Elasmobranch genome sequencing reveals evolutionary trends of vertebrate karyotype organization

Abstract

Genomic studies of vertebrate chromosome evolution have long been hindered by the scarcity of chromosome-scale DNA sequences of some key taxa. One of those limiting taxa has been the elasmobranchs (sharks and rays), which harbor species often with numerous chromosomes and enlarged genomes. Here, we report the chromosome-scale genome assembly for the zebra sharkStegostoma tigrinum, an endangered species that has the smallest genome sequenced to date among sharks (3.71 Gb), as well as for the whale sharkRhincodon typus. Our analysis employing a male–female comparison identified an X chromosome, the first genomically characterized shark sex chromosome. The X chromosome harbors a Hox C cluster whose intact linkage has not been shown for an elasmobranch fish. The sequenced shark genomes exhibit a gradualism of chromosome length with remarkable length-dependent characteristics—shorter chromosomes tend to have higher GC content, gene density, synonymous substitution rate, and simple tandem repeat content as well as smaller gene length, which resemble the edges of longer chromosomes. This pattern of intragenomic heterogeneity, previously recognized as peculiar to species with so-called microchromosomes, occurs in more vertebrates including elasmobranchs. We challenge the traditional binary classification of karyotypes as with and without microchromosomes, as even without microchromosomes, shorter chromosomes tend to have higher contents of GC and simple tandem repeats and harbor shorter and more rapid-evolving genes. Such characteristics also appear on the edges of longer chromosomes. Our investigation of elasmobranch karyotypes underpins their unique characteristics and provides clues for understanding how vertebrate karyotypes accommodate intragenomic heterogeneity to realize a complex readout.

The sensory shark: high-quality morphological, genomic and transcriptomic data for the small-spotted catsharkScyliorhinus caniculareveal the molecular bases of sensory organ evolution in jawed vertebrates

“…In accordance with previous studies (Oulion et al 2010), we identified 34 Hox genes in this dataset (Supplementary Figure 5, Supplementary Table 9). We found no evidence for the HoxC cluster known to be present in the elephant shark Callorhinchus milii (Ravi et al 2009) and the zebra shark Stegostoma tigrinum (Yamaguchi, Uno, et al 2023). Over 24,473 NCBI sequences, 11,945 (48.8%) were extended with a mean addition of about 1,845 bp per prolonged sequence.…”

“…Hox protein sequences from a range of cartilaginous fish (Supplementary Table 3) and humans were downloaded from NCBI, and used as queries in tBLASTn searches of the Scyliorhinus canicula gene model dataset (Mayeur et al 2021) and the genome assembly. We also used chondrichthyan and human protein sequences of the HoxC flanking genes tspan31 , ddx23 , rnd1 , adcy6 , smug1 , and copz1 (Yamaguchi, Uno, et al 2023) to identify the syntenic region in the S. canicula assembly.…”

Shark and ray genome size estimation: methodological optimization for inclusive and controllable biodiversity genomics

“…Our k-mer-based estimate of its genome size using raw sequence reads resulted in an even smaller value of approximately 1.7 Gbp. Similarly, for the zebra shark Stegostoma tigrinum whose nuclear DNA content was estimated to be 3.70 Gb (C-value =3.79 pg), the total sequence length of the genome assembly released previously by us 30 (sSteFas1.1; GCA_022316705.1) amounts to only 2.771 Gbp. Our k-mer-based estimate of its genome size using raw sequence reads resulted in approximately 2.805 Gbp.…”

“…In parallel with the genome size estimate using the flow cytometry and qPCR, those of the zebra shark and thorny skate were estimated in silico based on k-mer frequency distribution with a conventional procedure. For the zebra shark, short-read genomic data produced previously by us 30 (see Yamaguchi et al, 2022) were used. For the thorny skate, short-read genomic data produced by the Vertebrate Genomes Project 31 was downloaded from VGP GenomeArk (s3://genomeark/species/Amblyraja_radiata/sAmbRad1/genomic_data/illumina/).…”