Comparative genomic analysis of immune-related genes and chemosensory receptors provides insights into the evolution and adaptation of four major domesticated Asian carps

Abstract

Background: Ctenopharyngodon idella (grass carp), Mylopharyngodon piceus (black carp), Hypophthalmichthys nobilis (bighead carp), and Hypophthalmichthys molitrix (silver carp), collectively known as the four major domesticated Asian carp, are freshwater fish species from the family Cyprinidae and are widely consumed in China. Current studies on these species primarily focus on immune system regulation and the growth and development of individual species. However, in-depth genomic investigations and comprehensive comparative analysis remained limited.

Methods: The complete genomes of Ctenopharyngodon idella, Mylopharyngodon piceus and Hypophthalmichthys nobilis were assembled using a hybrid approach that integrated both next- and third-generation sequencing reads, followed by annotation using the MAKER2 pipeline. Based on the high-quality genomes of Ctenopharyngodon idella, Mylopharyngodon piceus Hypophthalmichthys nobilis, and Hypophthalmichthys molitrix, a comparative genomic analysis was conducted using bioinformatic tools to investigate gene family evolution in these four domesticated Asian carp species.

Results: High-quality genomes of Ctenopharyngodon idella, Mylopharyngodon piceus, and Hypophthalmichthys nobilis were assembled, achieving over 90% completeness. Immune-related gene families, including MHC class I and NLRC3-like genes, have undergone rapid evolution, with Ctenopharyngodon idella exhibiting significant expansion of NLRC3-like genes. Massive tandem duplication events were identified in trace amine-associated receptors (TAARs), and rapid expansion was observed in TAAR16 and TAAR29. Additionally, a novel TAAR gene cluster was identified in all four Asian carp species. Comparative genomic analysis revealed the expansion of type 1 taste receptor genes, particularly in Ctenopharyngodon idella and Mylopharyngodon piceus.

Conclusion: This study has successfully constructed the high-quality genomes of Ctenopharyngodon idella, Mylopharyngodon piceus, and Hypophthalmichthys nobilis. The comparative genomic analysis revealed the evolution of immune-related genes and chemosensory receptors in the four major domesticated Asian carp species. These findings suggested the enhanced immunity and sensory perception in these species, providing valuable insights into their adaptation, survival and reproduction.

Keywords: Chemosensory receptors; Comparative genomic analysis; Four major domesticated Asian carp species; Gene family evolution; Immune-related genes.

Fig. 1

The phylogenomic analysis of Asian carp and other Cyprinidae species. A The gene family expansion and contraction of 11 Cyprinidae speices: Carassius auratus, Cyprio carpio, Sinocyclocheilus grahami, Onychostoma macrolepis, Puntigrus tetrazona, Labeo rohita, Ctenopharyngodon idella, Mylopharyngodon piceus, Hypophthalmichthys nobilis and Hypophthalmichthys molitrix, Danio rerio and outgroup species Chanos chanos were analyzed by CAFE. The numbers indicate the number of orthogroups under expansion (+ and green) or contraction (- and red) and rapidly evolving orthogroups (* and blue). B Venn diagram of orthogroups of the group Asian carp species. The proteomes were assigned into orthogroups using OrthoFinder, and the overlapped orthogroups of the four Asian carp species were then presented using a Venn diagram

Fig. 2

The phylogenetic relationships of MHC class I gene family. A All the MHC class I genes in the four Asian carp species were classified into U, L and Z (Z1 and Z2) lineages based on the phylogenetic relationships. The phylogenetic analysis of MHC class I (B) U lineage genes, C Z1 lineage genes and (D) Z2 lineage genes in the four Asian carp species were examined. The number of MHC class I genes from different lineages in each Asian carp species was denoted, and all the T/PAGs were connected by curved lines

Fig. 3

The phylogenetic relationships of NLRC3/NLRC3-like gene in C1 and C3 cluster. All the NLRC3/NLRC3-like genes in the four Asian carp species were classified into three clusters (C1-C3) based on four categories of domain structures and the phylogenetic relationships. C1 cluster is consisted of genes with NACHT-LRR-SPRY structure, whereas C3 cluster is composed of genes with mainly NACHT-LRR structure. The phylogenetic relationships of (A) C1 cluster genes and (B) C3 cluster genes were examined, respectively. The number of NLRC3/NLRC3-like genes from C1 and C3 cluster in each Asian carp species was denoted, and all the T/PAGs were connected by curved lines

Fig. 4

The phylogenetic relationships of trace amine-associated receptors (TAARs). A All the TAAR genes in the four Asian carp species (C. idella, M. piceus, H. nobilis and H. molitrix) together with D. rerio and C. auratus were classified into 14 different TAAR subfamilies based on phylogenetic relationships. The phylogenetic relationships of (B) cluster A TAAR genes, C TAAR16 subfamily, and D TAAR29 subfamily were analyzed. Cluster A TAARs were exclusively observed in the four Asian carp species, while TAAR16 and TAAR29 genes can also be identified in D. rerio and C. auratus. The number of TAARs in different species was denoted, and all the T/PAGs were connected by curved lines

Fig. 5

The expansion of fish vomeronasal type-1 receptors (V1R/ORA). A The phylogenetic relationships of V1R/ORA family in the four Asian carp species and D. rerio were analyzed and classified into six clusters (ORA1-ORA6). The T/PAGs were connected by curved lines. B The gene synteny alignment of ORA5 genes in the four Asian carp species and D. rerio were compared, with an additional ORA5 gene identified in Asian carp. The black arrow indicated reverse complement. C The sequence alignment of ORA5 genes in the four Asian carp species, with “GC” as C. idella (grass carp), “BC” as M. piceus (black carp), BH as H. nobilis (bighead carp), and SC as H. molitrix (silver carp)

Fig. 6

The expansion of taste receptor type 1 genes (TAS1R). A The phylogenetic relationships of TAS1R genes were revealed in the four Asian carp species. All the TAS1R genes were classified into TAS1R1, TAS1R2 and TAS1R3 gene clusters. The number of TAS1R genes in each species was denoted and all the T/PAGs were connected by curved lines. B The gene synteny alignment of TAS1R2 genes in the four Asian carp species and D. rerio were analyzed. TAS1R2 A and TAS1R2B gene were tandemly arrayed in the five species examined. TAS1R2C, TAS1R2D, TAS1R2E and TAS1R2F gene were generated through tandem duplications in C. idella and M. piceus