Skip to main content
Log in

Molecular cloning, characterization, and expression patterns of the hatching enzyme genes during embryonic development of pikeperch (Sander lucioperca)

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Hatching enzyme (HE) is the most critical enzyme in the process of fish hatching. Pikeperch, Sander lucioperca, is one of economical and ferocious fish with long embryonic incubation and its long and irregular hatching time easily leads to the decrease of its fingerlings due to cannibalism. HE is one of the most important factors that affect the membrane effusion of fish eggs during incubation. The present study aimed to clone HE genes and to reveal the HE expression patterns of pikeperch during its hatching process. In this study, the full-length cDNAs of high choriolytic enzyme gene (HCE) and low choriolytic enzyme gene (LCE) from pikeperch were cloned and their expressions were performed using qRT-PCR and in situ hybridization. The results showed that the full-length cDNAs of HCE and LCE were comprised of 1189 bp and 1147 bp, respectively, and the open reading frames (ORFs) obtained were 876 bp and 798 bp, encoded proteins of 291 and 265 amino acids, respectively. Phylogenetic analysis showed high homology of HE in Percidae, far from amphibians, birds, and insects. HE genes maintained high expression from body segment appearance stage to hatching stage, and low expression in early embryo and larval stage of pikeperch. HE transcripts were initially detectable at body segment appearance stage in the head region and on the surface of the yolk sac. At hatching stage, strong staining was observed in the whole body from head to the tail. Compared with other fishes, the special spatiotemporal expression pattern of hatching enzyme may be the key factor leading to the irregular hatching time of pikeperch. Our study might enhance our understanding of the hatching mechanism of pikeperch.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Chakraborty T, Mohapatra S, Tobayama M, Ohta K, Ryu YW, Kazeto Y, Ohtak K, Zhou LY, Nagahama Y, Matsubara T (2017) Hatching enzymes disrupt aberrant gonadal degeneration by the autophagy/apoptosis cell fate decision. Sci Rep 7(1):3183

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu W, Zhang JP, Xu WT, He S, Long MD, Liao QQ, Liu JH, Peng LY, Liu WB, Xiao YM (2021) Characteristics of hatching enzymes and egg envelope in cross progenies from crucian carp (Carassius auratus var.) and zebrafish (Barchydanio rerio var.). Reprod Breed 1:2

    Google Scholar 

  • Geier G, Zwilling R (1998) Cloning and characterization of a cDNA coding for Astacus embryonic astacin, a member of the astacin family of metalloproteases from the crayfish (Astacus astacus). Eur J Biochem 253(3):796–803

    Article  CAS  PubMed  Google Scholar 

  • Guo JQ, Li CJ, Teng T, Shen FF, Chen YN, Wang YF, Pan CL, Ling QF (2018) Construction of the first high-density genetic linkage map of pikeperch (Sander lucioperca) using specific length amplified fragment (SLAF) sequencing and QTL analysis of growth-related traits. Aquaculture 497:299–305

    Article  CAS  Google Scholar 

  • He J, Liang YJ, Xie CH, Qiao HC, Xu P (2017) Expression patterns of the hatching enzyme genes during embryonic development of tilapia. Aquaculture 479:845–849

    Article  CAS  Google Scholar 

  • Hiroi J, Maruyama K, Kawazu K, Kaneko T, Ohtani-Kaneko R, Yasumasu S (2004) Structure and developmental expression of hatching enzyme genes of the Japanese eel Anguilla japonica: an aspect of the evolution of fish hatching enzyme gene. Dev Genes Evol 214:176–184

    Article  CAS  PubMed  Google Scholar 

  • Inohaya K, Yasumasu S, Ishimaru M, Ohyama A, Iuchi I, Yamagami K (1995) Temporal and spatial patterns of gene expression for the hatching enzyme in the teleost embryo, Oryzias Latipes. Dev Biol 171(2):374–385

    Article  CAS  PubMed  Google Scholar 

  • Inohaya K, Yasumasu S, Araki K, Naruse K, Yamazaki K, Yasumasu I, Iuchi I, Yamagami K (1997) Species-dependent migration of fish hatching gland cells that commonly express astacin-like proteases in common. Dev Growth Differ 39(2):191–197

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi M, Yasumasu S, Hiroi J, Naruse K, Suzuki T, Iuchi I (2007) Analysis of the exon–intron structures of fish, amphibian, bird and mammalian hatching enzyme genes, with special reference to the intron loss evolution of hatching enzyme genes in Teleostei. Gene 392(1–2):77–88

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi M, Nakagawa M, Noda T, Yoshizaki N, Hiroi J, Nishida M, Iuchi I, Yasumasu S (2008) Hatching enzyme of the ovoviviparous black rockfish Sebastes schlegelii - environmental adaptation of the hatching enzyme and evolutionary aspects of formation of the pseudogene. FEBS J 275(11):2884–2898

    Article  CAS  PubMed  Google Scholar 

  • Kawaguchi M, Hiroi J, Miya M, Nishida M, Iuchi I, Yasumasu S (2010) Intron-loss evolution of hatching enzyme genes in Teleostei. BMC Evol Biol 10:260. https://doi.org/10.1186/1471-2148-10-260

  • Kawaguchi M, Okazawa Y, Imafuku A, Nakano Y, Shimizu R, Ishizuka R, Jiang T, Nagasawa T, Hiroi J, Yasumasu S (2021) Pactacin is a novel digestive enzyme in teleosts. Sci Rep 11:7230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kimmel CB, Warga RM, Schilling TF (1990) Origin and organization of the zebrafish fate map. Development 108(4):581–594

    Article  CAS  PubMed  Google Scholar 

  • Kudo N, Yasumasu S, Iuchi I, Tanokura M (2004) Crystallization and preliminary X- ray analysis of HCE-1, a hatching enzyme of medaka fish, Oryzias latipes. Acta Crystallogr D Biol Crystallogr 60:725–726

    Article  PubMed  Google Scholar 

  • Lee KS, Yasumasu S, Nomura K, Iuchi I (1994) HCE, a constituent of the hatching enzymes of Oryzias latipes embryos, releases unique proline-rich polypeptides from its natural substrate, the hardened chorion. FEBS Lett 339(3):281–284

    Article  CAS  PubMed  Google Scholar 

  • Li CJ, Wang YF, Wang GC, Chen YN, Guo JQ, Pan CL, Liu EG, Ling QF (2019) Physicochemical changes in liver and Hsc70 expression in pikeperch Sander lucioperca under heat stress. Ecotoxicol Environ Saf 181:130–137

    Article  PubMed  Google Scholar 

  • Nagasawa T, Kawaguchi M, Nishi K, Yasumasu S (2022) Molecular evolution of hatching enzymes and their paralogous genes in vertebrates. BMC Ecol Evol 22(1):9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang S, Wu J, Zhao X, Wang H, Qiu Z, Shen X, Guo X (2012) Molecular cloning and characterization of hatching enzyme-like geneII (BmHELII) in the silkworm. Bombyx Mori Biochem Biophys Res Commun 419(2):194–199

    Article  CAS  PubMed  Google Scholar 

  • Yasumasu S, Iuchi I, Yamagami K (1989) Purification and partial characterization of high choriolytic enzyme (HCE), a component of the hatching enzyme of the Teleost, Oryzias Latipes. J Biochem 105(2):204–211

    Article  CAS  PubMed  Google Scholar 

  • Yasumasu S, Yamada K, Akasaka K, Mitsunaga K, Iuchi I, Shimada H, Yamagami K (1992) Isolation of cDNAs for LCE and HCE, two constituent proteases of the hatching enzyme of Oryzias latipes, and concurrent expression of their mRNAs during development. Dev Biol 153(2):250–258

    Article  CAS  PubMed  Google Scholar 

  • Yasumasu S, Shimada H, Inohaya K, Yamazaki K, Luchi I, Yasumasu I, Yamagami K (1996) Different exon-intron organizations of the genes for two astacin-like proteases, high choriolytic enzyme (choriolysin H) and low choriolytic enzyme (choriolysin L), the constituents of the fish hatching enzyme. Eur J Biochem 237(3):752–758

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zhang B, Kawaguchi M, Lin Q (2021) Effects of hatching enzymes on egg envelope digestion in the male-brooding seahorse. Mol Reprod Dev 88(6):459–470

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the Scientific Fund of Jiangsu Province (BY2015039-10), the Aquatic Three Project of Jiangsu Province (Y2017-37), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Authors and Affiliations

Authors

Contributions

Chenglong Pan; conceptualization, data curation, formal analysis, investigation, methodology, visualization, writing—original draft, writing—review and editing

Lingling Li; data curation, investigation, methodology, writing—review and editing

Hao Zhu; data curation, formal analysis, investigation, methodology

Wenjia Mao; data curation, formal analysis, investigation, methodology

Tao Han; data curation, formal analysis, investigation

Xuqian Zhao; Data curation, Investigation

Caijuan Li; data curation, investigation

Qufei Ling; conceptualization, funding acquisition, project administration, resources, supervision, validation, writing—review and editing

Corresponding author

Correspondence to Qufei Ling.

Ethics declarations

Ethics approval and consent to participate

All experiments performed on animals in this study were in accordance with the ethical guidelines of Soochow University on the care and use of experimental animals.

Human and animal ethics

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Handling Editor: Pierre Boudry

Publisher's note

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

Chenglong Pan and Lingling Li are co-first authors.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, C., Li, L., Zhu, H. et al. Molecular cloning, characterization, and expression patterns of the hatching enzyme genes during embryonic development of pikeperch (Sander lucioperca). Aquacult Int 31, 915–930 (2023). https://doi.org/10.1007/s10499-022-01006-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-022-01006-2

Keywords

Navigation