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

Zhu

et al. 2022

Biology

The hook snout carp Opsariichthys bidens is an important farmed fish in East Asia that shows sexual dimorphism in growth, with males growing faster and larger than females. To understand these complex traits and improve molecular breeding, chromosome-level genome assembly of male O. bidens was performed using Illumina, Nanopore, and Hi-C sequencing. The 992.9 Mb genome sequences with a contig N50 of 5.2 Mb were anchored to 38 chromosomes corresponding to male karyotypes. Of 30,922 functionally annotated genes, 97.5% of BUSCO genes were completely detected. Genome evolution analysis showed that the expanded and contracted gene families in the male O. bidens genome were enriched in 76 KEGG pathways, and 78 expanded genes were involved in the GnRH signaling pathway that regulates the synthesis and secretion of luteinizing hormone and glycoprotein hormones, further acting on male growth by inducing growth hormone. Compared to the released female O. bidens genome, the number of annotated genes in males was much higher (23,992). The male chromosome LG06 exhibited over 97% identity with the female GH14/GH38. Male-specific genes were identified for LG06, where structural variation, including deletions and insertions, occurred at a lower rate, suggesting a centric fusion of acrocentric chromosomes GH14 and GH38. The genome-synteny analysis uncovered significant inter-chromosome conservation between male O. bidens and grass carp, the former originating from ancestral chromosome breakage to increase the chromosome number. Our results provide a valuable genetic resource for studying the regulation of sexual dimorphism, sex-determining mechanisms, and molecular-guided breeding of O. bidens.

Section: Discussionmentioning

confidence: 69%

“…To uncover the unique chromosomal evolution mechanism of the O. bidens genome, synteny comparison of the hook snout carp and grass carp genomes [ 58 ] was performed using JCVI with c-scores of >0.7, and tandem-nmax = 10 as filtering values [ 59 ].…”

Section: Methodsmentioning

confidence: 99%

Chromosome-Level Assembly of Male Opsariichthys bidens Genome Provides Insights into the Regulation of the GnRH Signaling Pathway and Genome Evolution

Zhu

et al. 2022

Biology

“…The high-quality grass carp genome was re-sequenced and assembled by our laboratory, which has been deposited under NCBI BioProjects with the accession number: PRJNA745929 ( 24 ). The grass carp CD80/86 , CD28 , and CD152 genes were searched using the Basic Local Alignment Search Tool (BLAST).…”

Section: Methodsmentioning

confidence: 99%

Molecular and Functional Analyses of the Primordial Costimulatory Molecule CD80/86 and Its Receptors CD28 and CD152 (CTLA-4) in a Teleost Fish

et al. 2022

Front. Immunol.

Self Cite

The moderate activation of T cells in mammals requires the costimulatory molecules, CD80 and CD86, on antigen-presenting cells to interact with their respective T cell receptors, CD28 and CD152 (CTLA-4), to promote costimulatory signals. In contrast, teleost fish (except salmonids) only possess CD80/86 as their sole primordial costimulatory molecule. However, the mechanism, which underlies the interaction between CD80/86 and its receptors CD28 and CD152 still requires elucidation. In this study, we cloned and identified the CD80/86, CD28, and CD152 genes of the grass carp (Ctenopharyngodon idella). The mRNA expression analysis showed that CD80/86, CD28, and CD152 were constitutively expressed in various tissues. Further analysis revealed that CD80/86 was highly expressed in IgM+ B cells. Conversely, CD28 and CD152 were highly expressed in CD4+ and CD8+ T cells. Subcellular localization illustrated that CD80/86, CD28, and CD152 are all located on the cell membrane. A yeast two-hybrid assay exhibited that CD80/86 can bind with both CD28 and CD152. In vivo assay showed that the expression of CD80/86 was rapidly upregulated in Aeromonas hydrophila infected fish compared to the control fish. However, the expression of CD28 and CD152 presented the inverse trend, suggesting that teleost fish may regulate T cell activation through the differential expression of CD28 and CD152. Importantly, we discovered that T cells were more likely to be activated by A. hydrophila after CD152 was blocked by anti-CD152 antibodies. This suggests that the teleost CD152 is an inhibitory receptor of T cell activation, which is similar to the mammalian CD152. Overall, this study begins to define the interaction feature between primordial CD80/86 and its receptors CD28 and CD152 in teleost fish, alongside providing a cross-species understanding of the evolution of the costimulatory signals throughout vertebrates.

“…To uncover the unique chromosomal evolution mechanism of the O. bidens genome, synteny comparison of the hooks out carp and grass carp genomes (Wu et al, 2022) was performed using JCVI with c-scores of > 0.7, and tandem-nmax = 10 as filtering values (Tang et al, 2017).…”

Section: Comparison Analysis Of Chromosomesmentioning

confidence: 99%

“…Hook snout carp have similar fundamental arm numbers to Leuciscin fishes, suggesting that the 76 chromosomes of male O. bidens resulted from the 2n = 48 chromosomes of Leuciscin fishes by breakage at centromere sites. Considering that C. idellus is regarded as a primitive species in Leuciscin fish species evolution (Wu et al, 2022), the synteny-based chromosome comparison between male O. bidens and C. idellus showed that out of the 24 chromosomes in C. idellus , one breakage into two chromosomes occurred in 12 chromosomes, providing evidence of added chromosome number via breakage. Our results could serve as a framework for studies on sex-determining mechanisms and genome evolution in fish.…”

Section: Mechanism Underlying O Bidens Chromosome Number Varietymentioning

confidence: 99%

Chromosome-level assembly of male Opsariichthys bidens genome provides insights into the regulation of the GnRH signaling pathway and genome evolution

Gui

Zhu

et al. 2022

Preprint

Hook snout carp Opsariichthys bidens is an important farmed fish in East Asia that shows sexual dimorphism in growth, with males growing faster and larger than females. To understand these complex traits and improve molecular breeding, chromosome-level genome assembly of male O. bidens was performed using Illumina, Nanopore, and Hi-C sequencing. The 992.9 Mb genome sequences with a contig N50 of 5.2 Mb were anchored to 38 chromosomes corresponding to male karyotypes. Of 30,922 functionally annotated genes, 97.5% of BUSCO genes were completely detected. Genome evolution analysis showed that the expanded and contracted gene families in male o.bedins genome were enriched in 76 KEGG pathways, and 78 expanded genes were involved in the GnRH signaling pathway that regulates the synthesis and secretion of luteinizing hormone and glycoprotein hormones, further acting on male growth by inducing growth hormone. Compared to the released female O. bidens genome, the number of annotated genes in males was much higher than in females (23,992). The male chromosome LG06 exhibited over 97% of identity with the female’s GH14/GH38. Male-specific genes were identified for LG06, where structural variety, including deletions and insertions, occurred at a lower rate, suggesting a centric fusion of acrocentric chromosomes GH14 and GH38. The genome-synteny analysis uncovered significant inter-chromosome conservation between male O. bidens and grass carp, and the former originating from ancestral chromosome breakage to increase the chromosome number. Our results provide a valuable genetic resource for studying the regulation of sexual dimorphism, sex-determining mechanisms and molecular-guided breeding of O. bidens.