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Reconstruction of the Origin of a Neo-Y Sex Chromosome and Its Evolution in the Spotted Knifejaw, Oplegnathus punctatus.

ABSTRACT: Sex chromosomes are a peculiar constituent of the genome because the evolutionary forces that fix the primary sex-determining gene cause genic degeneration and accumulation of junk DNA in the heterogametic partner. One of the most spectacular phenomena in sex chromosome evolution is the occurrence of neo-Y chromosomes, which lead to X1X2Y sex-determining systems. Such neo-sex chromosomes are critical for understanding the processes of sex chromosome evolution because they rejuvenate their total gene content. We assembled the male and female genomes at the chromosome level of the spotted knifejaw (Oplegnathus punctatus), which has a cytogenetically recognized neo-Y chromosome. The full assembly and annotation of all three sex chromosomes allowed us to reconstruct their evolutionary history. Contrary to other neo-Y chromosomes, the fusion to X2 is quite ancient, estimated at 48 Ma. Despite its old age and being even older in the X1 homologous region which carries a huge inversion that occurred as early as 55-48 Ma, genetic degeneration of the neo-Y appears to be only moderate. Transcriptomic analysis showed that sex chromosomes harbor 87 genes, which may serve important functions in the testis. The accumulation of such male-beneficial genes, a large inversion on the X1 homologous region and fusion to X2 appear to be the main drivers of neo-Y evolution in the spotted knifejaw. The availability of high-quality assemblies of the neo-Y and both X chromosomes make this fish an ideal model for a better understanding of the variability of sex determination mechanisms and of sex chromosome evolution.

SUBMITTER: Li M

PROVIDER: S-EPMC8136494 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe barred knifejaw (Oplegnathus fasciatus), a member of the Oplegnathidae family of the Centrarchiformes, is a commercially important rocky reef fish native to East Asia. Oplegnathus fasciatus has become an important fishery resource for offshore cage aquaculture and fish stocking of marine ranching in China, Japan, and Korea. Recently, sexual dimorphism in growth with neo-sex chromosome and widespread biotic diseases in O. fasciatus have been increasing concern in the industry. However, adequate genome resources for gaining insight into sex-determining mechanisms and establishing genetically resistant breeding systems for O. fasciatus are lacking. Here, we analyzed the entire genome of a female O. fasciatus fish using long-read sequencing and Hi-C data to generate chromosome-length scaffolds and a highly contiguous genome assembly.FindingsWe assembled the O. fasciatus genome with a total of 245.0 Gb of raw reads that were generated using both Pacific Bioscience (PacBio) Sequel and Illumina HiSeq 2000 platforms. The final draft genome assembly was approximately 778.7 Mb, which reached a high level of continuity with a contig N50 of 2.1 Mb. The genome size was consistent with the estimated genome size (777.5 Mb) based on k-mer analysis. We combined Hi-C data with a draft genome assembly to generate chromosome-length scaffolds. Twenty-four scaffolds corresponding to the 24 chromosomes were assembled to a final size of 768.8 Mb with a contig N50 of 2.1 Mb and a scaffold N50 of 33.5 Mb using 1,372 contigs. The identified repeat sequences accounted for 33.9% of the entire genome, and 24 003 protein-coding genes with an average of 10.1 exons per gene were annotated using de novo methods, with RNA sequencing data and homologies to other teleosts. According to phylogenetic analysis using protein-coding genes, O. fasciatus is closely related to Larimichthys crocea, with O. fasciatus diverging from their common ancestor approximately 70.5-88.5 million years ago.ConclusionsWe generated a high-quality draft genome for O. fasciatus using long-read PacBio sequencing technology, which represents the first chromosome-level reference genome for Oplegnathidae species. Assembly of this genome assists research into fish sex-determining mechanisms and can serve as a resource for accelerating genome-assisted improvements in resistant breeding systems.

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Reconstruction of the Origin of a Neo-Y Sex Chromosome and Its Evolution in the Spotted Knifejaw, Oplegnathus punctatus.

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