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Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families

In the Japanese hagfish, Eptatretus burgeri, approximately 21% of the genomic DNA in germ cells (2n = 52) consists of 16 chromosomes (eliminated [E]-chromosomes) that are eliminated from presumptive somatic cells (2n = 36). To uncover the eliminated genome (E-genome), we have identified 16 eliminate...

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Autores principales: Nagao, Kohei, Tanaka, Yoshiki, Kajitani, Rei, Toyoda, Atsushi, Itoh, Takehiko, Kubota, Souichirou, Goto, Yuji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10461843/
https://www.ncbi.nlm.nih.gov/pubmed/37639389
http://dx.doi.org/10.1371/journal.pone.0286941
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author Nagao, Kohei
Tanaka, Yoshiki
Kajitani, Rei
Toyoda, Atsushi
Itoh, Takehiko
Kubota, Souichirou
Goto, Yuji
author_facet Nagao, Kohei
Tanaka, Yoshiki
Kajitani, Rei
Toyoda, Atsushi
Itoh, Takehiko
Kubota, Souichirou
Goto, Yuji
author_sort Nagao, Kohei
collection PubMed
description In the Japanese hagfish, Eptatretus burgeri, approximately 21% of the genomic DNA in germ cells (2n = 52) consists of 16 chromosomes (eliminated [E]-chromosomes) that are eliminated from presumptive somatic cells (2n = 36). To uncover the eliminated genome (E-genome), we have identified 16 eliminated repetitive DNA families from eight hagfish species, with 11 of these repeats being selectively amplified in the germline genome of E. burgeri. Furthermore, we have demonstrated that six of these sequences, namely EEEb1–6, are exclusively localized on all 16 E-chromosomes. This has led to the hypothesis that the eight pairs of E-chromosomes are derived from one pair of ancestral chromosomes via multiple duplication events over a prolonged evolutionary period. NGS analysis has recently facilitated the re-assembly of two distinct draft genomes of E. burgeri, derived from the testis and liver. This advancement allows for the prediction of not only nonrepetitive eliminated sequences but also over 100 repetitive and eliminated sequences, accomplished through K-mer-based analysis. In this study, we report four novel eliminated repetitive DNA sequences (designated as EEEb7–10) and confirm the relative chromosomal localization of all eliminated repeats (EEEb1–10) by fluorescence in situ hybridization (FISH). With the exception of EEEb10, all sequences were exclusively detected on EEEb1-positive chromosomes. Surprisingly, EEEb10 was detected as an intense signal on EEEb1-positive chromosomes and as a scattered signal on other chromosomes in germ cells. The study further divided the eight pairs of E-chromosomes into six groups based on the signal distribution of each DNA family, and fiber-FISH experiments showed that the EEEb2–10 family was dispersed in the EEEb1-positive extended chromatin fiber. These findings provide new insights into the mechanisms underlying chromosome elimination and the evolution of E-chromosomes, supporting our previous hypothesis.
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spelling pubmed-104618432023-08-29 Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families Nagao, Kohei Tanaka, Yoshiki Kajitani, Rei Toyoda, Atsushi Itoh, Takehiko Kubota, Souichirou Goto, Yuji PLoS One Research Article In the Japanese hagfish, Eptatretus burgeri, approximately 21% of the genomic DNA in germ cells (2n = 52) consists of 16 chromosomes (eliminated [E]-chromosomes) that are eliminated from presumptive somatic cells (2n = 36). To uncover the eliminated genome (E-genome), we have identified 16 eliminated repetitive DNA families from eight hagfish species, with 11 of these repeats being selectively amplified in the germline genome of E. burgeri. Furthermore, we have demonstrated that six of these sequences, namely EEEb1–6, are exclusively localized on all 16 E-chromosomes. This has led to the hypothesis that the eight pairs of E-chromosomes are derived from one pair of ancestral chromosomes via multiple duplication events over a prolonged evolutionary period. NGS analysis has recently facilitated the re-assembly of two distinct draft genomes of E. burgeri, derived from the testis and liver. This advancement allows for the prediction of not only nonrepetitive eliminated sequences but also over 100 repetitive and eliminated sequences, accomplished through K-mer-based analysis. In this study, we report four novel eliminated repetitive DNA sequences (designated as EEEb7–10) and confirm the relative chromosomal localization of all eliminated repeats (EEEb1–10) by fluorescence in situ hybridization (FISH). With the exception of EEEb10, all sequences were exclusively detected on EEEb1-positive chromosomes. Surprisingly, EEEb10 was detected as an intense signal on EEEb1-positive chromosomes and as a scattered signal on other chromosomes in germ cells. The study further divided the eight pairs of E-chromosomes into six groups based on the signal distribution of each DNA family, and fiber-FISH experiments showed that the EEEb2–10 family was dispersed in the EEEb1-positive extended chromatin fiber. These findings provide new insights into the mechanisms underlying chromosome elimination and the evolution of E-chromosomes, supporting our previous hypothesis. Public Library of Science 2023-08-28 /pmc/articles/PMC10461843/ /pubmed/37639389 http://dx.doi.org/10.1371/journal.pone.0286941 Text en © 2023 Nagao et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Nagao, Kohei
Tanaka, Yoshiki
Kajitani, Rei
Toyoda, Atsushi
Itoh, Takehiko
Kubota, Souichirou
Goto, Yuji
Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families
title Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families
title_full Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families
title_fullStr Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families
title_full_unstemmed Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families
title_short Bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the Japanese hagfish, Eptatretus burgeri, through analysis of repetitive DNA families
title_sort bioinformatic and fine-scale chromosomal mapping reveal the nature and evolution of eliminated chromosomes in the japanese hagfish, eptatretus burgeri, through analysis of repetitive dna families
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10461843/
https://www.ncbi.nlm.nih.gov/pubmed/37639389
http://dx.doi.org/10.1371/journal.pone.0286941
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