Chromosome-level genome assembly of grass carp (Ctenopharyngodon idella) provides insights into its genome evolution

Abstract

Background: The grass carp has great economic value and occupies an important evolutionary position. Genomic information regarding this species could help better understand its rapid growth rate as well as its unique body plan and environmental adaptation.

Results: We assembled the chromosome-level grass carp genome using the PacBio sequencing and chromosome structure capture technique. The final genome assembly has a total length of 893.2 Mb with a contig N50 of 19.3 Mb and a scaffold N50 of 35.7 Mb. About 99.85% of the assembled contigs were anchored into 24 chromosomes. Based on the prediction, this genome contained 30,342 protein-coding genes and 43.26% repetitive sequences. Furthermore, we determined that the large genome size can be attributed to the DNA-mediated transposable elements which accounted for 58.9% of the repetitive sequences in grass carp. We identified that the grass carp has only 24 pairs of chromosomes due to the fusion of two ancestral chromosomes. Enrichment analyses of significantly expanded and positively selected genes reflected evolutionary adaptation of grass carp to the feeding habits. We also detected the loss of conserved non-coding regulatory elements associated with the development of the immune system, nervous system, and digestive system, which may be critical for grass carp herbivorous traits.

Conclusions: The high-quality reference genome reported here provides a valuable resource for the genetic improvement and molecular-guided breeding of the grass carp.

Keywords: Adaptive evolution; Chromosome-level genome; Comparative genomics; Cyprinid fish; Grass carp.

Fig. 1

Structural characteristics and evolution of cyprinid genomes. A Chromosomal contact maps of grass carp using Hi-C data. The blocks refer to the contacts between one location and another. The deeper colors represent the higher intensity of contact. B Collinear blocks of genes shared by the zebrafish and grass carp genomes. Each colored line represents a best match between the two species. The number of genes in blocks is greater than 30. C The average genome sizes, TE sizes, and contents of different TE types of cyprinids. D The relationship between genome size and TE size in cyprinids using the spearman method

Fig. 2

The maximum likelihood phylogenetic tree from single-copy gene protein sequences of 19 teleosts. To compute the node supports, 1000 bootstraps were used, and all nodes have 100% support. The red marker represents cyprinids, blue marker represents the sister group of cyprinids, purple marker represents outgroup. (PEN: Permian, Ng: Neogene)

Fig. 3

Venn diagram of gene families among five cyprinids and functional enrichment analysis of gene families specific to zebrafish and grass carp. A Common and unique gene families among five cyprinids shown with a Venn diagram. B GO enrichment analysis of gene families specific to zebrafish. C GO enrichment analysis of gene families specific to grass carp

Fig. 4

Expanded gene families, contracted gene families, rapidly evolving gene families and positively selected genes (PSGs) among teleosts and functional enrichment analysis. A PSGs, rapidly evolving gene families, expanded and contracted gene families are shown along the phylogenetic tree (left). The number of four rapidly evolving histone genes in 19 teleosts (right). B KEGG enrichment analysis of expanded gene families in 10 cyprinids. C MP enrichment analysis of PSGs in grass carp

Fig. 5

CNE adjacent gene function enrichment analysis and CNEs in HoxBa cluster of cyprinids. A Top 20 statistically significant (p value < 0.01) GO biological process terms (specific presence in zebrafish and D. translucida, but specific deletion in other cyprinids). B Top 20 statistically significant (p value < 0.01) GO biological process terms (specific deletion in grass carp). C VISTA sequence conservation plot of the grass carp specific deletion CNE around Hoxb5a, Hoxb6a and Hoxb7a, using zebrafish (GRCz11) as reference