Duílio Mazzoni Zerbinato de Andrade Silva1, Francisco J Ruiz-Ruano2,3,4, Ricardo Utsunomia5,6, María Martín-Peciña7, Jonathan Pena Castro8,9, Paula Paccielli Freire1,10, Robson Francisco Carvalho1, Diogo T Hashimoto11, Alexander Suh12,13, Claudio Oliveira1, Fábio Porto-Foresti6, Roberto Ferreira Artoni8,9, Fausto Foresti1, Juan Pedro M Camacho14. 1. Departamento de Biologia Estrutural e Funcional, Instituto de Biociências de Botucatu, Universidade Estadual Paulista, UNESP, Distrito de Rubião Junior, Botucatu, SP, 18618-970, Brazil. 2. Department of Organismal Biology - Systematic Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36, Uppsala, Sweden. francisco.ruiz-ruano@ebc.uu.se. 3. Departamento de Genética, Universidad de Granada, 18071, Granada, Spain. francisco.ruiz-ruano@ebc.uu.se. 4. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TU, UK. francisco.ruiz-ruano@ebc.uu.se. 5. Departamento de Genética, Instituto de Ciências Biológicas e da Saúde, ICBS, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ, 23897-000, Brazil. 6. Departamento de Ciências Biológicas, Faculdade de Ciências, Universidade Estadual Paulista, UNESP, Campus de Bauru, Bauru, SP, 17033-360, Brazil. 7. Departamento de Genética, Universidad de Granada, 18071, Granada, Spain. 8. Departamento de Genética e Evolução, Universidade Federal de São Carlos, UFSCAR, São Carlos, SP, 13565-905, Brazil. 9. Departamento de Biologia Estrutural, Molecular e Genética, Universidade Estadual de Ponta Grossa, UEPG, Ponta Grossa, PR, 84030-900, Brazil. 10. Departamento de Imunologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, USP, São Paulo, SP, 05508-900, Brazil. 11. Centro de Aquicultura, Universidade Estadual Paulista, UNESP, Campus Jaboticabal, Jaboticabal, SP, 14884-900, Brazil. 12. Department of Organismal Biology - Systematic Biology, Evolutionary Biology Centre, Uppsala University, SE-752 36, Uppsala, Sweden. 13. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TU, UK. 14. Departamento de Genética, Universidad de Granada, 18071, Granada, Spain. jpmcamac@ugr.es.
Abstract
BACKGROUND: Eukaryote genomes frequently harbor supernumerary B chromosomes in addition to the "standard" A chromosome set. B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond species level has remained untested. RESULTS: Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus Astyanax arose in a common ancestor at least 4 million years ago. We generated transcriptomes of A. scabripinnis and A. paranae 0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of A. scabripinnis and A. paranae share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of A. bockmanni and A. fasciatus, respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to nobox, a gene involved in oogenesis regulation. Importantly, the B chromosome nobox paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction. CONCLUSIONS: Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation.
BACKGROUND: Eukaryote genomes frequently harbor supernumerary B chromosomes in addition to the "standard" A chromosome set. B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond species level has remained untested. RESULTS: Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus Astyanax arose in a common ancestor at least 4 million years ago. We generated transcriptomes of A. scabripinnis and A. paranae 0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of A. scabripinnis and A. paranae share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of A. bockmanni and A. fasciatus, respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to nobox, a gene involved in oogenesis regulation. Importantly, the B chromosome nobox paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction. CONCLUSIONS: Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation.
Entities:
Keywords:
Astyanax; B chromosomes; Evolution; Genomics; Transcriptomics
Authors: Duilio M Z A Silva; Ricardo Utsunomia; José C Pansonato-Alves; Cláudio Oliveira; Fausto Foresti Journal: Cytogenet Genome Res Date: 2015-09-02 Impact factor: 1.636
Authors: Syed F Ahmad; Maryam Jehangir; Adauto L Cardoso; Ivan R Wolf; Vladimir P Margarido; Diogo C Cabral-de-Mello; Rachel O'Neill; Guilherme T Valente; Cesar Martins Journal: BMC Genomics Date: 2020-09-23 Impact factor: 3.969
Authors: Duílio M Z de A Silva; José Carlos Pansonato-Alves; Ricardo Utsunomia; Cristian Araya-Jaime; Francisco J Ruiz-Ruano; Sandro Natal Daniel; Diogo Teruo Hashimoto; Cláudio Oliveira; Juan Pedro M Camacho; Fábio Porto-Foresti; Fausto Foresti Journal: PLoS One Date: 2014-04-15 Impact factor: 3.240
Authors: Duílio M Z A Silva; Jonathan P Castro; Caio A G Goes; Ricardo Utsunomia; Mateus R Vidal; Cristiano N Nascimento; Lucas F Lasmar; Fabilene G Paim; Letícia B Soares; Claudio Oliveira; Fábio Porto-Foresti; Roberto F Artoni; Fausto Foresti Journal: Animals (Basel) Date: 2022-08-25 Impact factor: 3.231