Skip to main content
Log in

Different resistance potential to reovirus in grass carp (Ctenopharyngodon idella) populations and their immune characteristics

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Our aim was to verify whether genes in the coagulation complement and cytokine interaction pathways are crucial to the resistance to grass carp hemorrhagic disease in grass carps (Ctenopharyngodon idella). To evaluate this, we acquired male grass carps with grass carp reovirus (GCRV) resistance, F1 generation, ordinary male fish, control F1 progenies (hybridized ordinary fish), and barbel chub (Squaliobarbus curriculus) as a positive control. We compared the expression variation of 13 immune factors in different tissues using real-time fluorescent quantitative PCR. Our results showed that the expression of the transforming growth factor-β3, nerve growth factor receptor, coagulation factor D, chemokine receptor XCR1, profibrinolysin, γ-globulin of complement component 1, complement component 2, and complement component 5 in the different tissues of the barbel chub were significantly higher than those in the grass carps populations under normal conditions. Except for a limited number of genes, their expression exhibited significant differences. There was no significant difference in these genes among grass carp populations with different GCRV resistance. These results indicate that the high gene expression in the coagulation complement and cytokine interaction pathways may be the main reason for the strong resistance of barbel chub to GCRV. However, high gene expression was not a factor affecting GCRV resistance between grass carp populations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data availability

Not applicable.

References

  • Aquaculture Research Group of Jianhu County of Jiangsu Province (1974) Hybrid test report of Ctenopharyngodon idellus (♀) × Erythroculter ilishae Formis (♂). Freshwater Fish 4(3):22–23

    Google Scholar 

  • Chen Y, Li J, Shen Y (2013) Cloning and expression of C1qC gene in grass carp (Ctenopharyngodon idella). J Fish Sci China 20:25–34

    Google Scholar 

  • Fish and Fisheries Administration of Ministry of Agriculture and Rural Affairs of the People’s Republic of China, National Aquatic Technology Promotion Terminal of China, Chinese Society of Fisheries (2019) 2019 China Fisheries Statistics Yearbook. Chinese Agriculture Press, Beijing

    Google Scholar 

  • He M, Xiao T, Liu Q, Li D, Li W, Deng Y (2015) Morphological characteristics andlysis of Ctenopharyngodon idellus, Squaliobarbus curriculus and their reciprocal hybrids F1. J Hunan Univ Arts Sci (Sci Technol) 27(4):36–42

    Google Scholar 

  • Jalili A, Marquez-Curtis L, Montano J, Shirvaikar N, Ratajczak MZ, Janowska-Wiezorek A et al (2006) A novel role of complement components C1q and C5a in hematopoietic stem/progenitor cell migration. Blood 108:4169. https://doi.org/10.1182/blood.V108.11.4169.4169

    Article  Google Scholar 

  • Jiang H, Liu S, Xiao TY, Cao YK, Xie M, Yin ZF (2019) Cellular biological and eumelanin-related gene expressional bases of pigment deviation of Leptobotia taeniops. Appl Ecol Environ Res 17:12181–12189. https://doi.org/10.15666/aeer/1705_1218112189

    Article  Google Scholar 

  • Li Y, Mao S (1990) Establishment of grass carp cell line AHZC88 resistant to hemorrhagic disease virus by UV mutagenesis. J Fish China 14(2):89–93

    Google Scholar 

  • Liao Z, Wan Q, Yuan G, Su J (2019) The systematic identification and mRNA expression profiles post viral and bacterial challenge of complement system in grass carp Ctenopharyngodon idella. Fish Shellfish Immun 86:107–115. https://doi.org/10.1016/j.fsi.2018.11.032

    Article  CAS  Google Scholar 

  • Liang HR, Li YG, Zeng WW, Wang YY, Wang Q, Wu SQ (2014) Pathogenicity and tissue distribution of grass carp reovirus after intraperitoneal administration. Virol J 11:178. https://doi.org/10.1186/1743-422X-11-178

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Xiao T, Liu M, Zhou W (2012) Research progress of biology in Squaliobarbus curriculus. Fish Sci 31(11):687–691

    CAS  Google Scholar 

  • Lv LG, Xu Y, Xu BH, Liu QL, Xiao TY, Liu Y, Su H (2020) Molecular mechanism of growth diversity for the first hybrid generation individuals of grass carp (Ctenopharyngodon idellus) (♀) × barbel chub (Squaliobarbus curriculus) (♂). Appl Ecol Environ Res 18:1151–1159. https://doi.org/10.15666/aeer/1801_11511159

    Article  Google Scholar 

  • Ni J, Yan Q, Yu Y, Zhang T (2014) Factors influencing the grass carp gut microbiome and its effect on metabolism. FEMS Microbiol Ecol 87:704–714. https://doi.org/10.1111/1574-6941.12256

    Article  CAS  PubMed  Google Scholar 

  • Ni JJ, Li XJ, Chen F, Wu HH, Xu MY (2018) Community structure and potential nitrogen metabolisms of subtropical aquaculture pond microbiota. Appl Ecol Environ Res 16:7687–7697. https://doi.org/10.15666/aeer/1606_76877697

    Article  Google Scholar 

  • Peng H, Liu M, Liu Q, Xiao T, Sun J, Xu B, Liu Y (2014) Molecular cloning and tissue expression analysis of Mx gene in Squaliobarbus curriculus. Acta Hydrobiologica Sinica 38:993–1001. https://doi.org/10.7541/2014.147

    Article  CAS  Google Scholar 

  • Scapigliati G, Bird S, Secombes CJ (2000) Invertebrate and fish cytokines. Eur Cytokine Netw 11(3):354–361

    CAS  PubMed  Google Scholar 

  • Savan R, Sakai M (2006) Genomics of fish cytokines. Comp Biochem Physiol D 1:89–101. https://doi.org/10.1016/j.cbd.2005.08.005

    Article  CAS  Google Scholar 

  • Secombes CJ, Hardie LJ, Daniels G (1996) Cytokines in fish: an update. Fish Shellfish Immun 6:291–304. https://doi.org/10.1006/fsim.1996.0030

    Article  Google Scholar 

  • Tang X, Fu Y, Zhao Y, Pi J, Wang H (2020) Dietary α-ketoglutarate supplementation alleviates harmful effects of high environmental ammonia on grass carp, Ctenopharyngodon idella. Aquac Res 51:1182–1189. https://doi.org/10.1111/are.14469

    Article  CAS  Google Scholar 

  • Wang H, Ding C, Wang J, Zhao X, Jin S, Liang J, Luo H, Li D, Li R, Li Y, Xiao T (2019) Molecular cloning and expression analysis of coagulation factor VIII and plasminogen involved in immune response to GCRV, and immunity activity comparison of grass carp Ctenopharyngodon idella with different viral resistance. Fish Shellfish Immun 86:794–804. https://doi.org/10.1016/j.fsi.2018.12.024

    Article  CAS  Google Scholar 

  • Wang Z, Zhang S, Wang G (2008) Advances on the complement components, characteristic and function of complement system in fish. Acta Hydrobiologica Sinica 32:760–769. https://doi.org/10.3724/SP.J.0000.2008.50760

    Article  CAS  Google Scholar 

  • Xiong L, He L, Luo L, Li Y, Liao L, Huang R, Zhu Z, Wang Y (2018) Global and complement gene-specific DNA methylation in grass carp after grass carp reovirus (GCRV) infection. Int J Mol Sci 19:1110. https://doi.org/10.3390/ijms19041110

    Article  CAS  PubMed Central  Google Scholar 

  • Xu B (2012) Comparative transcriptome analysis of spleen of infected grass carp (Ctenopharyngodon idellus). Hunan Agricultural University, Changsha

    Google Scholar 

  • Xu BH, Zhong L, Liu QL, Xiao TY, Su JM, Chen KJ, Wang HQ, Dai YJ, Chen J (2016) Characterization of grass carp spleen transcriptome during GCRV infection. Genet Mol Res 15: gmr.15026650. https://doi.org/10.4238/gmr.15026650

  • Zeng W, Wang Y, Liang H, Liu C, Song X, Shi C, Wu S, Wang Q (2014) A one-step duplex rRT-PCR assay for the simultaneous detection of grass carp reovirus genotypes I and II. J Virol Methods 210C:32–35. https://doi.org/10.1016/j.jviromet.2014.08.024

    Article  CAS  Google Scholar 

  • Zhang H, Zhang X, He T, Chen L, Chen T, Xiao T, Li J (1997) Transfer of exogenous DNA into fertilized eggs of grass carp by sperm vector method. J Fish China 21:74–76

    Google Scholar 

  • Zhang YB, Jiang J, Chen YD, Zhu R, Shi Y, Zhang QY, Gui JF (2007) The innate immune response to grass carp hemorrhagic virus (GCHV) in cultured Carassius auratus blastulae (CAB) cells. Dev Comp Immunol 31:232–243

    Article  CAS  Google Scholar 

  • Zhu Z, Li G, He L, Chen S (1985) Novel gene transfer into the fertilized eggs of gold fish (Carassius auratus. L. 1758). J Appl Ichthyol 1:31–34

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank anonymous technicians at Guangdong Meilikang Bio-Science Ltd., China, for assistance with data re-analysis and figure preparation.

Funding

This study was funded by the National Key R & D Program of China (No. 2018YFD0900302).

Author information

Authors and Affiliations

Authors

Contributions

Hongquan Wang, Hong Yang, and Tiaoyi Xiao contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Hongquan Wang, Hong Yang, Rui Li, and Yaoguo Li. The first draft of the manuscript was written by Hongquan Wang and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Tiaoyi Xiao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

All experiments were approved by the Animal Care and Use Committee of Hunan Agricultural University (approval number: 2013008) and performed in accordance with approved protocols.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Code availability

Not applicable.

Additional information

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, H., Yang, H., Li, R. et al. Different resistance potential to reovirus in grass carp (Ctenopharyngodon idella) populations and their immune characteristics. Aquacult Int 29, 253–260 (2021). https://doi.org/10.1007/s10499-020-00623-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-020-00623-z

Keywords

Navigation