The Origin, Evolution, and Translocation of Sex Chromosomes in Silurus Catfish Mediated by Transposons

Overview

Journal BMC Biol

Publisher Biomed Central

Specialty Biology

Date 2025 Feb 21

PMID 39984975

Authors

Shuqing Zheng

Hongyan Tao

Yuheng Song

Mao Li

Haowen Yang

Jianzhen Li

Hongwei Yan

Bakhtiyor Sheraliev

Wenjing Tao

Zuogang Peng

Yaoguang Zhang

Deshou Wang

Affiliations

Soon will be listed here.

Abstract

Background: Sex chromosome (SC) evolution is a longstanding topic of focus in evolutionary biology. Teleosts often exhibit rapid turnover of SCs and sex-determining (SD) genes, alongside a diverse range of SC differentiation mechanisms.

Results: On the basis of new chromosome-scale assemblies of three Silurus species (S. microdorsalis, S. glanis, and S. lanzhouensis) and two outgroup species (Pterocryptis cochinchinensis and Kryptopterus bicirrhis), along with our previous assemblies of S. meridionalis and S. asotus, we traced the evolution of SC in the Silurus genus (Siluriformes), following the fate of the known SD gene amhr2y. Phylogenetic analysis showed that amhr2y occurred at least before the divergence of Pterocryptis, Kryptopterus, and Silurus and lost in P. cochinchinensis and K. bicirrhis. Chr24 has become the SC in the ancestor of five Silurus species due to the duplication-and-translocation of amhr2 mediated by LTR transposon. Then, a proto Y was formed and maintained with a shared 60 kb male-specific region of the Y chromosome (MSY) by transposable elements (TEs) expansion and gene gathering. Due to the continuous TEs accumulation, genes other than amhr2y in MSYs have degenerated or been lost, while non-recombinant regions continue to expend, forming MSYs of different sizes in different Silurus species (from 320 to 550 kb). Two turnover events, one homologous (from the left arm to the right arm of Chr24) and one nonhomologous (from Chr24 to Chr5), occurring among five Silurus species were possibly mediated by hAT and Helitron transposons.

Conclusions: Our results on the dynamic evolutionary trajectory of SD gene amhr2y, MSYs, and SCs in Silurus catfish indicated the variability and diversity of fish SCs and confirmed that frequent turnover is an important way to maintain the homology and low differentiation of fish SCs.

References

Kopp A . Metamodels and phylogenetic replication: a systematic approach to the evolution of developmental pathways. Evolution. 2009; 63(11):2771-89. DOI: 10.1111/j.1558-5646.2009.00761.x. View

Montiel E, Badenhorst D, Tamplin J, Burke R, Valenzuela N . Discovery of the youngest sex chromosomes reveals first case of convergent co-option of ancestral autosomes in turtles. Chromosoma. 2016; 126(1):105-113. DOI: 10.1007/s00412-016-0576-7. View

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N . The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25(16):2078-9. PMC: 2723002. DOI: 10.1093/bioinformatics/btp352. View

Wicker T, Sabot F, Hua-Van A, Bennetzen J, Capy P, Chalhoub B . A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007; 8(12):973-82. DOI: 10.1038/nrg2165. View

Sharma A, Heinze S, Wu Y, Kohlbrenner T, Morilla I, Brunner C . Male sex in houseflies is determined by , a paralog of the generic splice factor gene . Science. 2017; 356(6338):642-645. DOI: 10.1126/science.aam5498. View

Tanaka K, Takehana Y, Naruse K, Hamaguchi S, Sakaizumi M . Evidence for different origins of sex chromosomes in closely related Oryzias fishes: substitution of the master sex-determining gene. Genetics. 2007; 177(4):2075-81. PMC: 2219477. DOI: 10.1534/genetics.107.075598. View

Franchini P, Jones J, Xiong P, Kneitz S, Gompert Z, Warren W . Long-term experimental hybridisation results in the evolution of a new sex chromosome in swordtail fish. Nat Commun. 2018; 9(1):5136. PMC: 6277394. DOI: 10.1038/s41467-018-07648-2. View

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25(14):1754-60. PMC: 2705234. DOI: 10.1093/bioinformatics/btp324. View

Ou S, Jiang N . LTR_retriever: A Highly Accurate and Sensitive Program for Identification of Long Terminal Repeat Retrotransposons. Plant Physiol. 2017; 176(2):1410-1422. PMC: 5813529. DOI: 10.1104/pp.17.01310. View

10.

Rondeau E, Laurie C, Johnson S, Koop B . A PCR assay detects a male-specific duplicated copy of Anti-Müllerian hormone (amh) in the lingcod (Ophiodon elongatus). BMC Res Notes. 2016; 9:230. PMC: 4840878. DOI: 10.1186/s13104-016-2030-6. View

11.

Kitano J, Ansai S, Takehana Y, Yamamoto Y . Diversity and Convergence of Sex-Determination Mechanisms in Teleost Fish. Annu Rev Anim Biosci. 2023; 12:233-259. DOI: 10.1146/annurev-animal-021122-113935. View

12.

Conte M, Gammerdinger W, Bartie K, Penman D, Kocher T . A high quality assembly of the Nile Tilapia (Oreochromis niloticus) genome reveals the structure of two sex determination regions. BMC Genomics. 2017; 18(1):341. PMC: 5414186. DOI: 10.1186/s12864-017-3723-5. View

13.

Schartl M, Schmid M, Nanda I . Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma. 2015; 125(3):553-71. DOI: 10.1007/s00412-015-0569-y. View

14.

Kondo M, Hornung U, Nanda I, Imai S, Sasaki T, Shimizu A . Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res. 2006; 16(7):815-26. PMC: 1484449. DOI: 10.1101/gr.5016106. View

15.

Bian C, Li R, Ruan Z, Chen W, Huang Y, Liu L . Chromosome-level genome assembly of the glass catfish ( ) reveals molecular clues to its transparent phenotype. Zool Res. 2024; 45(5):1027-1036. PMC: 11491783. DOI: 10.24272/j.issn.2095-8137.2023.396. View

16.

Tennessen J, Wei N, Straub S, Govindarajulu R, Liston A, Ashman T . Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries. PLoS Biol. 2018; 16(8):e2006062. PMC: 6128632. DOI: 10.1371/journal.pbio.2006062. View

17.

Kuhl H, Guiguen Y, Hohne C, Kreuz E, Du K, Klopp C . A 180 Myr-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes. Philos Trans R Soc Lond B Biol Sci. 2021; 376(1832):20200089. PMC: 8273502. DOI: 10.1098/rstb.2020.0089. View

18.

Bertho S, Herpin A, Schartl M, Guiguen Y . Lessons from an unusual vertebrate sex-determining gene. Philos Trans R Soc Lond B Biol Sci. 2021; 376(1832):20200092. PMC: 8273500. DOI: 10.1098/rstb.2020.0092. View

19.

Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T . DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature. 2002; 417(6888):559-63. DOI: 10.1038/nature751. View

20.

Marshall Graves J, Peichel C . Are homologies in vertebrate sex determination due to shared ancestry or to limited options?. Genome Biol. 2010; 11(4):205. PMC: 2884537. DOI: 10.1186/gb-2010-11-4-205. View