The Y chromosome sequence of the channel catfish suggests novel sex determination mechanisms in teleost fish

Lisui Bao, Changxu Tian, Shikai Liu, Yu Zhang, Ahmed Elaswad, Zihao Yuan, Karim Khalil, Fanyue Sun, Yujia Yang, Tao Zhou, Ning Li, Suxu Tan, Qifan Zeng, Yang Liu, Yueru Li, Yun Li, Dongya Gao, Rex Dunham, Kenneth Davis, Geoffrey WaldbieserZhanjian "John" Liu

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Background: Sex determination mechanisms in teleost fish broadly differ from mammals and birds, with sex chromosomes that are far less differentiated and recombination often occurring along the length of the X and Y chromosomes, posing major challenges for the identification of specific sex determination genes. Here, we take an innovative approach of comparative genome analysis of the genomic sequences of the X chromosome and newly sequenced Y chromosome in the channel catfish. Results: Using a YY channel catfish as the sequencing template, we generated, assembled, and annotated the Y genome sequence of channel catfish. The genome sequence assembly had a contig N50 size of 2.7 Mb and a scaffold N50 size of 26.7 Mb. Genetic linkage and GWAS analyses placed the sex determination locus within a genetic distance less than 0.5 cM and physical distance of 8.9 Mb. However, comparison of the channel catfish X and Y chromosome sequences showed no sex-specific genes. Instead, comparative RNA-Seq analysis between females and males revealed exclusive sex-specific expression of an isoform of the breast cancer anti-resistance 1 (BCAR1) gene in the male during early sex differentiation. Experimental knockout of BCAR1 gene converted genetic males (XY) to phenotypic females, suggesting BCAR1 as a putative sex determination gene. Conclusions: We present the first Y chromosome sequence among teleost fish, and one of the few whole Y chromosome sequences among vertebrate species. Comparative analyses suggest that sex-specific isoform expression through alternative splicing may underlie sex determination processes in the channel catfish, and we identify BCAR1 as a potential sex determination gene.

Original languageEnglish (US)
Article number6
JournalBMC Biology
Volume17
Issue number1
DOIs
StatePublished - Jan 25 2019

Fingerprint

Ictaluridae
sex determination
Y Chromosome
Ictalurus punctatus
Y chromosome
Chromosomes
teleost
Fish
chromosome
Fishes
Genes
gender
fish
gene
cancer
breast neoplasms
X Chromosome
X chromosome
Breast Neoplasms
genome

Keywords

  • Catfish
  • PacBio
  • RNA-Seq
  • Sex determination
  • Y chromosome

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

Cite this

The Y chromosome sequence of the channel catfish suggests novel sex determination mechanisms in teleost fish. / Bao, Lisui; Tian, Changxu; Liu, Shikai; Zhang, Yu; Elaswad, Ahmed; Yuan, Zihao; Khalil, Karim; Sun, Fanyue; Yang, Yujia; Zhou, Tao; Li, Ning; Tan, Suxu; Zeng, Qifan; Liu, Yang; Li, Yueru; Li, Yun; Gao, Dongya; Dunham, Rex; Davis, Kenneth; Waldbieser, Geoffrey; Liu, Zhanjian "John".

In: BMC Biology, Vol. 17, No. 1, 6, 25.01.2019.

Research output: Contribution to journalArticle

Bao, L, Tian, C, Liu, S, Zhang, Y, Elaswad, A, Yuan, Z, Khalil, K, Sun, F, Yang, Y, Zhou, T, Li, N, Tan, S, Zeng, Q, Liu, Y, Li, Y, Li, Y, Gao, D, Dunham, R, Davis, K, Waldbieser, G & Liu, ZJ 2019, 'The Y chromosome sequence of the channel catfish suggests novel sex determination mechanisms in teleost fish', BMC Biology, vol. 17, no. 1, 6. https://doi.org/10.1186/s12915-019-0627-7
Bao, Lisui ; Tian, Changxu ; Liu, Shikai ; Zhang, Yu ; Elaswad, Ahmed ; Yuan, Zihao ; Khalil, Karim ; Sun, Fanyue ; Yang, Yujia ; Zhou, Tao ; Li, Ning ; Tan, Suxu ; Zeng, Qifan ; Liu, Yang ; Li, Yueru ; Li, Yun ; Gao, Dongya ; Dunham, Rex ; Davis, Kenneth ; Waldbieser, Geoffrey ; Liu, Zhanjian "John". / The Y chromosome sequence of the channel catfish suggests novel sex determination mechanisms in teleost fish. In: BMC Biology. 2019 ; Vol. 17, No. 1.
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abstract = "Background: Sex determination mechanisms in teleost fish broadly differ from mammals and birds, with sex chromosomes that are far less differentiated and recombination often occurring along the length of the X and Y chromosomes, posing major challenges for the identification of specific sex determination genes. Here, we take an innovative approach of comparative genome analysis of the genomic sequences of the X chromosome and newly sequenced Y chromosome in the channel catfish. Results: Using a YY channel catfish as the sequencing template, we generated, assembled, and annotated the Y genome sequence of channel catfish. The genome sequence assembly had a contig N50 size of 2.7 Mb and a scaffold N50 size of 26.7 Mb. Genetic linkage and GWAS analyses placed the sex determination locus within a genetic distance less than 0.5 cM and physical distance of 8.9 Mb. However, comparison of the channel catfish X and Y chromosome sequences showed no sex-specific genes. Instead, comparative RNA-Seq analysis between females and males revealed exclusive sex-specific expression of an isoform of the breast cancer anti-resistance 1 (BCAR1) gene in the male during early sex differentiation. Experimental knockout of BCAR1 gene converted genetic males (XY) to phenotypic females, suggesting BCAR1 as a putative sex determination gene. Conclusions: We present the first Y chromosome sequence among teleost fish, and one of the few whole Y chromosome sequences among vertebrate species. Comparative analyses suggest that sex-specific isoform expression through alternative splicing may underlie sex determination processes in the channel catfish, and we identify BCAR1 as a potential sex determination gene.",
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AU - Bao, Lisui

AU - Tian, Changxu

AU - Liu, Shikai

AU - Zhang, Yu

AU - Elaswad, Ahmed

AU - Yuan, Zihao

AU - Khalil, Karim

AU - Sun, Fanyue

AU - Yang, Yujia

AU - Zhou, Tao

AU - Li, Ning

AU - Tan, Suxu

AU - Zeng, Qifan

AU - Liu, Yang

AU - Li, Yueru

AU - Li, Yun

AU - Gao, Dongya

AU - Dunham, Rex

AU - Davis, Kenneth

AU - Waldbieser, Geoffrey

AU - Liu, Zhanjian "John"

PY - 2019/1/25

Y1 - 2019/1/25

N2 - Background: Sex determination mechanisms in teleost fish broadly differ from mammals and birds, with sex chromosomes that are far less differentiated and recombination often occurring along the length of the X and Y chromosomes, posing major challenges for the identification of specific sex determination genes. Here, we take an innovative approach of comparative genome analysis of the genomic sequences of the X chromosome and newly sequenced Y chromosome in the channel catfish. Results: Using a YY channel catfish as the sequencing template, we generated, assembled, and annotated the Y genome sequence of channel catfish. The genome sequence assembly had a contig N50 size of 2.7 Mb and a scaffold N50 size of 26.7 Mb. Genetic linkage and GWAS analyses placed the sex determination locus within a genetic distance less than 0.5 cM and physical distance of 8.9 Mb. However, comparison of the channel catfish X and Y chromosome sequences showed no sex-specific genes. Instead, comparative RNA-Seq analysis between females and males revealed exclusive sex-specific expression of an isoform of the breast cancer anti-resistance 1 (BCAR1) gene in the male during early sex differentiation. Experimental knockout of BCAR1 gene converted genetic males (XY) to phenotypic females, suggesting BCAR1 as a putative sex determination gene. Conclusions: We present the first Y chromosome sequence among teleost fish, and one of the few whole Y chromosome sequences among vertebrate species. Comparative analyses suggest that sex-specific isoform expression through alternative splicing may underlie sex determination processes in the channel catfish, and we identify BCAR1 as a potential sex determination gene.

AB - Background: Sex determination mechanisms in teleost fish broadly differ from mammals and birds, with sex chromosomes that are far less differentiated and recombination often occurring along the length of the X and Y chromosomes, posing major challenges for the identification of specific sex determination genes. Here, we take an innovative approach of comparative genome analysis of the genomic sequences of the X chromosome and newly sequenced Y chromosome in the channel catfish. Results: Using a YY channel catfish as the sequencing template, we generated, assembled, and annotated the Y genome sequence of channel catfish. The genome sequence assembly had a contig N50 size of 2.7 Mb and a scaffold N50 size of 26.7 Mb. Genetic linkage and GWAS analyses placed the sex determination locus within a genetic distance less than 0.5 cM and physical distance of 8.9 Mb. However, comparison of the channel catfish X and Y chromosome sequences showed no sex-specific genes. Instead, comparative RNA-Seq analysis between females and males revealed exclusive sex-specific expression of an isoform of the breast cancer anti-resistance 1 (BCAR1) gene in the male during early sex differentiation. Experimental knockout of BCAR1 gene converted genetic males (XY) to phenotypic females, suggesting BCAR1 as a putative sex determination gene. Conclusions: We present the first Y chromosome sequence among teleost fish, and one of the few whole Y chromosome sequences among vertebrate species. Comparative analyses suggest that sex-specific isoform expression through alternative splicing may underlie sex determination processes in the channel catfish, and we identify BCAR1 as a potential sex determination gene.

KW - Catfish

KW - PacBio

KW - RNA-Seq

KW - Sex determination

KW - Y chromosome

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