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. 2020 Nov 2;23(11):101754.
doi: 10.1016/j.isci.2020.101754. eCollection 2020 Nov 20.

The White-Spotted Bamboo Shark Genome Reveals Chromosome Rearrangements and Fast-Evolving Immune Genes of Cartilaginous Fish

Yaolei Zhang  1   2   3 , Haoyang Gao  1   2 , Hanbo Li  1   2 , Jiao Guo  1   2 , Bingjie Ouyang  1   2 , Meiniang Wang  4   2 , Qiwu Xu  1   2 , Jiahao Wang  1   2 , Meiqi Lv  1   2 , Xinyu Guo  1   2 , Qun Liu  1   2 , Likun Wei  5 , Han Ren  4   2 , Yang Xi  4   2 , Yang Guo  1   2 , Bingzhao Ren  1   2 , Shanshan Pan  1   2 , Chuxin Liu  4   2 , Xiaoyan Ding  1   2 , Haitao Xiang  4   2 , Yingjia Yu  1   2 , Yue Song  1   2 , Lingfeng Meng  1   2 , Shanshan Liu  1   2 , Jun Wang  1   2 , Yuan Jiang  4   6 , Jiahai Shi  5 , Shiping Liu  4   2 , Jamal S M Sabir  7 , Mumdooh J Sabir  7 , Muhummadh Khan  7 , Nahid H Hajrah  7 , Simon Ming-Yuen Lee  8 , Xun Xu  4   2 , Huanming Yang  4   9 , Jian Wang  4   9 , Guangyi Fan  1   8   2 , Naibo Yang  4   6 , Xin Liu  1   4   2
Affiliations

The White-Spotted Bamboo Shark Genome Reveals Chromosome Rearrangements and Fast-Evolving Immune Genes of Cartilaginous Fish

Yaolei Zhang et al. iScience. .

Abstract

Chondrichthyan (cartilaginous fish) occupies a key phylogenetic position and is important for investigating evolutionary processes of vertebrates. However, limited whole genomes impede our in-depth knowledge of important issues such as chromosome evolution and immunity. Here, we report the chromosome-level genome of white-spotted bamboo shark. Combing it with other shark genomes, we reconstructed 16 ancestral chromosomes of bamboo shark and illustrate a dynamic chromosome rearrangement process. We found that genes on 13 fast-evolving chromosomes can be enriched in immune-related pathways. And two chromosomes contain important genes that can be used to develop single-chain antibodies, which were shown to have high affinity to human disease markers by using enzyme-linked immunosorbent assay. We also found three bone formation-related genes were lost due to chromosome rearrangements. Our study highlights the importance of chromosome rearrangements, providing resources for understanding of cartilaginous fish diversification and potential application of single-chain antibodies.

Keywords: Biological Sciences; Evolutionary Biology; Genetics; Genomics; Phylogenetics.

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Conflict of interest statement

The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Genome Assembly and Phylogeny of Bamboo Shark (A) Heatmap of chromatin interaction relationships at 125 kb resolution of 51 chromosomes. (B) Phylogenetic tree and divergence time estimation of cartilaginous fish and representative bony fishes. Red dots mean reference times from TimeTree database (http://www.timetree.org/).
Figure 2
Figure 2
Chromosome Evolution of Bamboo Shark (A) Construction of the ancestral chromosome model of elephant shark and bamboo shark. The lines on the left represent the phylogenetic tree. The dotted lines on the left represent the second WGD event for vertebrates and rearrangement events of ancestral chromosomes of sharks. Letters from A to P represent constructed ancestral chromosomes. Letters Q, R, S, T, and U represent small chromosomes that may be the result of more recent fissions from the larger chromosomes. The colored arrows represent rearrangements of chromosomes. The black arrows represent rearrangements specific to the bamboo shark. The dotted arrows represent potential rearrangements that are supported by gene pairs. The red star represents the second whole-genome duplication occurred before the divergence of sea lamprey and gnathostome (Smith et al., 2013) (earlier than ~601 Ma). The blue star represents rearrangement events of shark ancestral chromosomes. The times are cited from the TimeTree database. (B) (Top): Distribution of conserved genes of elephant shark, bamboo shark, whale shark, brownbanded bamboo shark, cloudy catshark, white shark and medaka. Magenta, conserved regions shared by four species (R1). Orange, common regions in six shark genomes excluding R1. Green, regions shared between the bamboo shark and medaka excluding R1. The red arrows point out 13 fast-evolving chromosomes. (Bottom) Heterozygosity of 51 chromosomes in bamboo shark genome. (C) Comparison of Ks values of single-copy orthologous genes between 13 fast-evolving chromosomes and other chromosomes.
Figure 3
Figure 3
Specific Immune-Related Genes of Bamboo Shark (A) Distribution of MHC genes on chromosome 37. The red and blue rectangles represent MHC class I and class II genes, respectively. The gray rectangles represent non-MHC genes. Here, we only show syntenic genes and shark MHC genes compared with chicken. (B) Distribution of identified IgNAR loci on chromosome 44. (C) Syntenic relationship of assemblies of IgNAR region by using shotgun WGS and stLFR data. The gray lines represent consistent region. The blue rectangles represent gaps. (D, E, and F) Binding efficiency of cloned vNARs to human disease markers (D) YKL40, (E) CD64, and (F) Ki67 by using monoclonal phage ELISA. NC represents negative control. The vertical axis represents the signal of binding measured using optical density (OD450).
Figure 4
Figure 4
The Loss of p2rx3, p2rx5, and p2rx7 Genes in Cartilaginous Fishes (A) The syntenic relationship of the p2rx5 region among bamboo shark, chicken, medaka, and zebrafish. The red rectangles represent P2X genes. The lines represent syntenic genes. The numbers besides the pink dots represent gene number in the gap regions. From the figure, we can see the gene loss of p2rx5 in bamboo shark genome after at least four chromosome rearrangements. (B) Phylogenetic tree of the P2X gene family. Dan: zebrafish, GAD: Atlantic cod, Gas: three-spined sticklebacks, Ory: medada, Lat: coelacanth, Sal: Atlantic salmon, Fug: torafugu, Lar: large yellow croaker, Rhi: whale shark, Cal: elephant shark, Bam: bamboo shark, Chp: brownbanded bamboo shark, Cac: white shark, Scy: cloudy catshark, PMZ: sea lamprey. The shark's P2X genes are marked red. Although many p2rx5 genes exist in PMZ, all these genes were less than 246 aa in length (10 of 14 less than 200 aa). This tree was constructed with protein sequences of these genes by using software of MUSCLE (v3.8.31) (Edgar, 2004) and FastTree (v2.1.10) (Price et al., 2010).
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