De Novo Assembly and Characterization of a Highly Degenerated ZW Sex Chromosome in the Fish Megaleporinus Macrocephalus

Overview

Journal Gigascience

Publisher Oxford University Press

Specialties Biology
Genetics

Date 2024 Nov 26

PMID 39589439

Authors

Carolina Heloisa Souza-Borges

Ricardo Utsunomia

Alessandro M Varani

Marcela Uliano-Silva

Lieschen Valeria G Lira

Arno J Butzge

John F Gomez Agudelo

Shisley Manso

Milena V Freitas

Raquel B Ariede

Vito A Mastrochirico-Filho

Carolina Penaloza

Agustin Barria

Fabio Porto-Foresti

Fausto Foresti

Ricardo Hattori

Yann Guiguen

Ross D Houston

Diogo Teruo Hashimoto

Affiliations

Soon will be listed here.

Abstract

Background: Megaleporinus macrocephalus (piauçu) is a Neotropical fish within Characoidei that presents a well-established heteromorphic ZZ/ZW sex determination system and thus constitutes a good model for studying W and Z chromosomes in fishes. We used PacBio reads and Hi-C to assemble a chromosome-level reference genome for M. macrocephalus. We generated family segregation information to construct a genetic map, pool sequencing of males and females to characterize its sex system, and RNA sequencing to highlight candidate genes of M. macrocephalus sex determination.

Results: The reference genome of M. macrocephalus is 1,282,030,339 bp in length and has a contig and scaffold N50 of 5.0 Mb and 45.03 Mb, respectively. In the sex chromosome, based on patterns of recombination suppression, coverage, FST, and sex-specific SNPs, we distinguished a putative W-specific region that is highly differentiated, a region where Z and W still share some similarities and is undergoing degeneration, and the PAR. The sex chromosome gene repertoire includes genes from the TGF-β family (amhr2, bmp7) and the Wnt/β-catenin pathway (wnt4, wnt7a), some of which are differentially expressed.

Conclusions: The chromosome-level genome of piauçu exhibits high quality, establishing a valuable resource for advancing research within the group. Our discoveries offer insights into the evolutionary dynamics of Z and W sex chromosomes in fish, emphasizing ongoing degenerative processes and indicating complex interactions between Z and W sequences in specific genomic regions. Notably, amhr2 and bmp7 are potential candidate genes for sex determination in M. macrocephalus.

References

Fowler R, Bonnewell V, Spann M, Skinner D . Sequences of three closely related variants of a complex satellite DNA diverge at specific domains. J Biol Chem. 1985; 260(15):8964-72. View

Venere P, Ferreira I, Martins C, Galetti Junior P . A novel ZZ/ZW sex chromosome system for the genus Leporinus (Pisces, Anostomidae, Characiformes). Genetica. 2004; 121(1):75-80. DOI: 10.1023/b:gene.0000019936.40970.7a. View

Cechova M, Vegesna R, Tomaszkiewicz M, Harris R, Chen D, Rangavittal S . Dynamic evolution of great ape Y chromosomes. Proc Natl Acad Sci U S A. 2020; 117(42):26273-26280. PMC: 7585023. DOI: 10.1073/pnas.2001749117. View

Kriventseva E, Kuznetsov D, Tegenfeldt F, Manni M, Dias R, Simao F . OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 2018; 47(D1):D807-D811. PMC: 6323947. DOI: 10.1093/nar/gky1053. View

Mitsuhashi S, Frith M, Mizuguchi T, Miyatake S, Toyota T, Adachi H . Tandem-genotypes: robust detection of tandem repeat expansions from long DNA reads. Genome Biol. 2019; 20(1):58. PMC: 6425644. DOI: 10.1186/s13059-019-1667-6. View

Logsdon G, Vollger M, Eichler E . Long-read human genome sequencing and its applications. Nat Rev Genet. 2020; 21(10):597-614. PMC: 7877196. DOI: 10.1038/s41576-020-0236-x. View

Hilsdorf A, Uliano-Silva M, Coutinho L, Montenegro H, Almeida-Val V, Pinhal D . Genome assembly and annotation of the tambaqui (): an emblematic fish of the Amazon River Basin. GigaByte. 2023; 2021:gigabyte29. PMC: 9650303. DOI: 10.46471/gigabyte.29. View

Ross A, Munger S, Capel B . Bmp7 regulates germ cell proliferation in mouse fetal gonads. Sex Dev. 2008; 1(2):127-37. DOI: 10.1159/000100034. View

Melo B, Sidlauskas B, Near T, Roxo F, Ghezelayagh A, Ochoa L . Accelerated Diversification Explains the Exceptional Species Richness of Tropical Characoid Fishes. Syst Biol. 2021; 71(1):78-92. PMC: 9034337. DOI: 10.1093/sysbio/syab040. View

10.

Zimin A, Salzberg S . The SAMBA tool uses long reads to improve the contiguity of genome assemblies. PLoS Comput Biol. 2022; 18(2):e1009860. PMC: 8849508. DOI: 10.1371/journal.pcbi.1009860. View

11.

de Carvalho D, Oliveira D, Pompeu P, Leal C, Oliveira C, Hanner R . Deep barcode divergence in Brazilian freshwater fishes: the case of the São Francisco River basin. Mitochondrial DNA. 2011; 22 Suppl 1:80-6. DOI: 10.3109/19401736.2011.588214. View

12.

Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P . Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet. 2014; 46(3):253-60. DOI: 10.1038/ng.2890. View

13.

Vurture G, Sedlazeck F, Nattestad M, Underwood C, Fang H, Gurtowski J . GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics. 2017; 33(14):2202-2204. PMC: 5870704. DOI: 10.1093/bioinformatics/btx153. View

14.

Carey S, Lovell J, Jenkins J, Leebens-Mack J, Schmutz J, Wilson M . Representing sex chromosomes in genome assemblies. Cell Genom. 2022; 2(5). PMC: 9205529. DOI: 10.1016/j.xgen.2022.100132. View

15.

Rautiainen M, Nurk S, Walenz B, Logsdon G, Porubsky D, Rhie A . Telomere-to-telomere assembly of diploid chromosomes with Verkko. Nat Biotechnol. 2023; 41(10):1474-1482. PMC: 10427740. DOI: 10.1038/s41587-023-01662-6. View

16.

Nurk S, Koren S, Rhie A, Rautiainen M, Bzikadze A, Mikheenko A . The complete sequence of a human genome. Science. 2022; 376(6588):44-53. PMC: 9186530. DOI: 10.1126/science.abj6987. View

17.

Jain C, Rhie A, Hansen N, Koren S, Phillippy A . Long-read mapping to repetitive reference sequences using Winnowmap2. Nat Methods. 2022; 19(6):705-710. PMC: 10510034. DOI: 10.1038/s41592-022-01457-8. View

18.

Reid D, Smith C, Rommens M, Blanchard B, Martin-Robichaud D, Reith M . A Genetic linkage map of Atlantic halibut (Hippoglossus hippoglossus L.). Genetics. 2007; 177(2):1193-205. PMC: 2034623. DOI: 10.1534/genetics.107.075374. View

19.

Ferreira I, Oliveira C, Venere P, Galetti Jr P, Martins C . 5S rDNA variation and its phylogenetic inference in the genus Leporinus (Characiformes: Anostomidae). Genetica. 2006; 129(3):253-7. DOI: 10.1007/s10709-006-0005-6. View

20.

Dudchenko O, Batra S, Omer A, Nyquist S, Hoeger M, Durand N . De novo assembly of the genome using Hi-C yields chromosome-length scaffolds. Science. 2017; 356(6333):92-95. PMC: 5635820. DOI: 10.1126/science.aal3327. View