Telomere-to-telomere assembly of a fish Y chromosome reveals the origin of a young sex chromosome pair

Abstract

Background The origin of sex chromosomes requires the establishment of recombination suppression between the proto-sex chromosomes. In many fish species, the sex chromosome pair is homomorphic with a recent origin, providing species for studying how and why recombination suppression evolved in the initial stages of sex chromosome differentiation, but this requires accurate sequence assembly of the X and Y (or Z and W) chromosomes, which may be difficult if they are recently diverged. Results Here we produce a haplotype-resolved genome assembly of zig-zag eel (Mastacembelus armatus), an aquaculture fish, at the chromosomal scale. The diploid assembly is nearly gap-free, and in most chromosomes, we resolve the centromeric and subtelomeric heterochromatic sequences. In particular, the Y chromosome, including its highly repetitive short arm, has zero gaps. Using resequencing data, we identify a ~7 Mb fully sex-linked region (SLR), spanning the sex chromosome centromere and almost entirely embedded in the pericentromeric heterochromatin. The SLRs on the X and Y chromosomes are almost identical in sequence and gene content, but both are repetitive and heterochromatic, consistent with zero or low recombination. We further identify an HMG-domain containing gene HMGN6 in the SLR as a candidate sex-determining gene that is expressed at the onset of testis development. Conclusions Our study supports the idea that preexisting regions of low recombination, such as pericentromeric regions, can give rise to SLR in the absence of structural variations between the proto-sex chromosomes.

Assembled chromosomes of the blood fluke Schistosoma mansoni provide insight into the evolution of its ZW sex-determination system

“…13.456314 doi: bioRxiv preprint 4 at a lower copy number than autosomes, and the problem of assembling them is compounded by difficult to resolve highly repetitive sequences and by genetic divergence between the sex chromosomes, such that they can vary along their lengths [5]. There are exceptions-notably the recent publication of the eel genome [6] included resolved centromeres, subtelomeric sequences and the highly repetitiive Y chromosome short arm containing no gaps-but other sex chromosome assemblies, such as the Drosophila Y chromosome [7] and Gallus gallus W chromosome [8], are in fragmented states and even the reference human Y chromosome assembly [9] lacks continuity between the heterochromatic and euchromatic regions.…”

Analysis of Sex Chromosome Evolution in the Clade Palaeognathae from Phased Genome Assembly

“…It is true that phased assemblies have already been obtained for the S1 region of emu in a previous study ( Liu et al 2021 ); however, the previous assembly was constructed from costly data produced by various platforms, such as PacBio, 10× Genomics-linked reads, Dovetail Chicago data, and Hi-C data, making this method not easily extendable to other species. Similarly, circulating consensus sequencing (CCS) using PacBio sequencers has made it possible to generate highly accurate 10–20 kb high-fidelity (HiFi) reads ( Wenger et al 2019 ) and combining this technology with Hi-C data has contributed to several published chromosome-scale phased assembly studies ( Garg et al 2021 ), including the construction of the zig-zag eel Y chromosome ( Xue et al 2021 ), which is expected to be applied to sex chromosome determination in other species. However, this combined method is less cost-effective than the method described in this study.…”

The Complete Mitochondrial Genome of One Breeding Strain of Asian Swamp Eel (Monopterus albus, Zuiew 1793) Using PacBio and Illumina Sequencing Technologies and Phylogenetic Analysis in Synbranchiformes

“…The divergence time of the Synbranchidae and Mastacembelidae families could be dated back to 64.1 Mya within the Paleocene epoch. With further mitogenome data for this order, these results would provide a consolidated framework for further studies, such as the karyotype or chromosome evolution [46][47][48], adaptive evolution to different environments [49] for those closely related species, and the dispersal history of the order Synbranchiformes [7,45] in the future.…”