The repetitive DNA content of fish sex chromosomes provides valuable insights into specificities and patterns of their genetic sex determination systems. In this study, we revealed the genomic satellite DNA (satDNA) content of Megaleporinuselongatus, a Neotropical fish species with Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosomes, through high-throughput analysis and graph-based clustering, isolating 68 satDNA families. By physically mapping these sequences in female metaphases, we discovered 15 of the most abundant satDNAs clustered in its chromosomes, 9 of which were found exclusively in the highly heterochromatic W1. This heteromorphic sex chromosome showed the highest amount of satDNA accumulations in this species. The second most abundant family, MelSat02-26, shared FISH signals with the NOR-bearing pair in similar patterns and is linked to the multiple sex chromosome system. Our results demonstrate the diverse satDNA content in M. elongatus, especially in its heteromorphic sex chromosome. Additionally, we highlighted the different accumulation patterns and distribution of these sequences across species by physically mapping these satDNAs in other Anostomidae, Megaleporinusmacrocephalus and Leporinusfriderici (a species without differentiated sex chromosomes).

Artoni RF, Bertollo LAC: Evolutionary aspects of the ZZ/ZW sex chromosome system in the Characidae fish, genus Triportheus. A monophyletic state and NOR location on the W chromosome. Heredity 89:15-19 (2002).
Bachtrog D, Kirkpatrick M, Mank JE, McDaniel SF, Pires JC, et al: Are all sex chromosomes created equal? Trends Genet 27:350-357 (2011).
Biscotti MA, Barucca M, Canapa A: New insights into the genome repetitive fraction of the Antarctic bivalve Adamussium colbecki. PLoS One 13:e0194502 (2018).
Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, et al: The genomic substrate for adaptive radiation in African cichlid fish. Nature 513:375-381 (2014).
Cabral-de-Mello DC, Moura RC, Martins C: Chromosomal mapping of repetitive DNAs in the beetle Dichotomius geminatus provides the first evidence for an association of 5S rRNA and histone H3 genes in insects, and repetitive DNA similarity between the B chromosome and A complement. Heredity 104:393-400 (2010).
Caetano de Barros L, Piscor D, Parise-Maltempi PP, Feldberg E: Differentiation and evolution of the W chromosome in the fish species of Megaleporinus (Characiformes, Anostomidae). Sex Dev 12:204-209 (2018).
Charlesworth B: The evolution of sex chromosomes. Science 251:1030-1033 (1991).
Charlesworth B, Sniegowski P, Stephan W: The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215-220 (1994).
da Silva EL, de Borba RS, Parise-Maltempi PP: Chromosome mapping of repetitive sequences in Anostomidae species: implications for genomic and sex chromosome evolution. Mol Cytogenet 5:45 (2012).
de Almeida Toledo LF, Foresti F: Morphologically differentiated sex chromosomes in neotropical freshwater fish. Genetica 111:91-100 (2001).
Ezaz T, Stiglec R, Veyrunes F, Marshall Graves JA: Relationships between vertebrate ZW and XY sex chromosome systems. Curr Biol 16:R736-743 (2006).
Ezaz T, Srikulnath K, Graves JA: Origin of amniote sex chromosomes: an ancestral super-sex chromosome, or common requirements? J Hered 108:94-105 (2017).
Foresti F, Almeida Toledo LF, Toledo SA: Polymorphic nature of nucleolus organizer regions in fishes. Cytogenet Cell Genet 31:137-144 (1981).
Galetti PM Jr, Foresti F: Evolution of the ZZ/ZW system in Leporinus (Pisces, Anostomidae). Cytogenet Cell Genet 43:43-46 (1986).
Galetti PM Jr, Cesar ACG, Venere PC: Heterochromatin and NORs variability in Leporinus fish (Anostomidae, Characiformes). Caryologia 44:287-292 (1991).
Galetti PM Jr, Lima NRW, Venere PC: A monophyletic ZW sex chromosome system in Leporinus (Anostomidae, Characiformes). Cytologia 60:375-382 (1995).
Gordon A, Hannon G: Fastx-toolkit. FASTQ/A short-reads pre-processing tools. (2010).
Graves JAM: Weird animal genomes and the evolution of vertebrate sex and sex chromosomes. Annu Rev Genet 42:565-586 (2008).
Hashimoto DT, Parise-Maltempi PP, Laudicina A, Bortolozzi J, Senhorini JA, et al: Repetitive DNA probe linked to sex chromosomes in hybrids between Neotropical fish Leporinus macrocephalus and Leporinus elongatus (Characiformes, Anostomidae). Cytogenet Genome Res 124:151-157 (2009).
Machado TC, Pansonato-Alves JC, Pucci MB, Nogaroto V, Almeida MC, et al: Chromosomal painting and ZW sex chromosomes differentiation in Characidium (Characiformes, Crenuchidae). BMC Genet 12:65 (2011).
Mank JE, Avise JC: Evolutionary diversity and turn-over of sex determination in teleost fishes. Sex Dev 3:60-67 (2009).
Marreta ME, Faldoni FLC, Parise-Maltempi PP: Cytogenetic mapping of the W chromosome in the genus Leporinus (Teleostei, Anostomidae) using a highly repetitive DNA sequence. J Fish Biol 80:630-637 (2012).
Meštrović N, Mravinac B, Pavlek M, Vojvoda-Zeljko T, Šatović E, Plohl M: Structural and functional liaisons between transposable elements and satellite DNAs. Chromosome Res 23:583-596 (2015).
Nakayama I, Foresti F, Tewari R, Schartl M, Chourrout D: Sex chromosome polymorphism and heterogametic males revealed by two cloned DNA probes in the ZW/ZZ fish Leporinus elongatus. Chromosoma 103:31-39 (1994).
Navrátilová A, Koblížková A, Macas J: Survey of extrachromosomal circular DNA derived from plant satellite repeats. BMC Plant Biol 8:90 (2008).
Novák P, Neumann P, Macas J: Graph-based clustering and characterization of repetitive sequences in next-generation sequencing data. BMC Bioinformatics 11:378 (2010).
Novák P, Neumann P, Pech J, Steinhaisl J, Macas J: RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads. Bioinformatics 29:792-793 (2013).
Parise-Maltempi PP, Martins C, Oliveira C, Foresti F: Identification of a new repetitive element in the sex chromosomes of Leporinus elongatus (Teleostei: Characiformes: Anostomidae): new insights into the sex chromosomes of Leporinus. Cytogenet Genome Res 116:218-223 (2007).
Parise-Maltempi PP, da Silva EL, Rens W, Dearden F, O'Brien PC, et al: Comparative analysis of sex chromosomes in Leporinus species (Teleostei, Characiformes) using chromosome painting. BMC Genet 14:60 (2013).
Pinkel D, Straume T, Gray JW: Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934-2938 (1986).
Plohl M, Mestrovic N, Mravinac B: Satellite DNA evolution. Genome Dyn 7:126-152 (2012).
Poltronieri J, Marquioni V, Bertollo LAC, Kejnovsky E, Molina WF, et al: Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet Genome Res 142:40-45 (2014).
Ramirez JL, Birindelli JLO, Galetti PM Jr: A new genus of Anostomidae (Ostariophysi: Characiformes): diversity, phylogeny and biogeography based on cytogenetic, molecular and morphological data. Mol Phylogenet Evol 107:308-323 (2017).
Ruiz-Ruano FJ, Cuadrado A, Montiel EE, Camacho JP, Lopez-Leon MD: Next generation sequencing and FISH reveal uneven and nonrandom microsatellite distribution in two grasshopper genomes. Chromosoma 124:221-234 (2015).
Ruiz-Ruano FJ, López-León MD, Cabrero J, Camacho JPM: High-throughput analysis of the satellitome illuminates satellite DNA evolution. Sci Rep 6:28333 (2016).
Schartl M, Schmid M, Nanda I: Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma 125:553-571 (2016).
Silva DMZA, Utsunomia R, Ruiz-Ruano FJ, Daniel SN, Porto-Foresti F, et al: High-throughput analysis unveils a highly shared satellite DNA library among three species of fish genus Astyanax. Sci Rep 7:12726 (2017).
Splendore de Borba R, Lourenço da Silva E, Parise-Maltempi PP: Chromosome mapping of retrotransposable elements Rex1 and Rex3 in Leporinus Spix, 1829 species (Characiformes: Anostomidae) and its relationships among heterochromatic segments and W sex chromosome. Mob Genet Elements 3:e27460 (2013).
Ugarković Ð, Plohl M: Variation in satellite DNA profiles - causes and effects. EMBO J 21:5955-5959 (2002).
Utsunomia R, Ruiz-Ruano FJ, Silva DMZA, Serrano EA, Rosa IF, et al: A glimpse into the satellite DNA library in Characidae fish (Teleostei, Characiformes). Front Genet 8:103 (2017).
Utsunomia R, Silva DMZA, Ruiz-Ruano FJ, Goes CAG, Melo S, et al: Satellitome landscape analysis of Megaleporinus macrocephalus (Teleostei, Anostomidae) reveals intense accumulation of satellite sequences on the heteromorphic sex chromosome. Sci Rep 9:5856 (2019).
Wright AE, Dean R, Zimmer F, Mank JE: How to make a sex chromosome. Nat Commun 7:12087 (2016).
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.