

Dynamic patterns of repeats and retrotransposons in the centromeres of Humulus lupulus L

Detection and classification of long terminal repeat sequences in plant LTR-retrotransposons and their analysis using explainable machine learning