Abstract
Sex chromosome differentiation is subject to independent evolutionary processes among different lineages. The accumulation of repetitive DNAs and consequent crossing-over restriction guide the origin of the heteromorphic sex chromosome region. Several Neotropical fish species have emerged as interesting models for understanding evolution and genome diversity, although knowledge of their genomes is scarce. Here, we investigate the content of repetitive DNAs between males and females of Apareiodon sp. based on large-scale genomic data focusing on W sex chromosome differentiation. In Apareiodon, females are the heterogametic sex (ZW) and males are the homogametic sex (ZZ). The genome size estimate for Apareiodon was 1.2 Gb (with ~ 42× and ~ 47× coverage for males and females, respectively). In Apareiodon sp., approximately 36% of the genome was composed of repetitive DNAs and transposable elements (TEs) were the most abundant class. Read coverage analysis revealed different amounts of repetitive DNAs in males and females. The female-enriched clusters were located on the W sex chromosome and were mostly composed of microsatellite expansions and DNA transposons. Landscape analysis of TE contents demonstrated two major waves of invasions of TEs in the Apareiodon genome. Estimation of TE insertion times correlated with in situ locations permitted the inference that helitron, Tc1-mariner, and CMC EnSpm DNA transposons accumulated repeated copies during W chromosome differentiation between 20 and 12 million years ago. DNA transposons and microsatellite expansions appeared to be major players in W chromosome differentiation and to guide modifications in the genome content of the heteromorphic sex chromosomes.
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References
Arkhipova I, Meselson M (2005) Deleterious transposable elements and the extinction of asexuals. Bioessays 27:76–85. https://doi.org/10.1002/bies.20159
Bachtrog D (2013) Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 14:113–124. https://doi.org/10.1038/nrg3366
Bellafronte E, Schemberger MO, Moreira-Filho O, Almeida MC, Artoni RF, Margarido VP, Vicari MR (2011) Chromosomal markers in Parodontidae: an analysis of new and reviewed data with phylogenetic inferences. Rev Fish Biol Fish 12:559–570. https://doi.org/10.1007/s11160-010-9177-3
Bergero R, Charlesworth D (2009) The evolution of restricted recombination in sex chromosomes. Trends Ecol Evol 24:94–102. https://doi.org/10.1016/j.tree.2008.09.010
Bertollo LAC, Takahashi CS, Moreira-Filho O (1978) Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae). Braz J Genet 1:103–120
Bradnam KR, Fass JN, Alexandrov A, Baranay P, Bechner M, Birol I, Boisvert S, Chapman JA, Chapuis G, Chikhi R, Chitsaz H, Chou WC, Corbeil J, del Fabbro C, Docking TR, Durbin R, Earl D, Emrich S, Fedotov P, Fonseca NA, Ganapathy G, Gibbs RA, Gnerre S, Godzaridis É, Goldstein S, Haimel M, Hall G, Haussler D, Hiatt JB, Ho IY, Howard J, Hunt M, Jackman SD, Jaffe DB, Jarvis ED, Jiang H, Kazakov S, Kersey PJ, Kitzman JO, Knight JR, Koren S, Lam TW, Lavenier D, Laviolette F, Li Y, Li Z, Liu B, Liu Y, Luo R, MacCallum I, MacManes MD, Maillet N, Melnikov S, Naquin D, Ning Z, Otto TD, Paten B, Paulo OS, Phillippy AM, Pina-Martins F, Place M, Przybylski D, Qin X, Qu C, Ribeiro FJ, Richards S, Rokhsar DS, Ruby JG, Scalabrin S, Schatz MC, Schwartz DC, Sergushichev A, Sharpe T, Shaw TI, Shendure J, Shi Y, Simpson JT, Song H, Tsarev F, Vezzi F, Vicedomini R, Vieira BM, Wang J, Worley KC, Yin S, Yiu SM, Yuan J, Zhang G, Zhang H, Zhou S, Korf IF (2013) Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. GigaScience 2(10). https://doi.org/10.1186/2047-217X-2-10
Chalopin D, Volff JN, Galiana D, Anderson JL, Schartl M (2015) Transposable elements and early evolution of sex chromosomes in fish. Chromosom Res 23:545–560. https://doi.org/10.1007/s10577-015-9490-8
Charlesworth B (1991) The evolution of sex chromosomes. Science 251:1030–1033. https://doi.org/10.1126/science.1998119
Charlesworth B (1996) The evolution of chromosomal sex determination and dosage compensation. Curr Biol 6:149–162. https://doi.org/10.1016/S0960-9822(02)00448-7
Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220. https://doi.org/10.1038/371215a0
Charlesworth D, Charlesworth B, Marais G (2005) Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128. https://doi.org/10.1038/sj.hdy.6800697
Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P, Song W, An N, Chalopin D, Volff JN, Hong Y, Li Q, Sha Z, Zhou H, Xie M, Yu Q, Liu Y, Xiang H, Wang N, Wu K, Yang C, Zhou Q, Liao X, Yang L, Hu Q, Zhang J, Meng L, Jin L, Tian Y, Lian J, Yang J, Miao G, Liu S, Liang Z, Yan F, Li Y, Sun B, Zhang H, Zhang J, Zhu Y, du M, Zhao Y, Schartl M, Tang Q, Wang J (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46:253–260. https://doi.org/10.1038/ng.2890
Chen X, Mei J, Wu J, Jing J, Ma W, Zhang J, Gui JF (2015) A comprehensive transcriptome provides candidate genes for sex determination/differentiation and SSR/SNP markers in yellow catfish. Mar Biotechnol 17:190–198. https://doi.org/10.1007/s10126-014-9607-7
Coates BS, Sumerford DV, Hellmich RL, Lewis LC (2010) Helitron-like transposon superfamily from Lepidoptera disrupts (GAAA)n microsatellites and is responsible for flanking sequence similarity within a microsatellite family. J Mol Evol 70:275–288. https://doi.org/10.1007/s00239-010-9330-6
de Koning AJ, Gu W, Castoe TA, Batzer MA, Pollock DD (2011) Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 71:e1002384. https://doi.org/10.1371/journal.pgen.1002384
de Oliveira EA, Sember A, Bertollo LAC, Yano CF, Ezaz T, Moreira-Filho O, Hatanaka T, Trifonov V, Liehr T, al-Rikabi ABH, Ráb P, Pains H, Cioffi MB (2018) Tracking the evolutionary pathway of sex chromosomes among fishes: characterizing the unique XX/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes). Chromosoma 127:115–128. https://doi.org/10.1007/s00412-017-0648-3
do Nascimento VD, Coelho KA, Nogaroto V, Almeida RB, Ziemniczak K, Centofante L, Pavanelli CS, Torres RA, Moreira-Filho O, Vicari MR (2018) Do multiple karyomorphs and population genetics of freshwater darter characines (Apareiodon affinis) indicate chromosomal speciation? Zool Anz 272:93–103. https://doi.org/10.1016/j.jcz.2017.12.006
Fernández-Medina RD, Ribeiro JMC, Carareto CMA, Velasque L, Struchiner CJ (2012) Losing identity: structural diversity of transposable elements belonging to different classes in the genome of Anopheles gambiae. BMC Genomics 13:272. https://doi.org/10.1186/1471-2164-13-272
Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9:397–405. https://doi.org/10.1038/nrg2337
Frank-Kamenetskii MD, Mirkin SM (1995) Triplex DNA structures. Annu Rev Biochem 64:65–95. https://doi.org/10.1146/annurev.bi.64.070195.000433
Gazoni T, Haddad CFB, Narimatsu H, Cabral-de-Mello DC, Lyra ML, Parise-Maltempi PP (2018) More sex chromosomes than autosomes in the Amazonian frog Leptodactylus pentadactylus. Chromosoma 127:269–278. https://doi.org/10.1007/s00412-018-0663-z
Heikkinen E, Launonen V, Muller E, Bachmann L (1995) The pvB370 BamIII satellite DNA family of the Drosophila virilis group and its evolutionary relation to mobile dispersed genetic pDv elements. J Mol Evol 41:604–614. https://doi.org/10.1007/BF00175819
Herpin A, Braasch I, Kraeussling M, Schmidt C, Thoma EC, Nakamura S, Tanaka M, Schartl M (2010) Transcriptional rewiring of the sex determining Dmrt1 gene duplicate by transposable elements. PLoS Genet 6:e1000844. https://doi.org/10.1371/journal.pgen.1000844
Kapitonov VV, Holmquist GP, Jurka J (1998) L1 repeat is a basic unit of heterochromatin satellites in Cetaceans. Mol Biol Evol 15:611–612
Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L, Bourque G, Yandell M, Feschotte C (2013) Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 9:e1003470. https://doi.org/10.1371/journal.pgen.1003470
Keinath MC, Timoshevskaya N, Timoshevskiy VA, Voss SR, Smith JJ (2018) Miniscule differences between the sex chromosomes in the giant genome of a salamander, Ambystoma mexicanum. Sci Rep 8:17882. https://doi.org/10.1038/s41598-018-36209-2
Kelkar YD, Eckert KA, Chiaromonte F, Makova KD (2011) A matter of life or death: how microsatellites emerge in and vanish from the human genome. Genome Res 21:2038–2048 http://www.genome.org/cgi/doi/10.1101/gr.122937.111
Kidwell MG, Lisch DR (2001) Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24. https://doi.org/10.1111/j.0014-3820.2001.tb01268.x
Kirkness EF, Bafna V, Halpern AL, Levy S, Remington K, Rusch DB, Delcher AL, Pop M, Wang W, Fraser CM, Venter JC (2003) The dog genome: survey sequencing and comparative analysis. Science 301:1898–1903. https://doi.org/10.1126/science.1086432
Komissarov AS, Galkina SA, Koshel EI, Kulak MM, Dyomin AG, O’Brien SJ, Gaginskaya ER, Saifitdinova AF (2018) New high copy tandem repeat in the content of the chicken W chromosome. Chromosoma 127:73–83. https://doi.org/10.1007/s00412-017-0646-5
Li SF, Guo YJ, Li JR, Zhang DX, Wang BX, Li N, Deng CL, Gao WJ (2019) The landscape of transposable elements and satellite DNAs in the genome of a dioecious plant spinach (Spinacia oleracea L.). Mob DNA 10(3). https://doi.org/10.1186/s13100-019-0147-6
Marino-Ramirez L, Lewis KC, Landsman D, Jordan IK (2005) Transposable elements donate lineage-specific regulatory sequences to host genomes. Cytogenet Genome Res 110:333–341. https://doi.org/10.1159/000084965
Milani D, Cabral-de-Mello DC (2014) Microsatellite organization in the grasshopper Abracris flavolineata (Orthoptera: Acrididae) revealed by FISH mapping: remarkable spreading in the A and B chromosomes. PLoS One 9:e97956. https://doi.org/10.1371/journal.pone.0097956
Mongue AJ, Nguyen P, Volenikova A, Walters JR (2017) Neo-sex chromosomes in the Monarch butterfly, Danaus plexippus. G3 (Bethesda) 7:3281–3294. https://doi.org/10.1534/g3.117.300187
Novak P, Neumann P, Macas J (2010) Graph-based clustering and characterization of repetitive sequences in 592 next-generation sequencing data. BMC Bioinformatics 11:378. https://doi.org/10.1186/1471-2105-11-378
Novak 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. https://doi.org/10.1093/bioinformatics/btt054
Pinkel D, Straume T, Gray JW (1986) Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci U S A 83:2934–2938. https://doi.org/10.1073/pnas.83.9.2934
Priyadarshini P, Murthy BS, Nagaraju J, Singh L (2003) GATA-binding protein expressed predominantly in the pupal ovary of the silkworm, Bombyx mori. Insect Biochem Mol Biol 33:185–195. https://doi.org/10.1016/S0965-1748(02)00190-X
Pucci MB, Barbosa P, Nogaroto V, Almeida MC, Artoni RF, Pansonato-Alves JC, Scacchetti PC, Foresti F, Moreira-Filho O, Vicari MR (2016) Chromosomal spreading of microsatellites and (TTAGGG)n sequences in the Characidium zebra and C. gomesi genomes (Characiformes: Crenuchidae). Cytogenet Genome Res 149:182–190. https://doi.org/10.1159/000447959
Raymond CS, Murphy MW, O'Sullivan MG, Bardwell VJ, Zarkower D (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14:2587–2595. https://doi.org/10.1101/gad.834100
Saitoh Y, Saitoh H, Ohtomo K, Mizuno S (1991) Occupancy of the majority of DNA in the chicken W chromosome by bent-repetitive sequences. Chromosoma 101:32–40. https://doi.org/10.1007/BF00360684
Schemberger MO, Bellafronte E, Nogaroto V, Almeida MC, Schühli GS, Artoni RF, Moreira-Filho O, Vicari MR (2011) Differentiation of repetitive DNA sites and sex chromosome systems reveal closely related group in Parodontidae (Actinopterygii: Characiformes). Genetica 139:1499–1508. https://doi.org/10.1007/s10709-012-9649-6
Schemberger MO, Oliveira JIN, Nogaroto V, Almeida MC, Artoni RF, Cestari MM, Moreira-Filho O, Vicari MR (2014) Construction and characterization of a repetitive DNA library in Parodontidae (Actinopterygii: Characiformes): a genomic and evolutionary approach to the degeneration of the W sex chromosome. Zebrafish 11:518–527. https://doi.org/10.1089/zeb.2014.1013
Schemberger MO, Nogaroto V, Almeida MC, Artoni RF, Valente GT, Martins C, Moreira-Filho O, Cestari MM, Vicari MR (2016) Sequence analyses and chromosomal distribution of the Tc1/Mariner element in Parodontidae fish (Teleostei: Characiformes). Gene 593:308–314. https://doi.org/10.1016/j.gene.2016.08.034
Singh L, Wadhwan R, Naidu S, Nagaraj R, Ganesan M (1994) Sex- and tissue-specific Bkm (GATA)-binding protein in the germ cells of heterogametic sex. J Biol Chem 269:25321–25327
Smit AFA, Hubley R (2008–2015) RepeatModeler Open—1.0 Available from http://www.repeatmasker.org. Accessed 26 Nov 2018
Smit AFA, Hubley R, Green P (2013–2015) RepeatMasker Open—4.0. Available at: http://www.repeatmasker.org. Accessed 26 Nov 2018
Steinemann S, Steinemann M (2005) Retroelements: tools for sex chromosome evolution. Cytogenet Genome Res 110:134–143. https://doi.org/10.1159/000084945
Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306. https://doi.org/10.1016/0014-4827(72)90558-7
Teaniniuraitemoana V, Huvet A, Levy P, Klopp C, Lhuillier E, Gaertner-Mazouni N, Le Moullac G (2014) Gonad transcriptome analysis of pearl oyster Pinctada margaritifera: identification of potential sex differentiation and sex determining genes. BMC Genomics 15:491. https://doi.org/10.1186/1471-2164-15-491
Traldi JB, Vicari MR, Martinez JDF, Blanco DR, Lui RL, Moreira-Filho O (2016) Chromosome analyses of Apareiodon argenteus and Apareiodon davisi (Characiformes, Parodontidae): an extensive chromosomal polymorphism of 45S and 5S ribosomal DNAs. Zebrafish 13:19–25. https://doi.org/10.1089/zeb.2015.1124
Treangen TJ, Salzberg SL (2012) Repetitive DNA and next-generation sequencing: computational challenges and solutions. Nat Rev Genet 13:36–46. https://doi.org/10.1038/nrg3117
Vicari MR, Moreira-Filho O, Artoni RF, Bertollo LAC (2006) ZZ/ZW sex chromosome system in an undescribed species of the genus Apareiodon Characiformes, Parodontidae. Cytogenet Genome Res 114:163–168. https://doi.org/10.1159/000093333
Vicari MR, Nogaroto V, Noleto RB, Cestari MM, Cioffi MB, Almeida MC, Moreira-Filho O, Bertollo LAC, Artoni RF (2010) Satellite DNA and chromosomes in Neotropical fishes: methods, applications and perspectives. J Fish Biol 76:1094–1116. https://doi.org/10.1111/j.1095-8649.2010.02564.x
Vicente VE, Bertollo LA, Valentini SR, Moreira-Filho O (2003) Origin and differentiation of sex chromosome system in Parodon hilarii (Pisces, Parodontidae). Satellite DNA, G and C banding. Genetica 119:115–120. https://doi.org/10.1023/A:1026082904672
Viger RS, Mertineit C, Trasler JM, Nemer M (1998) Transcription factor GATA 4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the MIS promoter. Development 125:2665–2675
Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C (2003) Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 19:674–678. https://doi.org/10.1016/j.tig.2003.10.006
Waterhouse RM, Seppey M, Simão FA, Manni M, Ioannidis P, Klioutchnikov G, Kriventseva EV, Zdobnov EM (2017) BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol Biol Evol 35:543–548. https://doi.org/10.1093/molbev/msx319
White MA, Kitano J, Peichel CL (2015) Purifying selection maintains dosage-sensitive genes during degeneration of the threespine stickleback Y chromosome. Mol Biol Evol 32:1981–1995. https://doi.org/10.1093/molbev/msv078
Wilder J, Hollocher H (2001) Mobile elements and the genesis of microsatellites in dipterans. Mol Biol Evol 18:384–392. https://doi.org/10.1093/oxfordjournals.molbev.a003814
Xin H, Zhang T, Han Y, Wu Y, Shi J, Xi M, Jiang J (2018) Chromosome painting and comparative physical mapping of the sex chromosomes in Populus tomentosa and Populus deltoides. Chromosoma 127:313–321. https://doi.org/10.1007/s00412-018-0664-y
Zerbino D, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res gr-074492. https://doi.org/10.1101/gr.074492.107
Ziemniczak K, Traldi JB, Nogaroto V, Almeida MC, Artoni RF, Moreira-Filho O, Vicari MR (2014) In situ localization of (GATA)n and (TTAGGG)n repeated DNAs and W sex chromosome differentiation in Parodontidae (Actinopterygii: Characiformes). Cytogenet Genome Res 144:325–332. https://doi.org/10.1159/000370297
Acknowledgments
The authors are grateful to ICMBio (Instituto Chico Mendes de Conservação da Biodiversidade) (license number 10538-1 to collect specimens). This study was supported by the Fundação Araucária (Fundação Araucária de Apoio ao Desenvolvimento Científico e Tecnológico do Estado do Paraná), FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo, grant number: 2015/16661-1), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Finance Code 001), and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, grant number: 304166/2016-2).
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Supplementary figure 2
Repeat landscape of DNA transposons in the male Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate the distinct element types described on the right side. (HTML 26 kb)
Supplementary figure 3
Repeat landscape of DNA transposons in the female Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate distinct element types described on the right side. (HTML 25 kb)
Supplementary figure 4
Repeat landscape of retrotransposons in the male Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate distinct element types described on the right. (HTML 40 kb)
Supplementary figure 5
Repeat landscape of retrotransposons in the male Apareiodon sp. genome. The graphs show, for each element, the sequence divergence from their consensus sequence (x-axis) in relation to their number of copies in the genome (y-axis). Peaks represent waves of insertion (yellow arrows) of specific elements in the genome. Elements with older waves of insertion are presented on the right side of the graph, while recent waves of insertions are depicted on the left side. Different colors indicate distinct element types described on the right side. (HTML 40 kb)
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Schemberger, M.O., Nascimento, V.D., Coan, R. et al. DNA transposon invasion and microsatellite accumulation guide W chromosome differentiation in a Neotropical fish genome. Chromosoma 128, 547–560 (2019). https://doi.org/10.1007/s00412-019-00721-9
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DOI: https://doi.org/10.1007/s00412-019-00721-9