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.
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Background
Grass carp has a breeding history of more than 1700 years in China. Since the 1980s, grass carp has been introduced directly or indirectly to various countries of the world, such as the United States, Mexico, India and Hungary [1]. Its artificial breeding began in 1958 and it is the most productive species in freshwater fish farming in the world, with great economic effects, providing a large amount of high-quality protein and trace elements for all mankind. In 2020, the total production of freshwater fish farming in China was 30.89 million tons, of which grass carp had the highest production (5.57 million tons), accounting for about 18% of the total production [2]. Due to strong adaptability, rapid growth, and large size of grass carp, it is known as one of the “Four Domesticated Fish” in freshwater culture in China, together with the bighead carp (Hypophthalmichthys nobilis), silver carp (Hypophthalmichthys molitrix), black carp (Mylopharyngodon piceus). It should be noted that the “Four Domesticated Fish” belong to the family Xenocyprididae in the latest classification system (Eschmeyer’s Catalog of Fishes), which previously classified them as Cyprinidae. Grass carp is a typical herbivorous fish and mainly distributed in the Yangtze, Pearl and Heilongjiang rivers in China. Food habit transition during the development of grass carp facilitates the rapid growth and development. Previous research has shown that the body weight, body length and intestine length of transitioned grass carp are significantly higher than that of the untransitioned grass carp. The genes involving circadian rhythm, lipid synthesis and metabolic pathways have undergone adaptive changes after transition of food habits, making it more effective to use the nutrients in plants [3].
Via high-throughput whole-genome sequencing technology we can accurately obtain the base sequences of a species to decipher its genetic information. It can reveal the complexity and genetic diversity of the species genome, which brings new research methods and solutions to explore the mechanism of species development and environmental adaptability, thereby speeding up the breeding process of new varieties [4, 5]. In recent years, the genome sequences of major freshwater economic fishes in China have constantly published. Such as blunt snout bream (Megalobrama amblycephala) [6,69] was used for multiple sequence alignment of clean data, and HTSeq (v.0.11.2) [70] was used to calculate TPM value for gene expression. Although the whole genomic sequence of M. amblycephala has been published, the resulting document of gene structure prediction has not been made public [Conservation or loss of CNEs in teleost fish genomes A CNE was considered present in a cyprinid fish genome if it showed a coverage of at least 30% with a zebrafish CNE in Multiz [81] alignment. To identify CNEs that could have been missed in the Multiz alignments due to rearrangements in the genomes, or due to partitioning of the CNEs among cyprinid fish duplicate genes, we searched the zebrafish CNEs against the genome of the cyprinid fish using BLASTN (E-value <1e-10; ≥ 80% identity; ≥ 30% coverage). Those CNEs that had no significant match in a cyprinid fish genome were considered as missing in that genome. The method of CNEs annotation refers to previous research [20, 82]. We visualized CNEs using the online tool VISTA (https://genome.lbl.gov/vista) [83]. For greater insight into the evolutionary dynamics of the genes, the expansion and contraction of the gene ortholog clusters were determined (p value < 0.01) among the 19 species by comparing cluster sizes between ancestors and each current species using CAFÉ software (v.4.2.1) [84]. The gene gain and loss along each lineage of the RAxML tree were calculated by CAFÉ software with a random birth and death process model. A probabilistic graphical model (PGM) was introduced to calculate the probability of transitions in gene family size from parent to child on the phylogeny. The expanded and contracted gene families in grass carp were identified by comparison with other species, and expanded and contracted gene families in other species were identified by comparison with ancestors. KEGG and GO analyses were conducted based on gene families exclusively presented and specifically expanded and contracted in cyprinid fish using clusterProfiler [85]. All one-to-one orthologous genes extracted from 19 species were used to identify PSGs. The multiple sequence alignments were generated and used to estimate three types of ω (the ratio of the rate of nonsynonymous substitutions to the rate of synonymous substitutions) using branch model in the codeml program of the PAML package (v.4.8) [78]. Branch model (model = 2, NS sites = 0) was used to detect ω of appointed branch to test (ω0) and average ω of all the other branches (ω1) and the mean of whole branches (ω2). Then χ2 test was used to check whether ω0 was significantly higher than ω1 and ω2 under the threshold p value < 0.01, which hinted that these genes would be under positive selection or fast evolution.Expansion and contraction of gene families
Identification of positively selected genes (PSGs)
Availability of data and materials
The raw genome, transcriptome and Hi-C data have been deposited in the SRA under bioproject number PRJNA745278 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA745278). The final chromosome assembly was submitted to NCBI under bioproject number PRJNA745929 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA745929).
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Acknowledgements
We thank Dr. Lianfu Chen (Huazhong Agricultural University, Wuhan, China.) for providing a bioinformatics analysis platform.
Funding
This research was funded by the National Natural Science Foundation of China (31930114).
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Contributions
Y.Z. and X.Z. conceived and initiated the study. S.Z. and G.Z. provided experimental materials. C.W. and Z.M. performed the genome sequencing and bioinformatics analyses. Y.Z. and C.W. wrote and revised the manuscript. All authors reviewed and approved the manuscript.
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All animal procedureexperimentss were performed in accordance with the Animal Ethic Committee of Huazhong Agricultural University (HZAU) and the protocols were approved by the Ethical Committee of HZAU (HZAUFI-2016-007). recommendations in the Guide for the Care and Use of Laboratory Animals of the Ministry of Science and Technology of China and were approved by the Animal Experiment Committee of Huazhong Agricultural University (permit number HZAUFI-2016-007). All efforts were made to minimize the suffering of the animals. This study also adheres to the ARRIVE Guidelines for reporting animal research [86].
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Supplementary Information
Additional file 1: Figure S1
. Distribution density of genes on grass carp chromosomes. Color from blue to red indicates increased gene density.
Additional file 2: Figure S2
. Ratio of syntenic depth between zebrafish and grass carp. Syntenic blocks of zebrafish per grass carp gene (left) and syntenic blocks of grass carp per zebrafish gene (right) are shown indicating 2:1 pattern of zebrafish to grass carp.
Additional file 3: Figure S3
. Coalescent species tree inferred by ASTRAL and MP-EST. Five thousand sixty-seven protein coding gene trees were used to infer the species tree using (A) ASTRAL and (B) MP-EST.
Additional file 4: Figure S4
. KEGG pathway annotation of grass carp newly evolved genes.
Additional file 5: Table S1
. Genomic information statistics of 19 teleosts (genome size information from NCBI public database).
Additional file 6: Table S2
. The summary of previous and current grass carp genomes.
Additional file 7: Table S3
. Completeness assessment of grass carp (previous and current genomes) and blunt snout bream (newly predicted genes) genomes by BUSCO.
Additional file 8: Table S4
. The statistically significant (p value < 0.001) GO biological process terms of grass carp and blunt snout bream common gene families.
Additional file 9: Table S5
. The top 20 statistically significant KEGG pathways of grass carp and blunt snout bream specially expanded gene family.
Additional file 10: Table S6
. The top 20 statistically significant GO biological process terms of grass carp specifically expanded gene families.
Additional file 11: Table S7
. The top 20 statistically significant KEGG pathways of grass carp specifically expanded gene families.
Additional file 12: Table S8
. The top 20 statistically significant GO biological process terms of grass carp and blunt snout bream PSGs.
Additional file 13: Table S9
. The top 20 statistically significant KEGG pathways of grass carp and blunt snout bream PSGs.
Additional file 14: Table S10
. The top 20 statistically significant GO biological process terms of grass carp PSGs.
Additional file 15: Table S11
. The top 20 statistically significant KEGG pathways of grass carp PSGs.
Additional file 16: Table S12
. Number of CNEs specific presence and deletion in one of the cyprinid genomes.
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Wu, CS., Ma, ZY., Zheng, GD. et al. Chromosome-level genome assembly of grass carp (Ctenopharyngodon idella) provides insights into its genome evolution. BMC Genomics 23, 271 (2022). https://doi.org/10.1186/s12864-022-08503-x
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DOI: https://doi.org/10.1186/s12864-022-08503-x