Cytogenetic and Genome Research

Original Article

Great Abundance of Satellite DNA in Proceratophrys (Anura, Odontophrynidae) Revealed by Genome Sequencing

da Silva M.J.a · Fogarin Destro R.a · Gazoni T.a · Narimatsu H.a · Pereira dos Santos P.S.a · Haddad C.F.B.b · Parise-Maltempi P.P.a

Author affiliations

aDepartamento de Biologia, Instituto de Biociências, Universidade Estadual Paulista - UNESP, Rio Claro, Brazil; bDepartamento de Zoologia e Centro de Aquicultura, Instituto de Biociências, Universidade Estadual Paulista - UNESP, Rio Claro, Brazil

Related Articles for ""

Cytogenet Genome Res 2020;160:141-147

Log in to MyKarger to check if you already have access to this content.


Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

CHF 38.00 *
EUR 35.00 *
USD 39.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!


If you would like to redeem your KAB credit, please log in.


Save over 20% compared to the individual article price.

Learn more

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restrictions apply

Rental: USD 8.50
Cloud: USD 20.00

Select

Subscribe

  • Access to all articles of the subscribed year(s) guaranteed for 5 years
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates


Select
* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview
Abstract of Original Article

Accepted: February 10, 2020
Published online: March 07, 2020
Issue release date: April 2020

Number of Print Pages: 7
Number of Figures: 2
Number of Tables: 1

ISSN: 1424-8581 (Print)
eISSN: 1424-859X (Online)

For additional information: https://www.karger.com/CGR

Abstract

Most eukaryotic genomes contain substantial portions of repetitive DNA sequences. These are located primarily in highly compacted heterochromatin and, in many cases, are one of the most abundant components of the sex chromosomes. In this sense, the anuran Proceratophrys boiei represents an interesting model for analyses on repetitive sequences by means of cytogenetic techniques, since it has a karyotype with large blocks of heterochromatin and a ZZ/ZW sex chromosome system. The present study describes, for the first time, families of satellite DNA (satDNA) in the frog P. boiei. Its genome size was estimated at 1.6 Gb, of which 41% correspond to repetitive sequences, including satDNAs, rDNAs, transposable elements, and other elements characterized as non-repetitive. The satDNAs were mapped by FISH in the centromeric and pericentromeric regions of all chromosomes, suggesting a possible involvement of these sequences in centromere function. SatDNAs are also present in the W sex chromosome, occupying the entire heterochromatic area, indicating a probable contribution of this class of repetitive DNA to the differentiation of the sex chromosomes in this species. This study is a valuable contribution to the existing knowledge on repetitive sequences in amphibians. We show the presence of repetitive DNAs, especially satDNAs, in the genome of P. boiei that might be of relevance in genome organization and regulation, setting the stage for a deeper functional genome analysis of Proceratophrys.

© 2020 S. Karger AG, Basel




Related Articles:


References

  1. Amaro RC, Rodrigues MT, Yonenaga-Yassuda Y, Carnaval ACQ: Demographic processes in the montane Atlantic rainforest: molecular and cytogenetic evidence from the endemic frog Proceratophrys boiei. Mol Phylogenet Evol 62:880-888 (2012).
  2. Ananias F, Modesto ADS, Mendes SC, Napoli MF: Unusual primitive heteromorphic ZZ/ZW sex chromosomes in Proceratophrys boiei (Anura, Cycloramphidae, Alsodinae), with description of C-Band interpopulational polymorphism. Hereditas 144:206-212 (2007).
  3. Bachmann L, Sperlich D: Gradual evolution of a specific satellite DNA family in Drosophila ambigua, D. tristis and D. obscura. Mol Biol Evol 10:647-659 (1993).
  4. Baldissera FA Jr, Oliveira PSL, Kasahara S: Cytogenetics of four Brazilian Hyla species (Amphibia-Anura) and description of a case with a supernumerary chromosome. Rev Bras Genét 16:335-345 (1993).
  5. Charlesworth B, Sniegowski P, Stephan W: The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215-220 (1994).
  6. Choo KH, Vissel B, Nagy A, Earle E, Kalitsis P: A survey of the genomic distribution of alpha satellite DNA on all the human chromosomes, and derivation of a new consensus sequence. Nucleic Acids Res 19:1179-1182 (1991).
  7. Conte CE, Machado RA: Riqueza de espécies e distribuição espacial e temporal em comunidade de anuros (Amphibia, Anura) em uma localidade de Tijucas do Sul, Paraná, Brasil. Rev Bras Zool 22:940-948 (2005).
    External Resources
  8. da Silva EL, Busso AF, Parise-Maltempi PP: Characterization and genome organization of a repetitive element associated with the nucleolar organizer region in Leporinus elongatus (Anostomidae: Characiformes). Cytogenet Genome Res 139:22-28 (2013).
  9. Dover G: Molecular drive: a cohesive mode of species evolution. Nature 299:111-117 (1982).
  10. Dover G: Molecular drive. Trends Genet 18:587-589 (2002).
  11. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797 (2004).
  12. Feliciello I, Akrap I, Brajkovi J, Zlatar I, Ugarkovi U: Satellite DNA as a driver of population divergence in the red flour beetle Tribolium castaneum. Genome Biol Evol 7:228-239 (2015).
  13. Frost DR: Amphibian Species of the World: an Online Reference. Version 6.0 (American Museum of Natural History, New York 2020). http://research.amnh.org/herpetology/amphibia/index.html
  14. Garrido-Ramos MA: Satellite DNA in plants: more than just rubbish. Cytogenet Genome Res 146:153-170 (2015).
  15. Garrido-Ramos MA: Satellite DNA: an evolving topic. Genes 8:E230 (2017).
  16. Gatto KP, Mattos JV, Seger KR, Lourenço LB: Sex chromosome differentiation in the frog genus Pseudis involves satellite DNA and chromosome rearrangements. Front Genet 9:301 (2018).
  17. Gordon A, Hannon GJ: FASTX-Toolkit, FASTQ/A short-reads pre-processing tools. (2010). http://hannonlab.cshl.edu/fastx_toolkit
  18. Haddad CFB, Sazima I: Anfíbios anuros da Serra do Japi, in Morellato PC (ed): História Natural da Serra do Japi: Ecologia e Preservação de uma Área Florestal no Sudeste do Brasil (Unicamp, Campinas 1992).
  19. Junier T, Pagni M: Dotlet: diagonal plots in a web browser. Bioinformatics 16:178-179 (2000).
  20. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J: Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462-467 (2005).
  21. López-Flores I, Garrido-Ramos MA: The repetitive DNA content of eukaryotic genomes. Genome Dyn 7:1-28 (2012).
  22. Mestriner CA, Galetti PM Jr, Valentini SR, Ruiz IR, Abel LD, et al: Structural and functional evidence that a B chromosome in the characid fish Astyanax scabripinnis is an isochromosome. Heredity 85:1-9 (2000).
  23. Novák P, Neumann P, Pech P, 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).
  24. Novák P, Avila Robledillo L, Koblizkova A, Vrbova I, Neumann P, Macas J: TAREAN: a computational tool for identification and characterization of satellite DNA from unassembled short reads. Nucleic Acids Res 45:e111 (2017).
  25. Palacios-Gimenez OM, Dias GB, de Lima LG, Kuhn GCES, Ramos E, et al: High-throughput analysis of the satellitome revealed enormous diversity of satellite DNAs in the neo-Y chromosome of the cricket Eneoptera surinamensis. Sci Rep 7:6422 (2017).
  26. Palacios-Gimenez OM, Bardella VB, Lemos B, Cabral-de-Mello DC: Satellite DNAs are conserved and differentially transcribed among Gryllus cricket species. DNA Res 25:137-147 (2018).
  27. Pinkel D, Straume T, Gray JW: Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934-2938 (1986).
  28. Piras FM, Nergadze SG, Magnani E, Bertoni L, Attolini C, et al: Uncoupling of satellite DNA and centromeric function in the genus Equus. PLoS Genet 6:e1000845 (2010).
  29. Plohl M, Meštrović N, Mravinac B: Satellite DNA evolution. Genome Dyn 7:126-152 (2012).
  30. Plohl M, Meštrović N, Mravinac B: Centromere identity from the DNA point of view. Chromosoma 123:313-325 (2014).
  31. Prado GM, Pombal JP: Espécies de Proceratophrys Miranda-Ribeiro, 1920 com apêndices palpebrais (Anura; Cycloramphidae). Arq Zool 39:1-85 (2008).
    External Resources
  32. 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).
  33. Serafim H, Ienne S, Cicchi PJP, Jim J: Anurofauna de remanescentes de floresta Atlântica do município de São José do Barreiro, estado de São Paulo, Brasil. Biota Neotropica 8:69 (2008).
    External Resources
  34. Sumner AT: A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304-306 (1972).
  35. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA: molecular evolutionary genetics using maximun likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731-2739 (2011).
  36. Ugarkovic D, Plohl M: Variation in satellite DNA profiles-causes and effects. EMBO J 21:5955-5959 (2002).
  37. Vittorazzi SE, Lourenço LB, Del-Grande ML, Recco-Pimentel SM: Satellite DNA derived from 5S rDNA in Physalaemus cuvieri (Anura, Leiuperidae). Cytogenet Genome Res 134:101-107 (2011).
  38. Vittorazzi SE, Lourenço LB, Recco-Pimentel SM: Long-time evolution and highly dynamic satellite DNA in leptodactylid and hylodid frogs. BMC Genet 15:111 (2014).
  39. Zhang T, Talbert PB, Zhang W, Wu Y, Yang Z, et al: The CentO satellite confers translational and rotational phasing on cenH3 nucleosomes in rice centromeres. Proc Natl Acad Sci USA 110:4875-4883 (2013).
  40. Ziegler CG, Lamatsch DK, Steinlein C, Engel W, Schartl M, Schmid M: The giant B chromosome of the cyprinid fish Alburnus alburnus harbours a retrotransposon-derived repetitive DNA sequence. Chromosome Res 11:23-35 (2003).
  41. Zina J, Ennser J, Pinheiro SCP, Haddad CFB, Toledo LF: Taxocenose de anuros de uma mata semidecídua do interior do Estado de São Paulo e comparações com outras taxocenoses do Estado, sudeste do Brasil. Biota Neotropica 7:1-9 (2007).

Article / Publication Details

First-Page Preview
Abstract of Original Article

Accepted: February 10, 2020
Published online: March 07, 2020
Issue release date: April 2020

Number of Print Pages: 7
Number of Figures: 2
Number of Tables: 1

ISSN: 1424-8581 (Print)
eISSN: 1424-859X (Online)

For additional information: https://www.karger.com/CGR


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.
TOP