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A genome-wide association study, supported by a new chromosome-level genome assembly, suggests sox2 as a main driver of the undifferentiatiated ZZ/ZW sex determination of turbot (Scophthalmus maximus)

Authors: Martínez, P. (Paulino); Robledo, D. (Diego); Taboada, X. (Xoana); Blanco, A.; Moser, M.; Maroso, F.; Hermida, M.; +7 Authors

A genome-wide association study, supported by a new chromosome-level genome assembly, suggests sox2 as a main driver of the undifferentiatiated ZZ/ZW sex determination of turbot (Scophthalmus maximus)

Abstract

Background: Understanding sex determination (SD) across taxa is a major challenge for evolutionary biology. The new genomic tools are paving the way to identify genomic features underlying SD in fish, a group frequently showing limited sex chromosome differentiation and high SD evolutionary turnover. Turbot (Scophthalmus maximus) is a commercially important flatfish with an undifferentiated ZW/ZZ SD system and remarkable sexual dimorphism. Here we describe a new long-read turbot genome assembly used to disentangle the genetic architecture of turbot SD by combining genomics and classical genetics approaches. Results: The new turbot genome assembly consists of 145 contigs (N50 = 22.9 Mb), 27 of them representing >95% of its estimated genome size. A genome wide association study (GWAS) identified a ~ 6.8 Mb region on chromosome 12 associated with sex in 69.4% of the 36 families analyzed. The highest associated markers flanked sox2, the only gene in the region showing differential expression between sexes before gonad differentiation. A single SNP showed consistent differences between Z and W chromosomes. The analysis of a broad sample of families suggested the presence of additional genetic and/or environmental factors on turbot SD. Conclusions: The new chromosome-level turbot genome assembly, one of the most contiguous fish assemblies to date, facilitated the identification of sox2 as a consistent candidate gene putatively driving SD in this species. This chromosome SD system barely showed any signs of differentiation, and other factors beyond the main QTL seem to control SD in a certain proportion of families

14 pages, 7 figures, 2 tables, supplementary material https://doi.org/10.1016/j.ygeno.2021.04.007.-- Availability of data and materials: All dataset generated during this study are included (in this article and as supplementary information files) or are available in public repositories. Turbot Genome Sequencing data are at NCBI databases (Bioproject: PRJNA631898) (https://www.ncbi.nlm.nih.gov/genome/?term=turbot) and BioProject es PRJNA649485 (https://www.ncbi.nlm.nih.gov/bioproject/649485; Accessión numbers: SRX8843737, SRX8843739, SRX8843738)

This work was supported by the Spanish Ministry of Economy and Competitiveness, Grant: AGL2014-57065-R, by the European Union's Horizon 2020 Research and Innovation Programme under grant agreement No 81792 (AQUA-FAANG) and by Consellería de Educación, Universidade e Formación Profesional. Xunta de Galicia, Grant number: ED431C 2018/28

With funding from the Spanish government through the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)

Peer reviewed

Countries
Spain, United Kingdom, Norway
Subjects by Vocabulary

Microsoft Academic Graph classification: Candidate gene Genomics Genome-wide association study Biology Gene Genome size Chromosome 12 Genetics Chromosome biology.organism_classification Turbot

Keywords

Fish Proteins, Chromosomes, access, Genetic, Interfamily variation, Genetics, sex, GWAS, sox2, Animals, fish, Turbot aquaculture, Genome assembly, Genome, zoology, SOXB1 Transcription Factors, Chromosome Mapping, Turbot, Sex determination, Oxford Nanopore, Flatfishes, Genome-Wide Association Study

80 references, page 1 of 8

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[2] P. Martínez, A.M. Vin˜as, L. S´anchez, et al., Genetic architecture of sex determination in fish: applications to sex ratio control in aquaculture, Front. Genet. 5 (2014) 340.

[3] B. Capel, Vertebrate sex determination: evolutionary plasticity of a fundamental switch, Nat. Rev. Genet. 18 (2017) 675-689.

[4] M.B. Cioffi, C.F. Yano, A. Sember, L.A.C. Bertollo, Chromosomal evolution in lower vertebrates: sex chromosomes in neotropical fishes, Genes 8 (2017) 258.

[5] M. Matsuda, Y. Nagahama, A. Shinomiya, et al., DMY is a Y-specific DM-domain gene required for male development in the medaka fish, Nature 417 (2002) 559-563.

[6] Y. Takehana, M. Matsuda, T. Myosho, et al., Co-option of Sox3 as the maledetermining factor on the Y chromosome in the fish Oryzias dancena, Nat. Commun. 5 (2014) 4157.

[7] T. Myosho, H. Otake, H. Masuyama, et al., Tracing the emergence of a novel sexdetermining gene in medaka, Oryzias luzonensis, Genetics 191 (2012) 163-170.

[8] R.S. Hattori, Y. Murai, M. Oura, et al., A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination, Proc. Natl. Acad. Sci. U. S. A. 109 (2012) 2955.

[9] Q. Pan, R. Feron, A. Yano, et al., Identification of the master sex determining gene in northern pike (Esox lucius) reveals restricted sex chromosome differentiation, PLoS Genet. 15 (2019), e1008013.

[10] T. Kamiya, W. Kai, S. Tasumi, et al., A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu), PLoS Genet. 8 (2012), e1002798.

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    This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
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citations
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
views
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43
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Funded by
WT
Project
  • Funder: Wellcome Trust (WT)
,
EC| FISHBOOST
Project
FISHBOOST
Improving European aquaculture by advancing selective breeding to the next level for the six main finfish species
  • Funder: European Commission (EC)
  • Project Code: 613611
  • Funding stream: FP7 | SP1 | KBBE
iis
,
EC| AQUA-FAANG
Project
AQUA-FAANG
Advancing European Aquaculture by Genome Functional Annotation
  • Funder: European Commission (EC)
  • Project Code: 817923
  • Funding stream: H2020 | RIA
Validated by funder | sysimport:crosswalk
Related to Research communities
European Marine Science
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