Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciata

Supernumerary B chromosomes are dispensable elements found in several groups of eukaryotes, and their impacts in host organisms are not clear. The cichlid fish Astatotilapia latifasciata presents one or two large metacentric B chromosomes. These elements affect the transcription of several classes o...

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Main Authors: Adauto Lima Cardoso, Bruno Evaristo de Almeida Fantinatti, Natália Bortholazzi Venturelli, Bianca de Oliveira Carmello, Rogério Antonio de Oliveira, Cesar Martins
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-04-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.00324/full
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author Adauto Lima Cardoso
Bruno Evaristo de Almeida Fantinatti
Natália Bortholazzi Venturelli
Bianca de Oliveira Carmello
Rogério Antonio de Oliveira
Cesar Martins
author_facet Adauto Lima Cardoso
Bruno Evaristo de Almeida Fantinatti
Natália Bortholazzi Venturelli
Bianca de Oliveira Carmello
Rogério Antonio de Oliveira
Cesar Martins
author_sort Adauto Lima Cardoso
collection DOAJ
description Supernumerary B chromosomes are dispensable elements found in several groups of eukaryotes, and their impacts in host organisms are not clear. The cichlid fish Astatotilapia latifasciata presents one or two large metacentric B chromosomes. These elements affect the transcription of several classes of RNAs. Here, we evaluated the epigenetic DNA modification status of B chromosomes using immunocytogenetics and assessed the impact of B chromosome presence on the global contents of 5-methylcytosine (5mC) and 5-hydroxymethylcytosine (5hmC) and the molecular mechanisms underlying these variations. We found that the B chromosome of A. latifasciata has an active pattern of DNA epimarks, and its presence promotes the loss of 5mC in gonads of females with B chromosome (FB+) and promotes the loss of 5hmC in the muscle of males with the B element (MB+). Based on the transcriptional quantification of DNA modification genes (dnmt, tet, and tdg) and their candidate regulators (idh genes, microRNAs, and long non-coding RNAs) and on RNA-protein interaction prediction, we suggest the occurrence of passive demethylation in gonads of FB+ and 5hmC loss by Tet inhibition or by 5hmC oxidation in MB+ muscle. We suggest that these results can also explain the previously reported variations in the transcription levels of several classes of RNA depending on B chromosome presence. The DNA modifications detected here are also influenced by sex. Although the correlation between B chromosomes and sex has been previously reported, it remains unexplained. The B chromosome of A. latifasciata seems to be active and impacts cell physiology in a very complex way, including at the epigenetic level.
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spelling doaj.art-f655b36107984017a4af609b4698d8822022-12-22T02:08:32ZengFrontiers Media S.A.Frontiers in Genetics1664-80212019-04-011010.3389/fgene.2019.00324437787Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciataAdauto Lima Cardoso0Bruno Evaristo de Almeida Fantinatti1Natália Bortholazzi Venturelli2Bianca de Oliveira Carmello3Rogério Antonio de Oliveira4Cesar Martins5Integrative Genomics Laboratory, Department of Morphology, Institute of Biosciences, São Paulo State University – Universidade Estadual Paulista, Botucatu, BrazilIntegrative Genomics Laboratory, Department of Morphology, Institute of Biosciences, São Paulo State University – Universidade Estadual Paulista, Botucatu, BrazilIntegrative Genomics Laboratory, Department of Morphology, Institute of Biosciences, São Paulo State University – Universidade Estadual Paulista, Botucatu, BrazilIntegrative Genomics Laboratory, Department of Morphology, Institute of Biosciences, São Paulo State University – Universidade Estadual Paulista, Botucatu, BrazilDepartment of Biostatistics, Institute of Biosciences, São Paulo State University – Universidade Estadual Paulista, Botucatu, BrazilIntegrative Genomics Laboratory, Department of Morphology, Institute of Biosciences, São Paulo State University – Universidade Estadual Paulista, Botucatu, BrazilSupernumerary B chromosomes are dispensable elements found in several groups of eukaryotes, and their impacts in host organisms are not clear. The cichlid fish Astatotilapia latifasciata presents one or two large metacentric B chromosomes. These elements affect the transcription of several classes of RNAs. Here, we evaluated the epigenetic DNA modification status of B chromosomes using immunocytogenetics and assessed the impact of B chromosome presence on the global contents of 5-methylcytosine (5mC) and 5-hydroxymethylcytosine (5hmC) and the molecular mechanisms underlying these variations. We found that the B chromosome of A. latifasciata has an active pattern of DNA epimarks, and its presence promotes the loss of 5mC in gonads of females with B chromosome (FB+) and promotes the loss of 5hmC in the muscle of males with the B element (MB+). Based on the transcriptional quantification of DNA modification genes (dnmt, tet, and tdg) and their candidate regulators (idh genes, microRNAs, and long non-coding RNAs) and on RNA-protein interaction prediction, we suggest the occurrence of passive demethylation in gonads of FB+ and 5hmC loss by Tet inhibition or by 5hmC oxidation in MB+ muscle. We suggest that these results can also explain the previously reported variations in the transcription levels of several classes of RNA depending on B chromosome presence. The DNA modifications detected here are also influenced by sex. Although the correlation between B chromosomes and sex has been previously reported, it remains unexplained. The B chromosome of A. latifasciata seems to be active and impacts cell physiology in a very complex way, including at the epigenetic level.https://www.frontiersin.org/article/10.3389/fgene.2019.00324/fullsupernumerary chromosome5-methylcytosine5-hydroxymethylcytosineDNA methylationDNA demethylationmicroRNA
spellingShingle Adauto Lima Cardoso
Bruno Evaristo de Almeida Fantinatti
Natália Bortholazzi Venturelli
Bianca de Oliveira Carmello
Rogério Antonio de Oliveira
Cesar Martins
Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciata
Frontiers in Genetics
supernumerary chromosome
5-methylcytosine
5-hydroxymethylcytosine
DNA methylation
DNA demethylation
microRNA
title Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciata
title_full Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciata
title_fullStr Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciata
title_full_unstemmed Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciata
title_short Epigenetic DNA Modifications Are Correlated With B Chromosomes and Sex in the Cichlid Astatotilapia latifasciata
title_sort epigenetic dna modifications are correlated with b chromosomes and sex in the cichlid astatotilapia latifasciata
topic supernumerary chromosome
5-methylcytosine
5-hydroxymethylcytosine
DNA methylation
DNA demethylation
microRNA
url https://www.frontiersin.org/article/10.3389/fgene.2019.00324/full
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