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Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing

BACKGROUND: The larvacean Oikopleura dioica is an abundant tunicate plankton with the smallest (65–70 Mbp) non-parasitic, non-extremophile animal genome identified to date. Currently, there are two genomes available for the Bergen (OdB3) and Osaka (OSKA2016) O. dioica laboratory strains. Both assemb...

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Autores principales: Bliznina, Aleksandra, Masunaga, Aki, Mansfield, Michael J., Tan, Yongkai, Liu, Andrew W., West, Charlotte, Rustagi, Tanmay, Chien, Hsiao-Chiao, Kumar, Saurabh, Pichon, Julien, Plessy, Charles, Luscombe, Nicholas M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8008620/
https://www.ncbi.nlm.nih.gov/pubmed/33781200
http://dx.doi.org/10.1186/s12864-021-07512-6
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author Bliznina, Aleksandra
Masunaga, Aki
Mansfield, Michael J.
Tan, Yongkai
Liu, Andrew W.
West, Charlotte
Rustagi, Tanmay
Chien, Hsiao-Chiao
Kumar, Saurabh
Pichon, Julien
Plessy, Charles
Luscombe, Nicholas M.
author_facet Bliznina, Aleksandra
Masunaga, Aki
Mansfield, Michael J.
Tan, Yongkai
Liu, Andrew W.
West, Charlotte
Rustagi, Tanmay
Chien, Hsiao-Chiao
Kumar, Saurabh
Pichon, Julien
Plessy, Charles
Luscombe, Nicholas M.
author_sort Bliznina, Aleksandra
collection PubMed
description BACKGROUND: The larvacean Oikopleura dioica is an abundant tunicate plankton with the smallest (65–70 Mbp) non-parasitic, non-extremophile animal genome identified to date. Currently, there are two genomes available for the Bergen (OdB3) and Osaka (OSKA2016) O. dioica laboratory strains. Both assemblies have full genome coverage and high sequence accuracy. However, a chromosome-scale assembly has not yet been achieved. RESULTS: Here, we present a chromosome-scale genome assembly (OKI2018_I69) of the Okinawan O. dioica produced using long-read Nanopore and short-read Illumina sequencing data from a single male, combined with Hi-C chromosomal conformation capture data for scaffolding. The OKI2018_I69 assembly has a total length of 64.3 Mbp distributed among 19 scaffolds. 99% of the assembly is contained within five megabase-scale scaffolds. We found telomeres on both ends of the two largest scaffolds, which represent assemblies of two fully contiguous autosomal chromosomes. Each of the other three large scaffolds have telomeres at one end only and we propose that they correspond to sex chromosomes split into a pseudo-autosomal region and X-specific or Y-specific regions. Indeed, these five scaffolds mostly correspond to equivalent linkage groups in OdB3, suggesting overall agreement in chromosomal organization between the two populations. At a more detailed level, the OKI2018_I69 assembly possesses similar genomic features in gene content and repetitive elements reported for OdB3. The Hi-C map suggests few reciprocal interactions between chromosome arms. At the sequence level, multiple genomic features such as GC content and repetitive elements are distributed differently along the short and long arms of the same chromosome. CONCLUSIONS: We show that a hybrid approach of integrating multiple sequencing technologies with chromosome conformation information results in an accurate de novo chromosome-scale assembly of O. dioica’s highly polymorphic genome. This genome assembly opens up the possibility of cross-genome comparison between O. dioica populations, as well as of studies of chromosomal evolution in this lineage. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07512-6.
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spelling pubmed-80086202021-03-31 Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing Bliznina, Aleksandra Masunaga, Aki Mansfield, Michael J. Tan, Yongkai Liu, Andrew W. West, Charlotte Rustagi, Tanmay Chien, Hsiao-Chiao Kumar, Saurabh Pichon, Julien Plessy, Charles Luscombe, Nicholas M. BMC Genomics Research Article BACKGROUND: The larvacean Oikopleura dioica is an abundant tunicate plankton with the smallest (65–70 Mbp) non-parasitic, non-extremophile animal genome identified to date. Currently, there are two genomes available for the Bergen (OdB3) and Osaka (OSKA2016) O. dioica laboratory strains. Both assemblies have full genome coverage and high sequence accuracy. However, a chromosome-scale assembly has not yet been achieved. RESULTS: Here, we present a chromosome-scale genome assembly (OKI2018_I69) of the Okinawan O. dioica produced using long-read Nanopore and short-read Illumina sequencing data from a single male, combined with Hi-C chromosomal conformation capture data for scaffolding. The OKI2018_I69 assembly has a total length of 64.3 Mbp distributed among 19 scaffolds. 99% of the assembly is contained within five megabase-scale scaffolds. We found telomeres on both ends of the two largest scaffolds, which represent assemblies of two fully contiguous autosomal chromosomes. Each of the other three large scaffolds have telomeres at one end only and we propose that they correspond to sex chromosomes split into a pseudo-autosomal region and X-specific or Y-specific regions. Indeed, these five scaffolds mostly correspond to equivalent linkage groups in OdB3, suggesting overall agreement in chromosomal organization between the two populations. At a more detailed level, the OKI2018_I69 assembly possesses similar genomic features in gene content and repetitive elements reported for OdB3. The Hi-C map suggests few reciprocal interactions between chromosome arms. At the sequence level, multiple genomic features such as GC content and repetitive elements are distributed differently along the short and long arms of the same chromosome. CONCLUSIONS: We show that a hybrid approach of integrating multiple sequencing technologies with chromosome conformation information results in an accurate de novo chromosome-scale assembly of O. dioica’s highly polymorphic genome. This genome assembly opens up the possibility of cross-genome comparison between O. dioica populations, as well as of studies of chromosomal evolution in this lineage. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-021-07512-6. BioMed Central 2021-03-29 /pmc/articles/PMC8008620/ /pubmed/33781200 http://dx.doi.org/10.1186/s12864-021-07512-6 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Bliznina, Aleksandra
Masunaga, Aki
Mansfield, Michael J.
Tan, Yongkai
Liu, Andrew W.
West, Charlotte
Rustagi, Tanmay
Chien, Hsiao-Chiao
Kumar, Saurabh
Pichon, Julien
Plessy, Charles
Luscombe, Nicholas M.
Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing
title Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing
title_full Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing
title_fullStr Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing
title_full_unstemmed Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing
title_short Telomere-to-telomere assembly of the genome of an individual Oikopleura dioica from Okinawa using Nanopore-based sequencing
title_sort telomere-to-telomere assembly of the genome of an individual oikopleura dioica from okinawa using nanopore-based sequencing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8008620/
https://www.ncbi.nlm.nih.gov/pubmed/33781200
http://dx.doi.org/10.1186/s12864-021-07512-6
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