Transposable elements (TEs) are able to jump to new locations (transposition) in the genome, usually after replication. They constitute the so-called selfish or junk DNA and take over large proportions of some genomes. Due to their ability to move around they can change the DNA landscape of genomes and are therefore a rich source of innovation in genes and gene regulation. Surge of sequence data in the past years has significantly facilitated large scale comparative studies. Cephalochordates have been regarded as a useful proxy to ancestral chordate condition partially due to the comparatively slow evolutionary rate at morphological and genomic level. In this study, we used opsin gene family from three Branchiostoma species as a window into cephalochordate genome evolution. We compared opsin complements in terms of family size, gene structure and sequence allowing us to identify gene duplication and gene loss events. Furthermore, analysis of the opsin containing genomic loci showed that they are populated by TEs. In summary, we provide evidence of the way transposable elements may have contributed to the evolution of opsin gene family and to the shaping of cephalochordate genomes in general.

Department of Transcriptional Regulation Institute of Molecular Genetics of the ASCR v v i Videnska 1083 14220 Prague 4 Czech Republic

Laboratory of Eye Biology Institute of Molecular Genetics of the ASCR v v i Division BIOCEV Prumyslová 595 252 50 Vestec Czech Republic

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Lankenau, D. & Volff, J. N. Transposons and the Dynamic Genome. Springer-Verlag Berlin Heidelberg, (2009).

Finnegan DJ. Eukaryotic transposable elements and genome evolution. Trends Genet. 1989;5:103–107. doi: 10.1016/0168-9525(89)90039-5. PubMed DOI

Curcio MJ, Derbyshire KM. The outs and ins of transposition: from mu to kangaroo. Nat. Rev. Mol. Cell Biol. 2003;4:865–877. doi: 10.1038/nrm1241. PubMed DOI

Wicker T, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8:973–982. doi: 10.1038/nrg2165. PubMed DOI

McClintock B. Controlling elements and the gene. Cold Spring Harb. Symp. Quant. Biol. 1956;21:197–216. doi: 10.1101/SQB.1956.021.01.017. PubMed DOI

Chuong, E. B., Elde, N. C. & Feschotte, C. Regulatory activities of transposable elements: from conflicts to benefits. Nat. Rev. Genet. advance online publication; 10.1038/nrg.2016.139 (2016). PubMed PMC

Bourque G. Transposable elements in gene regulation and in the evolution of vertebrate genomes. Curr. Opin. Genet. Dev. 2009;19:607–612. doi: 10.1016/j.gde.2009.10.013. PubMed DOI

Feschotte C. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 2008;9:397–405. doi: 10.1038/nrg2337. PubMed DOI PMC

Feschotte C. The contribution of transposable elements to the evolution of regulatory networks. Nat. Rev. Genet. 2008;9:397–405. doi: 10.1038/nrg2337. PubMed DOI PMC

McVean G. What drives recombination hotspots to repeat DNA in humans? Phil. Trans. R. Soc. B. 2010;365:1213–1218. doi: 10.1098/rstb.2009.0299. PubMed DOI PMC

Thornburg BG, Gotea V, Makalowski W. Transposable elements as a significant source of transcription regulating signals. Gene. 2006;365:104–110. doi: 10.1016/j.gene.2005.09.036. PubMed DOI

Feschotte C, Pritham EJ. DNA transposons and the evolution of eukaryotic genomes. Annu. Rev. Genet. 2007;41:331–368. doi: 10.1146/annurev.genet.40.110405.090448. PubMed DOI PMC

Arguello, J. R., Fan, C., Wang, W. & Long, M. Origination of chimeric genes through DNA-level recombination. Karger (2007). PubMed

Gray YH. It takes two transposons to tango: transposable-element-mediated chromosomal rearrangements. Trends Genet. 2000;16:461–468. doi: 10.1016/S0168-9525(00)02104-1. PubMed DOI

Canapa A, Barucca M, Biscotti MA, Forconi M, Olmo E. Transposons, genome size, and evolutionary insights in animals. Cytogenet. Genome Res. 2015;147:217–239. doi: 10.1159/000444429. PubMed DOI

Joly-Lopez Z, Bureau TE. Diversity and evolution of transposable elements in Arabidopsis. Chromosome Res. 2014;22:203–216. doi: 10.1007/s10577-014-9418-8. PubMed DOI

Kaminker, J. S. et al. The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol. 3, 10.1186/gb-2002-3-12-research0084 (2002). PubMed PMC

Mahillon J, Chandler M. Insertion Sequences. Microbiol. Mol. Biol. Rev. 1998;62:725–774. PubMed PMC

Mills RE, Bennett EA, Iskow RC, Devine SE. Which transposable elements are active in the human genome? Trends Genet. 2007;23:183–191. doi: 10.1016/j.tig.2007.02.006. PubMed DOI

Baucom RS, et al. Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet. 2009;5:e1000732. doi: 10.1371/journal.pgen.1000732. PubMed DOI PMC

Cordaux R, Batzer MA. The impact of retrotransposons on human genome evolution. Nat. Rev. Genet. 2009;10:691–703. doi: 10.1038/nrg2640. PubMed DOI PMC

Gu S, et al. Alu-mediated diverse and complex pathogenic copy-number variants within human chromosome 17 at p13.3. Hum. Mol. Genet. 2015;24:4061–4077. doi: 10.1093/hmg/ddv146. PubMed DOI PMC

Bertrand S, Escriva H. Evolutionary crossroads in developmental biology: amphioxus. Development. 2011;138:4819–4830. doi: 10.1242/dev.066720. PubMed DOI

Huang S, et al. Decelerated genome evolution in modern vertebrates revealed by analysis of multiple lancelet genomes. Nat. Commun. 2014;5:5896. doi: 10.1038/ncomms6896. PubMed DOI PMC

Chalopin D, Naville M, Plard F, Galiana D, Volff JN. Comparative analysis of transposable elements highlights mobilome diversity and evolution in vertebrates. Genome Biol. Evol. 2015;7:567–580. doi: 10.1093/gbe/evv005. PubMed DOI PMC

Canestro C, Albalat R. Transposon diversity is higher in amphioxus than in vertebrates: functional and evolutionary inferences. Briefings in functional genomics. 2012;11:131–141. doi: 10.1093/bfgp/els010. PubMed DOI

Igawa T, et al. Evolutionary history of the extant amphioxus lineage with shallow-branching diversification. Sci. Rep. 2017;7:1157. doi: 10.1038/s41598-017-00786-5. PubMed DOI PMC

Kim EB, et al. Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature. 2011;479:223–227. doi: 10.1038/nature10533. PubMed DOI PMC

Banyai L, Patthy L. Putative extremely high rate of proteome innovation in lancelets might be explained by high rate of gene prediction errors. Sci. Rep. 2016;6:30700. doi: 10.1038/srep30700. PubMed DOI PMC

Porter ML, et al. Shedding new light on opsin evolution. Proceedings. Biological sciences / The Royal Society. 2012;279:3–14. doi: 10.1098/rspb.2011.1819. PubMed DOI PMC

Liegertova M, et al. Cubozoan genome illuminates functional diversification of opsins and photoreceptor evolution. Scientific reports. 2015;5:11885. doi: 10.1038/srep11885. PubMed DOI PMC

Terakita A. The opsins. Genome biology. 2005;6:213. doi: 10.1186/gb-2005-6-3-213. PubMed DOI PMC

Shichida Y, Matsuyama T. Evolution of opsins and phototransduction. Phil Trans R Soc B. 2009;364:2881–2895. doi: 10.1098/rstb.2009.0051. PubMed DOI PMC

Feuda R, Hamilton SC, McInerney JO, Pisani D. Metazoan opsin evolution reveals a simple route to animal vision. Proc. Natl. Acad. Sci. USA. 2012;109:18868–18872. doi: 10.1073/pnas.1204609109. PubMed DOI PMC

Plachetzki DC, Degnan BM, Oakley TH. The origins of novel protein interactions during animal opsin evolution. PLoS One. 2007;2:e1054. doi: 10.1371/journal.pone.0001054. PubMed DOI PMC

Peirson SN, Halford S, Foster RG. The evolution of irradiance detection: melanopsin and the non-visual opsins. Philosophical transactions of the Royal Society of London. Series B, Biological sciences. 2009;364:2849–2865. doi: 10.1098/rstb.2009.0050. PubMed DOI PMC

D’Aniello S, et al. Opsin evolution in the Ambulacraria. Marine Genomics. 2015;24(Part 2):177–183. doi: 10.1016/j.margen.2015.10.001. PubMed DOI

Ramirez MD, et al. The last common ancestor of most bilaterian animals possessed at least 9 opsins. Genome Biol Evol. 2016;8:3640–3652. doi: 10.1093/gbe/evw135. PubMed DOI PMC

Suga H, Schmid V, Gehring WJ. Evolution and functional diversity of jellyfish opsins. Curr. Biol. 2008;18:51–55. doi: 10.1016/j.cub.2007.11.059. PubMed DOI

Pantzartzi, C. N., Pergner, J., Kozmikova, I. & Kozmik, Z. The opsin repertoire of the European lancelet: a window into light detection in a basal chordate. Int. J. Dev. Biol.61, 763–772, 10.1387/ijdb.170139zk (2017). PubMed

Holland LZ, et al. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome research. 2008;18:1100–1111. doi: 10.1101/gr.073676.107. PubMed DOI PMC

Koyanagi M, Kubokawa K, Tsukamoto H, Shichida Y, Terakita A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Curr. Biol. 2005;15:1065–1069. doi: 10.1016/j.cub.2005.04.063. PubMed DOI

Koyanagi M, Terakita A, Kubokawa K, Shichida Y. Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis- and all-trans-retinals as their chromophores. FEBS Lett. 2002;531:525–528. doi: 10.1016/S0014-5793(02)03616-5. PubMed DOI

Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 1997;268:78–94. doi: 10.1006/jmbi.1997.0951. PubMed DOI

Rogozin IB, Milanesi L. Analysis of donor splice sites in different eukaryotic organisms. J. Mol. Evol. 1997;45:50–59. doi: 10.1007/PL00006200. PubMed DOI

Sievers F, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011;7:539. doi: 10.1038/msb.2011.75. PubMed DOI PMC

Darzentas N. Circoletto: visualizing sequence similarity with Circos. Bioinformatics. 2010;26:2620–2621. doi: 10.1093/bioinformatics/btq484. PubMed DOI

Kohany O, Gentles AJ, Hankus L, Jurka J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics. 2006;7:474. doi: 10.1186/1471-2105-7-474. PubMed DOI PMC

Bao W, Kojima KK, Kohany O. Repbase Update, a database of repetitive elements in eukaryotic genomes. Mobile DNA. 2015;6:11. doi: 10.1186/s13100-015-0041-9. PubMed DOI PMC

Holland LZ, Yu JK. Cephalochordate (amphioxus) embryos: procurement, culture, and basic methods. Methods in cell biology. 2004;74:195–215. doi: 10.1016/S0091-679X(04)74009-1. PubMed DOI

Hirakow R, Kajita N. Electron microscopic study of the development of amphioxus, Branchiostoma belcheri tsingtauense: the neurula and larva. J. Anat. 1994;69:1–13. PubMed

Permanyer J, Albalat R, Gonzalez-Duarte R. Getting closer to a pre-vertebrate genome: the non-LTR retrotransposons of Branchiostoma floridae. International journal of biological sciences. 2006;2:48–53. doi: 10.7150/ijbs.2.48. PubMed DOI PMC

Muotri AR, Marchetto MC, Coufal NG, Gage FH. The necessary junk: new functions for transposable elements. Hum. Mol. Genet. 2007;16(R2):R159–R167. doi: 10.1093/hmg/ddm196. PubMed DOI

Osborne PW, Ferrier DE. Chordate Hox and ParaHox gene clusters differ dramatically in their repetitive element content. Mol. Biol. Evol. 2010;27:217–220. doi: 10.1093/molbev/msp235. PubMed DOI

Ferrier DE, Holland PW. Ciona intestinalis ParaHox genes: evolution of Hox/ParaHox cluster integrity, developmental mode, and temporal colinearity. Mol Phylogenet Evol. 2002;24:412–417. doi: 10.1016/S1055-7903(02)00204-X. PubMed DOI

Xing F, et al. Characterization of amphioxus GDF8/11 gene, an archetype of vertebrate MSTN and GDF11. Dev. Genes Evol. 2007;217:549–554. doi: 10.1007/s00427-007-0162-3. PubMed DOI

Matsumoto Y, Fukamachi S, Mitani H, Kawamura S. Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes) Gene. 2006;371:268–278. doi: 10.1016/j.gene.2005.12.005. PubMed DOI

Porath-Krause AJ, et al. Structural differences and differential expression among rhabdomeric opsins reveal functional change after gene duplication in the bay scallop, Argopecten irradians (Pectinidae) BMC Evol. Biol. 2016;16:250. doi: 10.1186/s12862-016-0823-9. PubMed DOI PMC

Watson CT, Lubieniecki KP, Loew E, Davidson WS, Breden F. Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri. BMC Evol. Biol. 2010;10:87–87. doi: 10.1186/1471-2148-10-87. PubMed DOI PMC

Dulai KS, von Dornum M, Mollon JD, Hunt DM. The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome research. 1999;9:629–638. PubMed

Neafsey DE, Hartl DL. Convergent loss of an anciently duplicated, functionally divergent RH2 opsin gene in the fugu and Tetraodon pufferfish lineages. Gene. 2005;350:161–171. doi: 10.1016/j.gene.2005.02.011. PubMed DOI

Holland LZ, Short S. Gene duplication, co-option and recruitment during the origin of the vertebrate brain from the invertebrate chordate brain. Brain Behav. Evol. 2008;72:91–105. doi: 10.1159/000151470. PubMed DOI

Molecular Fingerprint of Amphioxus Frontal Eye Illuminates the Evolution of Homologous Cell Types in the Chordate Retina