{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,13]],"date-time":"2026-05-13T20:57:13Z","timestamp":1778705833263,"version":"3.51.4"},"reference-count":72,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2023,1,18]],"date-time":"2023-01-18T00:00:00Z","timestamp":1674000000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,1,18]],"date-time":"2023-01-18T00:00:00Z","timestamp":1674000000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia","award":["SFRH\/BD\/131584\/2017"],"award-info":[{"award-number":["SFRH\/BD\/131584\/2017"]}]},{"DOI":"10.13039\/501100017642","name":"Spanish National Plan for Scientific and Technical Research and Innovation","doi-asserted-by":"publisher","award":["[RYC-2015-18241]"],"award-info":[{"award-number":["[RYC-2015-18241]"]}],"id":[{"id":"10.13039\/501100017642","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100017642","name":"Spanish National Plan for Scientific and Technical Research and Innovation","doi-asserted-by":"publisher","award":["[PID2019-107931GA-I00]."],"award-info":[{"award-number":["[PID2019-107931GA-I00]."]}],"id":[{"id":"10.13039\/501100017642","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100005727","name":"Universidade de Coimbra","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100005727","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Mol Evol"],"published-print":{"date-parts":[[2023,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Type IB topoisomerases relax the torsional stress associated with DNA metabolism in the nucleus and mitochondria and constitute important molecular targets of anticancer drugs. Vertebrates stand out among eukaryotes by having two Type IB topoisomerases acting specifically in the nucleus (TOP1) and mitochondria (TOP1MT). Despite their major importance, the origin and evolution of these paralogues remain unknown. Here, we examine the molecular evolutionary processes acting on both TOP1 and TOP1MT in Chordata, taking advantage of the increasing number of available genome sequences. We found that both TOP1 and TOP1MT evolved under strong purifying selection, as expected considering their essential biological functions. Critical active sites, including those associated with resistance to anticancer agents, were found particularly conserved. However, TOP1MT presented a higher rate of molecular evolution than TOP1, possibly related with its specialized activity on the mitochondrial genome and a less critical role in cells. We could place the duplication event that originated the <jats:italic>TOP1<\/jats:italic> and <jats:italic>TOP1MT<\/jats:italic> paralogues early in the radiation of vertebrates, most likely associated with the first round of vertebrate tetraploidization (1R). Moreover, our data suggest that cyclostomes present a specialized mitochondrial Type IB topoisomerase. Interestingly, we identified two missense mutations replacing amino acids in the Linker region of TOP1MT in Neanderthals, which appears as a rare event when comparing the genome of both species. In conclusion, TOP1 and TOP1MT differ in their rates of evolution, and their evolutionary histories allowed us to better understand the evolution of chordates.<\/jats:p>","DOI":"10.1007\/s00239-022-10091-z","type":"journal-article","created":{"date-parts":[[2023,1,18]],"date-time":"2023-01-18T08:03:58Z","timestamp":1674029038000},"page":"192-203","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Evolution of TOP1 and TOP1MT Topoisomerases in Chordata"],"prefix":"10.1007","volume":"91","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3757-9496","authenticated-orcid":false,"given":"Filipa","family":"Moreira","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0516-2717","authenticated-orcid":false,"given":"Miguel","family":"Arenas","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7267-4459","authenticated-orcid":false,"given":"Arnaldo","family":"Videira","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8950-1036","authenticated-orcid":false,"given":"Filipe","family":"Pereira","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2023,1,18]]},"reference":[{"key":"10091_CR1","doi-asserted-by":"publisher","first-page":"429","DOI":"10.3389\/fevo.2021.703163","volume":"9","author":"ME Aase-Remedios","year":"2021","unstructured":"Aase-Remedios ME, Ferrier DEK (2021) Improved understanding of the role of gene and genome duplications in chordate evolution with new genome and transcriptome sequences. Front Ecol Evol 9:429","journal-title":"Front Ecol Evol"},{"key":"10091_CR2","doi-asserted-by":"publisher","first-page":"12408","DOI":"10.1016\/S0021-9258(18)42288-0","volume":"267","author":"J Alsner","year":"1992","unstructured":"Alsner J, Svejstrup J, Kjeldsen E, S\u00f8rensen B, Westergaard O (1992) Identification of an N-terminal domain of eukaryotic DNA topoisomerase I dispensable for catalytic activity but essential for in vivo function. J Biol Chem 267:12408\u201312411","journal-title":"J Biol Chem"},{"key":"10091_CR3","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1093\/nar\/28.1.235","volume":"28","author":"HM Berman","year":"2000","unstructured":"Berman HM et al (2000) The protein data bank. Nucleic Acids Res 28:235\u2013242","journal-title":"Nucleic Acids Res"},{"key":"10091_CR4","doi-asserted-by":"publisher","first-page":"2169","DOI":"10.1021\/acs.jmedchem.6b00966","volume":"60","author":"G Capranico","year":"2017","unstructured":"Capranico G, Marinello J, Chillemi G (2017) Type i DNA topoisomerases. J Med Chem 60:2169\u20132192","journal-title":"J Med Chem"},{"key":"10091_CR71","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1093\/oxfordjournals.molbev.a026334","volume":"17","author":"J Castresana","year":"2000","unstructured":"Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540\u2013552","journal-title":"Mol Biol Evol"},{"key":"10091_CR5","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/S0079-6603(08)60891-0","volume":"60","author":"JJ Champoux","year":"1998","unstructured":"Champoux JJ (1998) Domains of human topoisomerase I and associated functions. Prog Nucleic Acid Res Mol Biol 60:111\u2013132","journal-title":"Prog Nucleic Acid Res Mol Biol"},{"key":"10091_CR6","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1146\/annurev.biochem.70.1.369","volume":"70","author":"JJ Champoux","year":"2001","unstructured":"Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369\u2013413","journal-title":"Annu Rev Biochem"},{"key":"10091_CR7","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1016\/S0092-8674(00)81411-7","volume":"92","author":"C Cheng","year":"1998","unstructured":"Cheng C, Kussie P, Pavletich N, Shuman S (1998) Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell 92:841\u2013850","journal-title":"Cell"},{"key":"10091_CR8","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1016\/j.jmb.2004.03.077","volume":"339","author":"JE Chrencik","year":"2004","unstructured":"Chrencik JE, Staker BL, Burgin AB, Pourquier P, Pommier Y, Stewart L, Redinbo MR (2004) Mechanisms of camptothecin resistance by human topoisomerase I mutations. J Mol Biol 339:773\u2013784","journal-title":"J Mol Biol"},{"key":"10091_CR9","doi-asserted-by":"publisher","first-page":"2052","DOI":"10.1101\/gr.1252603","volume":"13","author":"GC Conant","year":"2003","unstructured":"Conant GC, Wagner A (2003) Asymmetric sequence divergence of duplicate genes. Genome Res 13:2052\u20132058","journal-title":"Genome Res"},{"key":"10091_CR10","first-page":"91","volume":"56","author":"E Cretaio","year":"2007","unstructured":"Cretaio E, Pattarello L, Fontebasso Y, Benedetti P, Losasso C (2007) Human DNA topoisomerase IB: structure and functions. Ital J Biochem 56:91\u2013102","journal-title":"Ital J Biochem"},{"key":"10091_CR11","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.bbapap.2005.03.007","volume":"1749","author":"A Czubaty","year":"2005","unstructured":"Czubaty A et al (2005) Proteomic analysis of complexes formed by human topoisomerase I. Biochim Et Biophys Acta (BBA)-Proteins Proteom 1749:133\u2013141","journal-title":"Biochim Et Biophys Acta (BBA)-Proteins Proteom"},{"key":"10091_CR12","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1093\/molbev\/msz189","volume":"37","author":"D Darriba","year":"2020","unstructured":"Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Mol Biol Evol 37:291\u2013294","journal-title":"Mol Biol Evol"},{"key":"10091_CR13","doi-asserted-by":"publisher","first-page":"e26","DOI":"10.1093\/nar\/gkn1087","volume":"37","author":"MD de la Loza","year":"2009","unstructured":"de la Loza MD, Wellinger RE (2009) A novel approach for organelle-specific DNA damage targeting reveals different susceptibility of mitochondrial DNA to the anticancer drugs camptothecin and topotecan. Nucleic Acids Res 37:e26\u2013e26","journal-title":"Nucleic Acids Res"},{"key":"10091_CR14","doi-asserted-by":"publisher","first-page":"bbaa431","DOI":"10.1093\/bib\/bbaa431","volume":"22","author":"R Del Amparo","year":"2021","unstructured":"Del Amparo R, Branco C, Arenas J, Vicens A, Arenas M (2021) Analysis of selection in protein-coding sequences accounting for common biases. Brief Bioinform 22:bbaa431","journal-title":"Brief Bioinform"},{"key":"10091_CR15","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1038\/nature04336","volume":"439","author":"F Delsuc","year":"2006","unstructured":"Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965\u2013968","journal-title":"Nature"},{"key":"10091_CR16","doi-asserted-by":"publisher","first-page":"W465","DOI":"10.1093\/nar\/gkn180","volume":"36","author":"A Dereeper","year":"2008","unstructured":"Dereeper A et al (2008) Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465\u2013W469","journal-title":"Nucleic Acids Res"},{"key":"10091_CR17","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0041094","volume":"7","author":"C Douarre","year":"2012","unstructured":"Douarre C et al (2012) Mitochondrial topoisomerase I is critical for mitochondrial integrity and cellular energy metabolism. PLoS ONE 7:e41094","journal-title":"PLoS ONE"},{"key":"10091_CR18","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1093\/sysbio\/syu084","volume":"64","author":"T Flouri","year":"2015","unstructured":"Flouri T et al (2015) The phylogenetic likelihood library. Syst Biol 64:356\u2013362","journal-title":"Syst Biol"},{"key":"10091_CR19","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1016\/j.biochi.2006.12.009","volume":"89","author":"P Forterre","year":"2007","unstructured":"Forterre P, Gribaldo S, Gadelle D, Serre M-C (2007) Origin and evolution of DNA topoisomerases. Biochimie 89:427\u2013446","journal-title":"Biochimie"},{"key":"10091_CR20","doi-asserted-by":"publisher","first-page":"710","DOI":"10.1126\/science.1188021","volume":"328","author":"RE Green","year":"2010","unstructured":"Green RE et al (2010) A draft sequence of the Neandertal genome. Science 328:710\u2013722","journal-title":"Science"},{"key":"10091_CR21","doi-asserted-by":"publisher","first-page":"754","DOI":"10.1093\/bioinformatics\/17.8.754","volume":"17","author":"JP Huelsenbeck","year":"2001","unstructured":"Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754\u2013755","journal-title":"Bioinformatics"},{"key":"10091_CR22","doi-asserted-by":"publisher","first-page":"bay 119","DOI":"10.1093\/database\/bay119","volume":"2018","author":"SE Hunt","year":"2018","unstructured":"Hunt SE et al (2018) Ensembl variation resources. Database 2018:bay 119","journal-title":"Database"},{"key":"10091_CR23","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1007\/978-1-4939-1438-8_4","volume-title":"Parasite genomics protocols","author":"DC Jeffares","year":"2015","unstructured":"Jeffares DC, Tomiczek B, Sojo V, dos Reis M (2015) A beginners guide to estimating the non-synonymous to synonymous rate ratio of all protein-coding genes in a genome. Parasite genomics protocols. Springer, New York, pp 65\u201390"},{"key":"10091_CR24","doi-asserted-by":"publisher","first-page":"8910","DOI":"10.1073\/pnas.85.23.8910","volume":"85","author":"C-C Juan","year":"1988","unstructured":"Juan C-C et al (1988) Human DNA topoisomerase I is encoded by a single-copy gene that maps to chromosome region 20q12-13.2. Proc Natl Acad Sci 85:8910\u20138913","journal-title":"Proc Natl Acad Sci"},{"key":"10091_CR25","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1101\/gr.229102","volume":"12","author":"WJ Kent","year":"2002","unstructured":"Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2002) The human genome browser at UCSC. Genome Res 12:996\u20131006","journal-title":"Genome Res"},{"key":"10091_CR26","doi-asserted-by":"publisher","first-page":"11282","DOI":"10.1073\/pnas.1511016112","volume":"112","author":"S Khiati","year":"2015","unstructured":"Khiati S et al (2015) Lack of mitochondrial topoisomerase I (TOP1mt) impairs liver regeneration. Proc Natl Acad Sci 112:11282\u201311287","journal-title":"Proc Natl Acad Sci"},{"key":"10091_CR27","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1093\/molbev\/msi105","volume":"22","author":"SL Kosakovsky Pond","year":"2005","unstructured":"Kosakovsky Pond SL, Frost SD (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208\u20131222","journal-title":"Mol Biol Evol"},{"key":"10091_CR28","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1093\/molbev\/msz197","volume":"37","author":"SL Kosakovsky Pond","year":"2020","unstructured":"Kosakovsky Pond SL et al (2020) HyPhy 2.5\u2014a customizable platform for evolutionary hypothesis testing using phylogenies. Mol Biol Evol 37:295\u2013299","journal-title":"Mol Biol Evol"},{"key":"10091_CR29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-019-44877-x","volume":"9","author":"M Kuhlwilm","year":"2019","unstructured":"Kuhlwilm M, Boeckx C (2019) A catalog of single nucleotide changes distinguishing modern humans from archaic hominins. Sci Rep 9:1\u201314","journal-title":"Sci Rep"},{"key":"10091_CR30","doi-asserted-by":"publisher","first-page":"6656","DOI":"10.1073\/pnas.90.14.6656","volume":"90","author":"MP Lee","year":"1993","unstructured":"Lee MP, Brown SD, Chen A, Hsieh T-s (1993) DNA topoisomerase I is essential in Drosophila melanogaster. Proc Natl Acad Sci 90:6656\u20136660","journal-title":"Proc Natl Acad Sci"},{"key":"10091_CR31","first-page":"1","volume-title":"2010 gateway computing environments workshop (GCE)","author":"MA Miller","year":"2010","unstructured":"Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 gateway computing environments workshop (GCE). Ieee, United States, pp 1\u20138"},{"key":"10091_CR32","doi-asserted-by":"publisher","first-page":"41107","DOI":"10.1074\/jbc.M003135200","volume":"275","author":"Y-Y Mo","year":"2000","unstructured":"Mo Y-Y, Wang C, Beck WT (2000) A novel nuclear localization signal in human DNA topoisomerase I. J Biol Chem 275:41107\u201341113","journal-title":"J Biol Chem"},{"key":"10091_CR33","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1007\/s00239-021-10011-7","volume":"89","author":"F Moreira","year":"2021","unstructured":"Moreira F, Arenas M, Videira A, Pereira F (2021) Molecular evolution of DNA topoisomerase III beta (TOP3B) in metazoa. J Mol Evol 89:384\u2013395","journal-title":"J Mol Evol"},{"key":"10091_CR34","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1007\/s00239-022-10048-2","volume":"90","author":"F Moreira","year":"2022","unstructured":"Moreira F, Arenas M, Videira A, Pereira F (2022) Evolutionary history of TOPIIA topoisomerases in animals. J Mol Evol 90:149\u2013165","journal-title":"J Mol Evol"},{"key":"10091_CR35","doi-asserted-by":"publisher","first-page":"6804","DOI":"10.1128\/MCB.16.12.6804","volume":"16","author":"SG Morham","year":"1996","unstructured":"Morham SG, Kluckman KD, Voulomanos N, Smithies O (1996) Targeted disruption of the mouse topoisomerase I gene by camptothecin selection. Mol Cell Biol 16:6804\u20136809","journal-title":"Mol Cell Biol"},{"key":"10091_CR36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-020-20314-w","volume":"12","author":"Y Nakatani","year":"2021","unstructured":"Nakatani Y, Shingate P, Ravi V, Pillai NE, Prasad A, McLysaght A, Venkatesh B (2021) Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution. Nat Commun 12:1\u201314","journal-title":"Nat Commun"},{"key":"10091_CR37","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1126\/science.abj6987","volume":"376","author":"S Nurk","year":"2022","unstructured":"Nurk S et al (2022) The complete sequence of a human genome. Science 376:44\u201353","journal-title":"Science"},{"key":"10091_CR38","volume-title":"Evolution by gene duplication","author":"S Ohno","year":"2013","unstructured":"Ohno S (2013) Evolution by gene duplication. Springer Science & Business Media, Germany"},{"key":"10091_CR39","doi-asserted-by":"publisher","first-page":"27767","DOI":"10.1074\/jbc.M804826200","volume":"283","author":"K Palle","year":"2008","unstructured":"Palle K, Pattarello L, van der Merwe M, Losasso C, Benedetti P, Bjornsti M-A (2008) Disulfide cross-links reveal conserved features of DNA topoisomerase I architecture and a role for the N terminus in clamp closure. J Biol Chem 283:27767\u201327775","journal-title":"J Biol Chem"},{"key":"10091_CR40","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1016\/j.str.2010.03.007","volume":"18","author":"A Patel","year":"2010","unstructured":"Patel A, Yakovleva L, Shuman S, Mondrag\u00f3n A (2010) Crystal structure of a bacterial topoisomerase IB in complex with DNA reveals a secondary DNA binding site. Structure 18:725\u2013733","journal-title":"Structure"},{"key":"10091_CR41","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1016\/j.molcel.2006.06.015","volume":"23","author":"K Perry","year":"2006","unstructured":"Perry K, Hwang Y, Bushman FD, Van Duyne GD (2006) Structural basis for specificity in the poxvirus topoisomerase. Mol Cell 23:343\u2013354","journal-title":"Mol Cell"},{"key":"10091_CR42","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1038\/nrc1977","volume":"6","author":"Y Pommier","year":"2006","unstructured":"Pommier Y (2006) Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 6:789\u2013802","journal-title":"Nat Rev Cancer"},{"key":"10091_CR43","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1016\/j.chembiol.2010.04.012","volume":"17","author":"Y Pommier","year":"2010","unstructured":"Pommier Y, Leo E, Zhang H, Marchand C (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 17:421\u2013433","journal-title":"Chem Biol"},{"key":"10091_CR44","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1038\/nrm.2016.111","volume":"17","author":"Y Pommier","year":"2016","unstructured":"Pommier Y, Sun Y, Shar-yin NH, Nitiss JL (2016) Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat Rev Mol Cell Biol 17:703\u2013721","journal-title":"Nat Rev Mol Cell Biol"},{"key":"10091_CR45","doi-asserted-by":"publisher","DOI":"10.1038\/s41580-022-00452-3","author":"Y Pommier","year":"2022","unstructured":"Pommier Y, Nussenzweig A, Takeda S, Austin C (2022) Human topoisomerases and their roles in genome stability and organization. Nat Rev Mol Cell Biol. https:\/\/doi.org\/10.1038\/s41580-022-00452-3","journal-title":"Nat Rev Mol Cell Biol"},{"key":"10091_CR46","doi-asserted-by":"publisher","first-page":"1064","DOI":"10.1038\/nature06967","volume":"453","author":"NH Putnam","year":"2008","unstructured":"Putnam NH et al (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453:1064\u20131071","journal-title":"Nature"},{"key":"10091_CR47","doi-asserted-by":"publisher","first-page":"1504","DOI":"10.1126\/science.279.5356.1504","volume":"279","author":"MR Redinbo","year":"1998","unstructured":"Redinbo MR, Stewart L, Kuhn P, Champoux JJ, Hol WG (1998) Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279:1504\u20131513","journal-title":"Science"},{"key":"10091_CR48","doi-asserted-by":"publisher","first-page":"1053","DOI":"10.1038\/nature09710","volume":"468","author":"D Reich","year":"2010","unstructured":"Reich D et al (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053\u20131060","journal-title":"Nature"},{"key":"10091_CR49","doi-asserted-by":"publisher","first-page":"1572","DOI":"10.1093\/bioinformatics\/btg180","volume":"19","author":"F Ronquist","year":"2003","unstructured":"Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572\u20131574","journal-title":"Bioinformatics"},{"key":"10091_CR50","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1111\/j.1749-6632.2000.tb07024.x","volume":"922","author":"A Saleem","year":"2000","unstructured":"Saleem A, Edwards TK, Rasheed Z, Rubin EH (2000) Mechanisms of resistance to camptothecins. Ann N Y Acad Sci 922:46\u201355","journal-title":"Ann N Y Acad Sci"},{"key":"10091_CR51","doi-asserted-by":"publisher","first-page":"20141729","DOI":"10.1098\/rspb.2014.1729","volume":"281","author":"N Satoh","year":"2014","unstructured":"Satoh N, Rokhsar D, Nishikawa T (2014) Chordate evolution and the three-phylum system. Proc R Soc b: Biol Sci 281:20141729","journal-title":"Proc R Soc b: Biol Sci"},{"key":"10091_CR52","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1101\/gr.6341207","volume":"18","author":"DR Scannell","year":"2008","unstructured":"Scannell DR, Wolfe KH (2008) A burst of protein sequence evolution and a prolonged period of asymmetric evolution follow gene duplication in yeast. Genome Res 18:137\u2013147","journal-title":"Genome Res"},{"key":"10091_CR53","doi-asserted-by":"publisher","first-page":"w431","DOI":"10.1093\/nar\/gkab314","volume":"49","author":"D Sehnal","year":"2021","unstructured":"Sehnal D et al (2021) Mol* viewer: modern web app for 3D visualization and analysis of large biomolecular structures. Nucleic Acids Res 49:w431\u2013w437","journal-title":"Nucleic Acids Res"},{"key":"10091_CR54","doi-asserted-by":"publisher","first-page":"820","DOI":"10.1038\/s41559-020-1156-z","volume":"4","author":"O Simakov","year":"2020","unstructured":"Simakov O et al (2020) Deeply conserved synteny resolves early events in vertebrate evolution. Nat Ecol Evol 4:820\u2013830","journal-title":"Nat Ecol Evol"},{"key":"10091_CR55","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1101\/gr.184135.114","volume":"25","author":"JJ Smith","year":"2015","unstructured":"Smith JJ, Keinath MC (2015) The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications. Genome Res 25:1081\u20131090","journal-title":"Genome Res"},{"key":"10091_CR56","doi-asserted-by":"publisher","first-page":"7593","DOI":"10.1074\/jbc.271.13.7593","volume":"271","author":"L Stewart","year":"1996","unstructured":"Stewart L, Ireton GC, Parker LH, Madden KR, Champoux JJ (1996) Biochemical and biophysical analyses of recombinant forms of human topoisomerase I (\u2217). J Biol Chem 271:7593\u20137601","journal-title":"J Biol Chem"},{"key":"10091_CR57","doi-asserted-by":"publisher","first-page":"1534","DOI":"10.1126\/science.279.5356.1534","volume":"279","author":"L Stewart","year":"1998","unstructured":"Stewart L, Redinbo MR, Qiu X, Hol WG, Champoux JJ (1998) A model for the mechanism of human topoisomerase I. Science 279:1534\u20131541","journal-title":"Science"},{"key":"10091_CR58","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41467-021-27686-7","volume":"13","author":"DT Takahashi","year":"2022","unstructured":"Takahashi DT et al (2022) Topoisomerase I (TOP1) dynamics: conformational transition from open to closed states. Nat Commun 13:1\u201311","journal-title":"Nat Commun"},{"key":"10091_CR72","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1080\/10635150701472164","volume":"56","author":"G Talavera","year":"2007","unstructured":"Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564\u2013577","journal-title":"Syst Biol"},{"key":"10091_CR59","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1016\/S0300-9084(97)80028-4","volume":"79","author":"A Tua","year":"1997","unstructured":"Tua A, Wang J, Kulpa V, Wernette C (1997) Mitochondrial DNA topoisomerase I of saccharomyces cerevisiae. Biochimie 79:341\u2013350","journal-title":"Biochimie"},{"key":"10091_CR60","doi-asserted-by":"publisher","first-page":"436","DOI":"10.1007\/s002390010233","volume":"53","author":"Y Van de Peer","year":"2001","unstructured":"Van de Peer Y, Taylor JS, Braasch I, Meyer A (2001) The ghost of selection past: rates of evolution and functional divergence of anciently duplicated genes. J Mol Evol 53:436\u2013446","journal-title":"J Mol Evol"},{"key":"10091_CR61","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1038\/nrg2600","volume":"10","author":"Y Van de Peer","year":"2009","unstructured":"Van de Peer Y, Maere S, Meyer A (2009) The evolutionary significance of ancient genome duplications. Nat Rev Genet 10:725\u2013732","journal-title":"Nat Rev Genet"},{"key":"10091_CR62","doi-asserted-by":"publisher","first-page":"723","DOI":"10.1006\/bbrc.1995.2345","volume":"214","author":"J Wang","year":"1995","unstructured":"Wang J, Kearney K, Derby M, Wernette CM (1995) On the relationship of the ATP-independent, mitochondrial-associated DNA topoisomerase of saccharomyces cerevisiae to the nuclear topoisomerase I. Biochem Biophys Res Commun 214:723\u2013729","journal-title":"Biochem Biophys Res Commun"},{"key":"10091_CR63","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2148-9-275","volume":"9","author":"X Wang","year":"2009","unstructured":"Wang X, Huang Y, Lavrov DV, Gu X (2009) Comparative study of human mitochondrial proteome reveals extensive protein subcellular relocalization after gene duplications. BMC Evol Biol 9:1\u201311","journal-title":"BMC Evol Biol"},{"key":"10091_CR64","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/0378-1119(90)90095-9","volume":"91","author":"G Yang","year":"1990","unstructured":"Yang G, Kunze N, Baumg\u00e4rtner B, Jiang Z, Sapp M, Knippers R, Richter A (1990) Molecular structures of two human DNA topoisomerase I retrosequences. Gene 91:247\u2013253","journal-title":"Gene"},{"key":"10091_CR65","doi-asserted-by":"publisher","first-page":"11196","DOI":"10.1021\/bi800774b","volume":"47","author":"H Zhang","year":"2008","unstructured":"Zhang H, Pommier Y (2008) Mitochondrial topoisomerase I sites in the regulatory D-loop region of mitochondrial DNA. Biochemistry 47:11196\u201311203","journal-title":"Biochemistry"},{"key":"10091_CR66","doi-asserted-by":"publisher","first-page":"10608","DOI":"10.1073\/pnas.191321998","volume":"98","author":"H Zhang","year":"2001","unstructured":"Zhang H, Barcel\u00f3 JM, Lee B, Kohlhagen G, Zimonjic DB, Popescu NC, Pommier Y (2001) Human mitochondrial topoisomerase I. Proc Natl Acad Sci 98:10608\u201310613","journal-title":"Proc Natl Acad Sci"},{"key":"10091_CR67","doi-asserted-by":"publisher","first-page":"2087","DOI":"10.1093\/nar\/gkh525","volume":"32","author":"H Zhang","year":"2004","unstructured":"Zhang H, Meng LH, Zimonjic DB, Popescu NC, Pommier Y (2004) Thirteen-exon-motif signature for vertebrate nuclear and mitochondrial type IB topoisomerases. Nucleic Acids Res 32:2087\u20132092","journal-title":"Nucleic Acids Res"},{"key":"10091_CR68","doi-asserted-by":"publisher","first-page":"474","DOI":"10.1016\/j.biochi.2006.11.002","volume":"89","author":"H Zhang","year":"2007","unstructured":"Zhang H, Meng L-H, Pommier Y (2007) Mitochondrial topoisomerases and alternative splicing of the human TOP1mt gene. Biochimie 89:474\u2013481","journal-title":"Biochimie"},{"key":"10091_CR69","doi-asserted-by":"publisher","first-page":"7259","DOI":"10.1093\/nar\/gku384","volume":"42","author":"H Zhang","year":"2014","unstructured":"Zhang H, Zhang Y-W, Yasukawa T, Dalla Rosa I, Khiati S, Pommier Y (2014) Increased negative supercoiling of mtDNA in TOP1mt knockout mice and presence of topoisomerases II\u03b1 and II\u03b2 in vertebrate mitochondria. Nucleic Acids Res 42:7259\u20137267","journal-title":"Nucleic Acids Res"},{"key":"10091_CR70","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-016-0028-x","volume":"7","author":"H Zhang","year":"2017","unstructured":"Zhang H, Seol Y, Agama K, Neuman KC, Pommier Y (2017) Distribution bias and biochemical characterization of TOP1MT single nucleotide variants. Sci Rep 7:1\u201311","journal-title":"Sci Rep"}],"container-title":["Journal of Molecular Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00239-022-10091-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00239-022-10091-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00239-022-10091-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,8]],"date-time":"2023-04-08T04:09:17Z","timestamp":1680926957000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00239-022-10091-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,18]]},"references-count":72,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2023,4]]}},"alternative-id":["10091"],"URL":"https:\/\/doi.org\/10.1007\/s00239-022-10091-z","relation":{},"ISSN":["0022-2844","1432-1432"],"issn-type":[{"value":"0022-2844","type":"print"},{"value":"1432-1432","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,18]]},"assertion":[{"value":"10 September 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 December 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 January 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"None to declare.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical Approval"}},{"value":"Not applicable.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for Publication"}},{"value":"Not applicable.","order":5,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent to Participate"}}]}}