What Can Long Terminal Repeats Tell Us About the Age of LTR Retrotransposons, Gene Conversion and Ectopic Recombination?

. 2020 ; 11 () : 644. [epub] 20200520

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32508870

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.

Zobrazit více v PubMed

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

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. Science 332 960–963. 10.1126/science.1203810 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

Benovoy D., Drouin G. (2009). Ectopic gene conversions in the human genome. Genomics 93 27–32. 10.1016/j.ygeno.2008.09.007 PubMed DOI

Bowen N. J., McDonald J. F. (2001). Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res. 11 1527–1540. 10.1101/gr.164201 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. Genetics 180 1071–1086. 10.1534/genetics.108.092304 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. Plant Cell 22 1686–1701. 10.1105/tpc.110.074187 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. Genome Biol. Evol. 9 3449–3462. 10.1093/gbe/evx260 PubMed DOI PMC

Cummings W. J., Yabuki M., Ordinario E. C., Bednarski D. W., Quay S., Maizels N. (2007). Chromatin structure regulates gene conversion. PLoS Biol. 5:e246. 10.1371/journal.pbio.0050246 PubMed DOI PMC

Derr L. K. (1998). The involvement of cellular recombination and repair genes in RNA-mediated recombination in Saccharomyces cerevisiae. Genetics 148 937–945. PubMed PMC

Derr L. K., Strathern J. N. (1993). A role of reverse transcription in gene conversion. Nature 361 170–173. 10.1038/361170a0 PubMed DOI

Derr L. K., Strathern J. N., Garfinkel D. J. (1991). RNA-mediated recombination in S. cerevisiae. Cell 67 355–364. 10.1016/0092-8674(91)90187-4 PubMed DOI

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

D’Hont A., Denoeud F., Aury J. (2012). The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488 213–217. 10.1038/nature11241 PubMed DOI

Doolittle W. F. (1985). RNA-mediated gene conversion? Trends Genet. 1 64–65. 10.1016/0168-9525(85)90028-9 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. Plant J. 63 584–598. 10.1111/j.1365-313X.2010.04263.x PubMed DOI

Ezawa K., OOta S., Saitou N. (2006). Genome-wide search of gene conversions in duplicated genes of mouse and rat. Mol. Biol. Evol. 23 927–940. 10.1093/molbev/msj093 PubMed DOI

Fedoroff N. V. (2012). Transposable elements, epigenetics, and genome evolution. Science 338 758–768. 10.1126/science.338.6108.758 PubMed DOI

Feschotte C., Jiang N., Wessler S. R. (2002). Plant transposable elements: where genetics meets genomics. Nat. Rev. Genet. 3 329–341. 10.1038/nrg793 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. Proc. Natl. Acad. Sci. U.S.A. 93 10274–10279. 10.1073/pnas.93.19.10274 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. PLoS Comp. Biol. 3:e137. 10.1371/journal.pcbi.0030137 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. Nucleic Acids Res. 40 D1178–D1186. 10.1093/nar/gkr944 PubMed DOI PMC

Grandbastien M.-A. (1998). Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3 181–187. 10.1016/S1360-1385(98)01232-1 DOI

Guindon S., Gascuel O. (2003). A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 696–704. 10.1080/10635150390235520 PubMed DOI

Hirochika H. (1997). Retrotransposons of rice: their regulation and use for genome analysis. Plant Mol. Biol. 35 231–240. 10.1023/A:100577470 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. bioRxiv [Preprint]. 10.1101/767764 DOI

International Brachypodium Initiative. (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463 763–768. 10.1038/nature08747 PubMed DOI

Jurka J. (1998). Repeats in genomic DNA: mining and meaning. Curr. Opin. Struct. Biol. 8 333–337. 10.1016/s0959-440x(98)80067-5 PubMed DOI

Kass D. H., Batzer M. A., Deininger P. L. (1995). Gene conversion as a secondary mechanism of short interspersed element (SINE) evolution. Mol. Cell. Biol. 15 19–25. 10.1128/mcb.15.1.19 PubMed DOI PMC

Kejnovsky E., Hawkins J. S., Feschotte C. (2012). “Plant transposable elements: biology and evolution,” in Diversity of Genomes in Plants, eds Wendel J. F., Greilhuber J., Leitch I. J., Dolezel J. (Berlin: Springer; ), 17–34. 10.5808/GI.2014.12.3.87 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? Gene 390 92–97. 10.1016/j.gene.2006.10.007 PubMed DOI

Kejnovsky E., Leitch I., Leitch A. (2009). Contrasting evolutionary dynamics between angiosperm and mammalian genomes. Trends Ecol. Evol. 24 572–582. 10.1016/j.tree.2009.04.010 PubMed DOI

Kijima T. E., Innan H. (2009). On the estimation of the insertion time of LTR retrotransposable elements. Mol. Biol. Evol. 27 896–904. 10.1093/molbev/msp295 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. J. Korean Med. Sci. 19 177–185. 10.3346/jkms.2004.19.2.177 PubMed DOI PMC

Koch M. A., Haubold B., Mitchell-Olds T. (2000). Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol. Biol. Evol. 17 1483–1498. 10.1093/oxfordjournals.molbev.a026248 PubMed DOI

Krzywinski J., Sangare D., Besansky N. J. (2005). Satellite DNA from the Y chromosome of the malarial vector Anopheles gambiae. Genetics 169 185–196. 10.1534/genetics.104.034264 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. Nucleic Acids Res. 40 D1202–D1210. 10.1093/nar/gkr1090 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. Plant J. 93 515–533. 10.1111/tpj.13801 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. Bioinformatics 23 2947–2948. 10.1093/bioinformatics/btm404 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 Proceedings of the 2018 IEEE International Conference on Bioinformatics and Biomedicine, Madrid, 2776–2778. 10.1109/BIBM.2018.8621071 DOI

Li W. (1997). Molecular Evolution. Sunderland, MA: Sinauer.

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. Chromosoma 109 161–172. 10.1007/s004120050424 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. Nucleic Acids Res. 39(Suppl. 1), D70–D74. 10.1093/nar/gkq1061 PubMed DOI PMC

Ma J., Bennetzen J. L. (2004). Rapid recent growth and divergence of rice nuclear genomes. Proc. Natl. Acad. Sci. U.S.A. 101 12404–12410. 10.1073/pnas.0403715101 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. Genome Res. 14 860–869. 10.1101/gr.1466204 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. PLoS One 10:e0143424. 10.1371/journal.pone.0143424 PubMed DOI PMC

Mansai S. P., Innan H. (2010). The power of the methods for detecting interlocus gene conversion. Genetics 184 517–527. 10.1534/genetics.109.111161 PubMed DOI PMC

Mansai S. P., Kado T., Innan H. (2011). The rate and tract length of gene conversion between duplicated genes. Genes 2 313–331. 10.3390/genes2020313 PubMed DOI PMC

Martins H., Villesen P. (2011). Improved integration time estimation of endogenous retroviruses with phylogenetic data. PLoS One 6:e14745. 10.1371/journal.pone.0014745 PubMed DOI PMC

Maumus F., Quesneville H. (2014). Ancestral repeats have shaped epigenome and genome composition for millions of years in Arabidopsis thaliana. Nat. Commun. 5:4104. 10.1038/ncomms5104 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. Plant J. 93 338–354. 10.1111/tpj.13781 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. Science 318 245–250. 10.1126/science.1143609 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. Mobile DNA 10:1. 10.1186/s13100-018-0144-1 PubMed DOI PMC

Ou S., Jiang N. (2018). LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 176 1410–1422. 10.1104/pp.17.01310 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. Nucleic Acids Res. 35 D883–D887. 10.1093/nar/gkl976 PubMed DOI PMC

Pereira V. (2004). Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol. 5:R79. 10.1186/gb-2004-5-10-r79 PubMed DOI PMC

Pereira V. (2008). Automated paleontology of repetitive DNA with REANNOTATE. BMC Genomics 9:614. 10.1186/1471-2164-9-614 PubMed DOI PMC

Quinlan A. R., Hall I. M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26 841–842. 10.1093/bioinformatics/btq033 PubMed DOI PMC

Rawat V., Abdelsamad A., Pietzenuk B., Seymour D. K., Koenig D., Weigel D., et al. (2015). Improving the annotation of Arabidopsis lyrata using RNA-seq data. PLoS One 10:e0137391. 10.1371/journal.pone.0137391 PubMed DOI PMC

Rice P., Longden I., Bleasby A. (2000). EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16 276–277. 10.1016/s0168-9525(00)02024-2 PubMed DOI

Roeder G. S., Fink G. R. (1982). Movement of yeast transposable elements by gene conversion. Proc. Natl. Acad. Sci. U.S.A. 79 5621–5625. 10.1073/pnas.79.18.5621 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. Genome Res. 10 1485–1495. 10.1101/gr.152300 PubMed DOI

SanMiguel P., Gaut B., Tikhonov A., Nakajima Y., Bennetzen J. L. (1998). The paleontology of intergene retrotransposons of maize. Nat. Genet. 20 43–45. 10.1038/1695 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. Funct. Integr. Genomics 2 70–80. 10.1007/s10142-002-0056-4 PubMed DOI

Sato S., Nakamura Y., Kaneko T., Asamizu E., Kato T., Nakao M., et al. (2008). Genome structure of the legume, Lotus japonicus. DNA Res. 15 227–239. 10.1093/dnares/dsn008 PubMed DOI PMC

Sawyer S. A. (1999). GENECONV: A Computer Package for the Statistical Detection of Gene Conversion. Washington, DC: University in St. Louis.

Schmutz J., Cannon S. B., Schlueter J., Ma J., Mitros T., Nelson W., et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature 463 178–183. 10.1038/nature08670 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. Science 326 1112–1115. 10.1126/science.1178534 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. G3, 2031–2047. 10.1534/g3.113.007153 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. Genome Res. 10 908–915. 10.1101/gr.10.7.908 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 Medicago truncatula. BMC Genomics 15:312. 10.1186/1471-2164-15-312 PubMed DOI PMC

Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485 635–641. 10.1038/nature11119 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. Sci. Rep. 6:28710. 10.1038/srep28710 PubMed DOI PMC

Tuskan G. A., Difazio S., Jansson S., Bohlmann J., Grigoriev I., Hellsten U., et al. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313 1596–1604. 10.1126/science.1128691 PubMed DOI

Vitte C., Panaud O. (2003). Formation of solo-LTRs through unequal homologous recombination counterbalances amplifications of LTR retrotransposons in rice Oryza sativa L. Mol. Biol. Evol. 20 528–540. 10.1093/molbev/msg055 PubMed DOI

Vitte C., Panaud O. (2005). LTR retrotransposons and flowering plant genome size: emergence of the increase/decrease model. Cytogenet. Genome Res. 110 91–107. 10.1159/000084941 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. Genome Biol. 19:103. 10.1186/s13059-018-1479-0 PubMed DOI PMC

Wicker T., Keller B. (2007). Genome-wide comparative analysis of copia retrotransposons in Triticeae, rice, and Arabidopsis reveals conserved ancient evolutionary lineages and distinct dynamics of individual copia families. Genome Res. 17 1072–1081. 10.1101/gr.6214107 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. Plant Cell 15 1186–1197. 10.1105/tpc.011023 PubMed DOI PMC

Xu Y., Du J. (2014). Young but not relatively old retrotransposons are preferentially located in gene-rich euchromatic regions in tomato (Solanum lycopersicum) plants. Plant J. 80 582–591. 10.1111/tpj.12656 PubMed DOI

Xu Z., Wang H. (2007). LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 35 W265–W268. 10.1093/nar/gkm286 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 Oryza species. G3 7 1875–1885. 10.1534/g3.116.037572 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...