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.