Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway

Melissa K. Holborn; Anthony L. Einfeldt; Tony Kess; Steve J. Duffy; Amber M. Messmer; Barbara L. Langille; Matthew K. Brachmann; Johanne Gauthier; Paul Bentzen; Tim Martin Knutsen; Matthew Kent; Danny Boyce; Ian R Bradbury

doi:10.1111/1755-0998.13565

Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway

Melissa K. Holborn, Anthony L. Einfeldt, Tony Kess, Steve J. Duffy, Amber M. Messmer, Barbara L. Langille, Matthew K. Brachmann, Johanne Gauthier, Paul Bentzen, Tim Martin Knutsen, Matthew Kent, Danny Boyce, Ian R Bradbury

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19 Citas (Scopus)

Resumen

Teleosts exhibit extensive diversity of sex determination (SD) systems and mechanisms, providing the opportunity to study the evolution of SD and sex chromosomes. Here we sequenced the genome of the common lumpfish (Cyclopterus lumpus Linnaeus), a species of increasing importance to aquaculture, and identified the SD region and master SD locus using a 70 K single nucleotide polymorphism array and tissue-specific expression data. The chromosome-level assembly identified 25 diploid chromosomes with a total size of 572.89 Mb, a scaffold N50 of 23.86 Mb and genome annotation-predicted 21,480 protein-coding genes. Genome-wide association analysis located a highly sex-associated region on chromosome 13, suggesting that anti-Müllerian hormone (AMH) is the putative SD factor. Linkage disequilibrium and heterozygosity across chromosome 13 support a proto-XX/XY system, with an absence of widespread chromosome divergence between sexes. We identified three copies of AMH in the lumpfish primary and alternate haplotype assemblies localized in the SD region. Comparison to sequences from other teleosts suggested a monophyletic relationship and conservation within the Cottioidei. One AMH copy showed similarity to AMH/AMHY in a related species and was also the only copy with expression in testis tissue, suggesting this copy may be the functional copy of AMH in lumpfish. The two other copies arranged in tandem inverted duplication were highly similar, suggesting a recent duplication event. This study provides a resource for the study of early sex chromosome evolution and novel genomic resources that benefits lumpfish conservation management and aquaculture.

Idioma original	English
Páginas (desde-hasta)	1427-1439
Número de páginas	13
Publicación	Molecular Ecology Resources
Volumen	22
N.º	4
DOI	https://doi.org/10.1111/1755-0998.13565
Estado	Published - may. 2022

Nota bibliográfica

Funding Information:
We thank Olivier Fedrigo for coordination of DNA extraction and sequencing for the genome assembly at VGP Rockefeller. Genome curation and gEVAL was facilitated by Wellcome Sanger Institute. We also thank the Department of Ocean Sciences Centre/Dr Joe Brown Aquatic Research Building staff members Jessica Fry, Jennifer Monk, Kelsie Jeannot and Denise Tucker for expert technical assistance. Thanks are extended to the Canadian Coast Guard crews and to the scientists who participated in the ecosystem research surveys in the northern Gulf of St. Lawrence allowing the collection of lumpfish samples. SNP genotyping was provided by staff at the Centre for Integrative Genetics (CIGENE). Funding and support for this project was provided by Fisheries and Oceans Canada funding programmes; the Aquaculture Collaborative Research and Development Program in partnership with Newfoundland Aquaculture Industry Association (NAIA), Grieg NL Seafarms Ltd, Cooke Aquaculture Inc., and Mowi Canada East, and the Program for Aquaculture Regulatory Research.

Funding Information:
We thank Olivier Fedrigo for coordination of DNA extraction and sequencing for the genome assembly at VGP Rockefeller. Genome curation and gEVAL was facilitated by Wellcome Sanger Institute. We also thank the Department of Ocean Sciences Centre/Dr Joe Brown Aquatic Research Building staff members Jessica Fry, Jennifer Monk, Kelsie Jeannot and Denise Tucker for expert technical assistance. Thanks are extended to the Canadian Coast Guard crews and to the scientists who participated in the ecosystem research surveys in the northern Gulf of St. Lawrence allowing the collection of lumpfish samples. SNP genotyping was provided by staff at the Centre for Integrative Genetics (CIGENE). Funding and support for this project was provided by Fisheries and Oceans Canada funding programmes; the Aquaculture Collaborative Research and Development Program in partnership with Newfoundland Aquaculture Industry Association (NAIA), Grieg NL Seafarms Ltd, Cooke Aquaculture Inc., and Mowi Canada East, and the Program for Aquaculture Regulatory Research.

Publisher Copyright:
wileyonlinelibrary.com/journal/men.

ASJC Scopus Subject Areas

Biotechnology
Ecology, Evolution, Behavior and Systematics
Genetics

PubMed: MeSH publication types

Journal Article

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10.1111/1755-0998.13565

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Holborn, M. K., Einfeldt, A. L., Kess, T., Duffy, S. J., Messmer, A. M., Langille, B. L., Brachmann, M. K., Gauthier, J., Bentzen, P., Knutsen, T. M., Kent, M., Boyce, D., & Bradbury, IR. (2022). Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway. Molecular Ecology Resources, 22(4), 1427-1439. https://doi.org/10.1111/1755-0998.13565

Holborn, MK, Einfeldt, AL, Kess, T, Duffy, SJ, Messmer, AM, Langille, BL, Brachmann, MK, Gauthier, J, Bentzen, P, Knutsen, TM, Kent, M, Boyce, D & Bradbury, IR 2022, 'Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway', Molecular Ecology Resources, vol. 22, n.º 4, pp. 1427-1439. https://doi.org/10.1111/1755-0998.13565

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title = "Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway",

abstract = "Teleosts exhibit extensive diversity of sex determination (SD) systems and mechanisms, providing the opportunity to study the evolution of SD and sex chromosomes. Here we sequenced the genome of the common lumpfish (Cyclopterus lumpus Linnaeus), a species of increasing importance to aquaculture, and identified the SD region and master SD locus using a 70 K single nucleotide polymorphism array and tissue-specific expression data. The chromosome-level assembly identified 25 diploid chromosomes with a total size of 572.89 Mb, a scaffold N50 of 23.86 Mb and genome annotation-predicted 21,480 protein-coding genes. Genome-wide association analysis located a highly sex-associated region on chromosome 13, suggesting that anti-M{\"u}llerian hormone (AMH) is the putative SD factor. Linkage disequilibrium and heterozygosity across chromosome 13 support a proto-XX/XY system, with an absence of widespread chromosome divergence between sexes. We identified three copies of AMH in the lumpfish primary and alternate haplotype assemblies localized in the SD region. Comparison to sequences from other teleosts suggested a monophyletic relationship and conservation within the Cottioidei. One AMH copy showed similarity to AMH/AMHY in a related species and was also the only copy with expression in testis tissue, suggesting this copy may be the functional copy of AMH in lumpfish. The two other copies arranged in tandem inverted duplication were highly similar, suggesting a recent duplication event. This study provides a resource for the study of early sex chromosome evolution and novel genomic resources that benefits lumpfish conservation management and aquaculture.",

author = "Holborn, {Melissa K.} and Einfeldt, {Anthony L.} and Tony Kess and Duffy, {Steve J.} and Messmer, {Amber M.} and Langille, {Barbara L.} and Brachmann, {Matthew K.} and Johanne Gauthier and Paul Bentzen and Knutsen, {Tim Martin} and Matthew Kent and Danny Boyce and Ian R Bradbury",

note = "Funding Information: We thank Olivier Fedrigo for coordination of DNA extraction and sequencing for the genome assembly at VGP Rockefeller. Genome curation and gEVAL was facilitated by Wellcome Sanger Institute. We also thank the Department of Ocean Sciences Centre/Dr Joe Brown Aquatic Research Building staff members Jessica Fry, Jennifer Monk, Kelsie Jeannot and Denise Tucker for expert technical assistance. Thanks are extended to the Canadian Coast Guard crews and to the scientists who participated in the ecosystem research surveys in the northern Gulf of St. Lawrence allowing the collection of lumpfish samples. SNP genotyping was provided by staff at the Centre for Integrative Genetics (CIGENE). Funding and support for this project was provided by Fisheries and Oceans Canada funding programmes; the Aquaculture Collaborative Research and Development Program in partnership with Newfoundland Aquaculture Industry Association (NAIA), Grieg NL Seafarms Ltd, Cooke Aquaculture Inc., and Mowi Canada East, and the Program for Aquaculture Regulatory Research. Funding Information: We thank Olivier Fedrigo for coordination of DNA extraction and sequencing for the genome assembly at VGP Rockefeller. Genome curation and gEVAL was facilitated by Wellcome Sanger Institute. We also thank the Department of Ocean Sciences Centre/Dr Joe Brown Aquatic Research Building staff members Jessica Fry, Jennifer Monk, Kelsie Jeannot and Denise Tucker for expert technical assistance. Thanks are extended to the Canadian Coast Guard crews and to the scientists who participated in the ecosystem research surveys in the northern Gulf of St. Lawrence allowing the collection of lumpfish samples. SNP genotyping was provided by staff at the Centre for Integrative Genetics (CIGENE). Funding and support for this project was provided by Fisheries and Oceans Canada funding programmes; the Aquaculture Collaborative Research and Development Program in partnership with Newfoundland Aquaculture Industry Association (NAIA), Grieg NL Seafarms Ltd, Cooke Aquaculture Inc., and Mowi Canada East, and the Program for Aquaculture Regulatory Research. Publisher Copyright: wileyonlinelibrary.com/journal/men.",

year = "2022",

month = may,

doi = "10.1111/1755-0998.13565",

language = "English",

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T1 - Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway

AU - Holborn, Melissa K.

AU - Einfeldt, Anthony L.

AU - Kess, Tony

AU - Duffy, Steve J.

AU - Messmer, Amber M.

AU - Langille, Barbara L.

AU - Brachmann, Matthew K.

AU - Gauthier, Johanne

AU - Bentzen, Paul

AU - Knutsen, Tim Martin

AU - Kent, Matthew

AU - Boyce, Danny

AU - Bradbury, Ian R

N1 - Funding Information: We thank Olivier Fedrigo for coordination of DNA extraction and sequencing for the genome assembly at VGP Rockefeller. Genome curation and gEVAL was facilitated by Wellcome Sanger Institute. We also thank the Department of Ocean Sciences Centre/Dr Joe Brown Aquatic Research Building staff members Jessica Fry, Jennifer Monk, Kelsie Jeannot and Denise Tucker for expert technical assistance. Thanks are extended to the Canadian Coast Guard crews and to the scientists who participated in the ecosystem research surveys in the northern Gulf of St. Lawrence allowing the collection of lumpfish samples. SNP genotyping was provided by staff at the Centre for Integrative Genetics (CIGENE). Funding and support for this project was provided by Fisheries and Oceans Canada funding programmes; the Aquaculture Collaborative Research and Development Program in partnership with Newfoundland Aquaculture Industry Association (NAIA), Grieg NL Seafarms Ltd, Cooke Aquaculture Inc., and Mowi Canada East, and the Program for Aquaculture Regulatory Research. Funding Information: We thank Olivier Fedrigo for coordination of DNA extraction and sequencing for the genome assembly at VGP Rockefeller. Genome curation and gEVAL was facilitated by Wellcome Sanger Institute. We also thank the Department of Ocean Sciences Centre/Dr Joe Brown Aquatic Research Building staff members Jessica Fry, Jennifer Monk, Kelsie Jeannot and Denise Tucker for expert technical assistance. Thanks are extended to the Canadian Coast Guard crews and to the scientists who participated in the ecosystem research surveys in the northern Gulf of St. Lawrence allowing the collection of lumpfish samples. SNP genotyping was provided by staff at the Centre for Integrative Genetics (CIGENE). Funding and support for this project was provided by Fisheries and Oceans Canada funding programmes; the Aquaculture Collaborative Research and Development Program in partnership with Newfoundland Aquaculture Industry Association (NAIA), Grieg NL Seafarms Ltd, Cooke Aquaculture Inc., and Mowi Canada East, and the Program for Aquaculture Regulatory Research. Publisher Copyright: wileyonlinelibrary.com/journal/men.

PY - 2022/5

Y1 - 2022/5

N2 - Teleosts exhibit extensive diversity of sex determination (SD) systems and mechanisms, providing the opportunity to study the evolution of SD and sex chromosomes. Here we sequenced the genome of the common lumpfish (Cyclopterus lumpus Linnaeus), a species of increasing importance to aquaculture, and identified the SD region and master SD locus using a 70 K single nucleotide polymorphism array and tissue-specific expression data. The chromosome-level assembly identified 25 diploid chromosomes with a total size of 572.89 Mb, a scaffold N50 of 23.86 Mb and genome annotation-predicted 21,480 protein-coding genes. Genome-wide association analysis located a highly sex-associated region on chromosome 13, suggesting that anti-Müllerian hormone (AMH) is the putative SD factor. Linkage disequilibrium and heterozygosity across chromosome 13 support a proto-XX/XY system, with an absence of widespread chromosome divergence between sexes. We identified three copies of AMH in the lumpfish primary and alternate haplotype assemblies localized in the SD region. Comparison to sequences from other teleosts suggested a monophyletic relationship and conservation within the Cottioidei. One AMH copy showed similarity to AMH/AMHY in a related species and was also the only copy with expression in testis tissue, suggesting this copy may be the functional copy of AMH in lumpfish. The two other copies arranged in tandem inverted duplication were highly similar, suggesting a recent duplication event. This study provides a resource for the study of early sex chromosome evolution and novel genomic resources that benefits lumpfish conservation management and aquaculture.

AB - Teleosts exhibit extensive diversity of sex determination (SD) systems and mechanisms, providing the opportunity to study the evolution of SD and sex chromosomes. Here we sequenced the genome of the common lumpfish (Cyclopterus lumpus Linnaeus), a species of increasing importance to aquaculture, and identified the SD region and master SD locus using a 70 K single nucleotide polymorphism array and tissue-specific expression data. The chromosome-level assembly identified 25 diploid chromosomes with a total size of 572.89 Mb, a scaffold N50 of 23.86 Mb and genome annotation-predicted 21,480 protein-coding genes. Genome-wide association analysis located a highly sex-associated region on chromosome 13, suggesting that anti-Müllerian hormone (AMH) is the putative SD factor. Linkage disequilibrium and heterozygosity across chromosome 13 support a proto-XX/XY system, with an absence of widespread chromosome divergence between sexes. We identified three copies of AMH in the lumpfish primary and alternate haplotype assemblies localized in the SD region. Comparison to sequences from other teleosts suggested a monophyletic relationship and conservation within the Cottioidei. One AMH copy showed similarity to AMH/AMHY in a related species and was also the only copy with expression in testis tissue, suggesting this copy may be the functional copy of AMH in lumpfish. The two other copies arranged in tandem inverted duplication were highly similar, suggesting a recent duplication event. This study provides a resource for the study of early sex chromosome evolution and novel genomic resources that benefits lumpfish conservation management and aquaculture.

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Reference genome of lumpfish Cyclopterus lumpus Linnaeus provides evidence of male heterogametic sex determination through the AMH pathway

Resumen

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ASJC Scopus Subject Areas

PubMed: MeSH publication types

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