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

Genome Biol. 2021 Jul 12;22(1):203. doi: 10.1186/s13059-021-02430-y.

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.

Keywords: Centromere; Fish genome; Heterochromatin; Recombination suppression; Sex chromosome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Centromere
  • Eels / genetics*
  • Fish Proteins / genetics
  • Fish Proteins / metabolism
  • Gene Expression
  • Genome*
  • HMGN Proteins / genetics*
  • HMGN Proteins / metabolism
  • Heterochromatin / chemistry
  • Karyotype
  • Male
  • Sex Determination Processes*
  • Telomere*
  • Testis / growth & development
  • Testis / metabolism
  • X Chromosome
  • Y Chromosome / chemistry*

Substances

  • Fish Proteins
  • HMGN Proteins
  • Heterochromatin