Skip to main content

Advertisement

SpringerLink
Log in

Genome Structural Variation Landscape and Its Selection Signatures in the Fast-growing Strains of the Pacific Oyster, Crassostrea gigas

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

The Pacific oyster (Crassostrea gigas) genome is highly polymorphic and affluent in structural variations (SVs), a significant source of genetic variation underlying inter-individual differences. Here, we used two genome assemblies and 535 individuals of genome re-sequencing data to construct a comprehensive landscape of structural variations in the Pacific oyster. Through whole-genome alignment, 11,087 short SVs and 11,561 copy number variations (CNVs) were identified. While analysis of re-sequencing data revealed 511,170 short SVs and 979,486 CNVs, a total of 63,100 short SVs and 58,182 CNVs were identified in at least 20 samples and regarded as common variations. Based on the common short SVs, both Fst and Pi ratio statistical methods were employed to detect the selective sweeps between 20 oyster individuals from the fast-growing strain and 20 individuals from their corresponding wild population. A total of 514 overlapped regions (8.76 Mb), containing 746 candidate genes, were identified by both approaches, in addition with 103 genes within 61 common CNVs only detected in the fast-growing strains. The GO enrichment and KEGG pathway analysis indicated that the identified candidate genes were mostly associated with apical part of cell and were significantly enriched in several metabolism-related pathways, including tryptophan metabolism and histidine metabolism. This work provided a comprehensive landscape of SVs and revealed their responses to selection, which will be valuable for further investigations on genome evolution under selection in the oysters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alkan C, Coe BP, Eichler EE (2011) Genome structural variation discovery and genotyping. Nat Rev Genet 12:363–376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alonge M, Wang X, Benoit M et al (2020) Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell 182:145-161.e23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertolotti AC, Layer RM, Gundappa MK et al (2020) The structural variation landscape in 492 Atlantic salmon genomes. Nat Commun 11:5176

  • Brosnan ME, Brosnan JT (2020) Histidine metabolism and function. J Nutr 150:2570S-2575S

    Article  PubMed  PubMed Central  Google Scholar 

  • Chakraborty M, Emerson JJ, Macdonald SJ, Long AD (2019) Structural variants exhibit widespread allelic heterogeneity and shape variation in complex traits. Nat Commun 10:4872

  • Charbonneau NL, Ono RN, Corson GM et al (2004) Fine tuning of growth factor signals depends on fibrillin microfibril networks. Birth Defects Res Part C Embryo Today Rev 72:37–50

    Article  CAS  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018) Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chiang C, Scott AJ, Davis JR et al (2017) The impact of structural variation on human gene expression. Nat Genet 49:692–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawood MAO, Koshio S (2018) Vitamin C supplementation to optimize growth, health and stress resistance in aquatic animals. Rev Aquac 10:334–350

    Article  Google Scholar 

  • de Melo CMR, Durland E, Langdon C (2016) Improvements in desirable traits of the Pacific oyster, Crassostrea gigas, as a result of five generations of selection on the West Coast, USA. Aquaculture 460:105–115

    Article  Google Scholar 

  • Dennis MY, Harshman L, Nelson BJ et al (2017) The evolution and population diversity of human-specific segmental duplications. Nat Ecol Evol 1:69

  • Dharmayanthi AB, Terai Y, Sulandari S et al (2017) The origin and evolution of fibromelanosis in domesticated chickens: genomic comparison of Indonesian Cemani and Chinese Silkie breeds. PLoS One 12:e0173147

  • Dorshorst B, Harun-Or-Rashid M, Bagherpoor AJ et al (2015) A genomic duplication is associated with ectopic eomesodermin expression in the embryonic chicken comb and two Duplex-comb phenotypes. PLoS Genet 11:e1004947

  • Duan P, Xu J, Zeng D et al (2017) Natural variation in the promoter of GSE5 contributes to grain size diversity in rice. Mol Plant 10:685–694

    Article  CAS  PubMed  Google Scholar 

  • Dyck JRB, Gao G, Widmer J et al (1996) Regulation of 5′-AMP-activated protein kinase activity by the noncatalytic β and γ subunits. J Biol Chem 271:17798–17803

    Article  CAS  PubMed  Google Scholar 

  • Evans S, Langdon C (2006) Direct and indirect responses to selection on individual body weight in the Pacific oyster (Crassostrea gigas). Aquaculture 261:546–555

    Article  Google Scholar 

  • Fukuwatari T, Shibata K (2013) Nutritional aspect of tryptophan metabolism. Int J Tryptophan Res 6:3–8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gansner JM, Madsen EC, Mecham RP, Gitlin JD (2008) Essential role for fibrillin-2 in zebrafish notochord and vascular morphogenesis. Dev Dyn 237:2844–2861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan P, Sung WK (2016) Structural variation detection using next-generation sequencing data: a comparative technical review. Methods 102:36–49

    Article  CAS  PubMed  Google Scholar 

  • Hardies K, De Kovel CGF, Weckhuysen S et al (2015) Recessive mutations in SLC13A5 result in a loss of citrate transport and cause neonatal epilepsy, developmental delay and teeth hypoplasia. Brain 138:3238–3250

    Article  PubMed  Google Scholar 

  • He Y, Luo X, Zhou B et al (2019) Long-read assembly of the Chinese rhesus macaque genome and identification of ape-specific structural variants. Nat Commun 10:4233

  • Hiruma K, Fukunaga S, Bednarek P et al (2013) Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs. Proc Natl Acad Sci USA 110:9589–9594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huerta-Cepas J, Forslund K, Coelho LP et al (2017) Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol 34:2115–2122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurles ME, Dermitzakis ET, Tyler-Smith C (2008) The functional impact of structural variation in humans. Trends Genet 24:238–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingle RA (2011) Histidine biosynthesis. Arabidopsis Book 9:e0141

  • Inoue K, Zhuang L, Ganapathy V (2002) Human Na+-coupled citrate transporter: primary structure, genomic organization, and transport function. Biochem Biophys Res Commun 299:465–471

    Article  CAS  PubMed  Google Scholar 

  • Jensen SA, Handford PA (2016) New insights into the structure, assembly and biological roles of 10–12 nm connective tissue microfibrils from fibrillin-1 studies. Biochem J 473:827–838

    Article  CAS  PubMed  Google Scholar 

  • Jin YL, Kong LF, Yu H, Li Q (2014) Development, inheritance and evaluation of 55 novel single nucleotide polymorphism markers for parentage assignment in the Pacific oyster (Crassostrea gigas). Genes and Genomics 36:129–141

    Article  CAS  Google Scholar 

  • Kim T, Seo HD, Hennighausen L et al (2018) Octopus-toolkit: a workflow to automate mining of public epigenomic and transcriptomic next-generation sequencing data. Nucleic Acids Res 46:e53

  • Kong L, Bai J, Li Q (2014) Comparative assessment of genomic SSR, EST-SSR and EST-SNP markers for evaluation of the genetic diversity of wild and cultured Pacific oyster Crassostrea gigas Thunberg. Aquaculture 420–421:S85-S91

  • Kosugi S, Momozawa Y, Liu X et al (2019) Comprehensive evaluation of structural variation detection algorithms for whole genome sequencing. Genome Biol 20:117

  • Kumari J, Sahoo PK (2005) High dietary vitamin C affects growth, non-specific immune responses and disease resistance in Asian catfish, Clarias batrachus. Mol Cell Biochem 280:25–33

  • Kurtz S, Phillippy A, Delcher AL et al (2004) Versatile and open software for comparing large genomes Genome Biol 5:R12

  • Le Floc’h N, Otten W, Merlot E, (2011) Tryptophan metabolism, from nutrition to potential therapeutic applications. Amino Acids 41:1195–1205

    Article  CAS  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A et al (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Li A, Song K et al (2018) Divergence and plasticity shape adaptive potential of the Pacific oyster. Nat Ecol Evol 2:1751–1760

    Article  PubMed  Google Scholar 

  • Li Q, Wang Q, Liu S, Kong L (2011) Selection response and realized heritability for growth in three stocks of the Pacific oyster Crassostrea gigas. Fish Sci 77:643–648

    Article  CAS  Google Scholar 

  • Li Q, Yu H, Yu R (2006) Genetic variability assessed by microsatellites in cultured populations of the Pacific oyster (Crassostrea gigas) in China. Aquaculture 259:95–102

    Article  CAS  Google Scholar 

  • Li X, Yang J, Shen M et al (2020) Whole-genome resequencing of wild and domestic sheep identifies genes associated with morphological and agronomic traits. Nat Commun 11:2815

  • Li Z, Li D, Choi EY et al (2017) Silencing of solute carrier family 13 member 5 disrupts energy homeostasis and inhibits proliferation of human hepatocarcinoma cells. J Biol Chem 292:13890–13901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Linster CL, Van Schaftingen E (2007) Vitamin C: biosynthesis, recycling and degradation in mammals. FEBS J 274:1–22

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Zhou Y, Rosen BD et al (2019) Diversity of copy number variation in the worldwide goat population. Heredity (edinb) 122:636–646

    Article  CAS  Google Scholar 

  • MacDonald JR, Ziman R, Yuen RKC et al (2014) The Database of Genomic Variants: a curated collection of structural variation in the human genome. Nucleic Acids Res 42:986–992

    Article  CAS  Google Scholar 

  • Mayans O, van der Ven PFM, Wilm M et al (1998) Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature 395:863–869

    Article  CAS  PubMed  Google Scholar 

  • Nattestad M, Schatz MC (2016) Assemblytics: a web analytics tool for the detection of variants from an assembly. Bioinformatics 32:3021–3023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ono RN, Sengle G, Charbonneau NL et al (2009) Latent transforming growth factor β-binding proteins and fibulins compete for fibrillin-1 and exhibit exquisite specificities in binding sites. J Biol Chem 284:16872–16881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powell S, Bidner TD, Payne RL, Southern LL (2011) Growth performance of 20- to 50-kilogram pigs fed low-crude-protein diets supplemented with histidine, cystine, glycine, glutamic acid, or arginine. J Anim Sci 89:3643–3650

    Article  CAS  PubMed  Google Scholar 

  • Qi H, Li L, Zhang G (2021) Construction of a chromosome-level genome and variation map for the Pacific oyster Crassostrea gigas. Mol Ecol Resour 21:1670-1685

  • Quinlan AR, Hall IM (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rausch T, Zichner T, Schlattl A et al (2012) DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics 28:333–339

    Article  CAS  Google Scholar 

  • Saha M, Mitsuhashi S, Jones MD et al (2017) Consequences of MEGF10 deficiency on myoblast function and Notch1 interactions. Hum Mol Genet 26:2984–3000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sealey WM, Gatlin DM (2002) Dietary vitamin C and vitamin E interact to influence growth and tissue composition of juvenile hybrid striped bass (Morone chrysops ♀ × M. saxatilis ♂) but have limited effects on immune responses1,2. J Nutr 132:748–755

    Article  CAS  PubMed  Google Scholar 

  • Sengle G, Charbonneau NL, Ono RN et al (2008) Targeting of bone morphogenetic protein growth factor complexes to fibrillin. J Biol Chem 283:13874–13888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simam J, Rono M, Ngoi J et al (2018) Gene copy number variation in natural populations of Plasmodium falciparum in Eastern Africa. BMC Genomics 19:372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stankiewicz P, Lupski JR (2010) Structural variation in the human genome and its role in disease. Annu Rev Med 61:437–455

    Article  CAS  PubMed  Google Scholar 

  • Takayama K, Mitsuhashi S, Shin JY et al (2016) Japanese multiple epidermal growth factor 10 (MEGF10) myopathy with novel mutations: a phenotype–genotype correlation. Neuromuscul Disord 26:604–609

  • Troost K (2010) Causes and effects of a highly successful marine invasion: case-study of the introduced Pacific oyster Crassostrea gigas in continental NW European estuaries. J Sea Res 64:145–165

    Article  Google Scholar 

  • Vacic V, McCarthy S, Malhotra D et al (2011) Duplications of the neuropeptide receptor gene VIPR2 confer significant risk for schizophrenia. Nature 471:499-503

  • Vlad D, Rappaport F, Simon M, Loudet O (2010) Gene transposition causing natural variation for growth in Arabidopsis thaliana. PLoS Genet 6:e1000945

  • Walton MJ, Coloso RM, Cowey CB et al (1984) The effects of dietary tryptophan levels on growth and metabolism of rainbow trout (Salmo gairdneri). Br J Nutr 51:279–287

  • Wang GD, Shao XJ, Bai B et al (2019) Structural variation during dog domestication: insights from gray wolf and dhole genomes. Natl Sci Rev 6:110–122. https://doi.org/10.1093/nsr/nwy076

  • Wang J, Li Q (2017) Characterization of novel EST-SNP markers and their association analysis with growth-related traits in the Pacific oyster Crassostrea gigas. Aquac Int 25:1707–1719

    Article  CAS  Google Scholar 

  • Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:e164

  • Weischenfeldt J, Symmons O, Spitz F, Korbel JO (2013) Phenotypic impact of genomic structural variation: insights from and for human disease. Nat Rev Genet 14:125–138

    Article  CAS  PubMed  Google Scholar 

  • Winder WW, Thomson DM (2007) Cellular energy sensing and signaling by AMP-activated protein kinase. Cell Biochem Biophys 47:332–347

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Cole JB, Bickhart DM et al (2014) Genome wide CNV analysis reveals additional variants associated with milk production traits in Holsteins. BMC Genomics 15:683

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang N, Liu J, Gao Q et al (2019) Genome assembly of a tropical maize inbred line provides insights into structural variation and crop improvement. Nat Genet 51:1052–1059

    Article  CAS  PubMed  Google Scholar 

  • Yu G, Wang L-G, Han Y, He Q-Y (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. Omi A J Integr Biol 16:284–287

    Article  CAS  Google Scholar 

  • Zhao X, Yu H, Kong L, Li Q (2012) Transcriptomic responses to salinity stress in the Pacific oyster Crassostrea gigas. PLoS One 7:e46244

  • Zhong X, Li Q, Yu H, Kong L (2013) Development and validation of single-nucleotide polymorphism markers in the Pacific Oyster, Crassostrea gigas, using high-resolution melting analysis. J World Aquac Soc 44:455–465

    Article  CAS  Google Scholar 

  • Zhou Y, Minio A, Massonnet M et al (2019) The population genetics of structural variants in grapevine domestication. Nat Plants 5:965–979

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the grants from the National Natural Science Foundation of China (Nos. 31802293, 41976098, and 31741122) and the Young Talent Program of Ocean University of China (No. 201812013).

Author information

Author notes

  1. Zexin Jiao and Yuan Tian contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Mariculture (Ocean University of China), Ocean University of China Ministry of Education College of Fisheries, Qingdao, 266003, China

    Zexin Jiao, Yuan Tian, Boyang Hu, Qi Li & Shikai Liu

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Qi Li & Shikai Liu

Authors
  1. Zexin Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuan Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Boyang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shikai Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shikai Liu.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiao, Z., Tian, Y., Hu, B. et al. Genome Structural Variation Landscape and Its Selection Signatures in the Fast-growing Strains of the Pacific Oyster, Crassostrea gigas. Mar Biotechnol 23, 736–748 (2021). https://doi.org/10.1007/s10126-021-10060-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-021-10060-5

Keywords

Search

Navigation