Skip to main content

Advertisement

Log in

Delta of Exopalaemon carinicauda: molecular characterization, expression in different tissues and developmental stages, and its SNPs association analysis with development

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Background

The Notch signaling pathway plays a significant role in the gene regulatory network of development of vertebrate and invertebrate. However, as a ligand for the Notch signaling pathway, the mechanism of Delta in the development of Exopalaemon carinicauda is still unclear.

Methods and results

The Delta’s molecular characteristics, tissue distribution and their association with development in E. carinicauda were studied by RACE (rapid amplification of cDNA end), qRT-PCR (quantitative Real-time PCR) and SNP (single nucleotide polymorphism), respectively. The delta in E. carinicauda had a full-length cDNA of 2807 bp and its Delta of 808 amino-acid residue had the highest identity with the Delta of Homarus americanus (identity = 76.63%). Delta had the highest expression in the ovary, and its expression varied with different stages of embryonic, larval, and ovarian development. After delta RNA interference (with a highest interference efficiency of 66% at 24 h), the expression of Notch signaling pathway genes and developmental related genes was significantly reduced, and the ovarian development was significantly delayed. Further study found that there were 4 SNPs (ds1-4) in delta cDNA, of which two (ds2 T1521G caused a mutation Asn422Lys and ds3 G1674A caused a mutation Tyr473Cys in the EGF-like domain) were associated with the development of E. carinicauda. The Gonadosomatic Index (GSI) of the ds2 TT genotypes was 37.28% and 134.60% higher than E. carinicauda of GT and GG genotype respectively (P < 0.05).

Conclusion

Our research indicated that delta was involved in the development of E. carinicauda and provided new insights for molecular breeding with SNP markers in E. carinicauda.

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

Similar content being viewed by others

Data availability

The data generated in this study are available from the corresponding author on reasonable request.

References

  1. Pei Z, Baker N (2008) Competition between delta and the Abruptex domain of Notch. BMC Dev Biol 8(1):4. https://doi.org/10.1186/1471-213X-8-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Richards GS, Degnan BM (2012) The expression of delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for notch signaling in metazoan development. EvoDevo 3:15. https://doi.org/10.1186/2041-9139-3-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lai X, Chen H, Mi X, Shen S, Gao H (2023) Molecular characterization and developmental function of jagged-1 in Exopalaemon carinicauda (Decapoda, Caridea, Palaemonidae). Crustaceana 96(7):683–702. https://doi.org/10.1163/15685403-bja10301

    Article  Google Scholar 

  4. Liao B, Oates CA (2016) Delta-Notch signalling in segmentation. Arthropod Struct Dev 46(3):429–447. https://doi.org/10.1016/j.asd.2016.11.007

    Article  PubMed  Google Scholar 

  5. Medwig-Kinney TN, Sirota SS, Gibney TV, Pani AM, Matus DQ (2022) An in vivo toolkit to visualize endogenous LAG-2/delta and LIN-12/Notch signaling in C. elegans. Micro Publ Biol 2022:602. https://doi.org/10.17912/micropub.biology.000602

    Article  Google Scholar 

  6. Revinski RD, Paganelli RA, Carrasco EA, López SL (2010) Delta-Notch signaling is involved in the segregation of the three germ layers in Xenopus laevis. Dev Biol 339(2):477–492. https://doi.org/10.1016/j.ydbio.2010.01.010

    Article  CAS  PubMed  Google Scholar 

  7. Zhao X, Guo S (2023) Antibody uptake assay for tracking notch/delta endocytosis during the asymmetric division of zebrafish radial glia progenitors. J Vis Exp 191:65030. https://doi.org/10.3791/65030

    Article  CAS  Google Scholar 

  8. Horita N, Keeley TM, Hibdon ES, Delgado E, Lafkas D, Siebel CW, Samuelson LC (2022) Delta-like 1-expressing cells at the gland base promote proliferation of gastric antral stem cells in mouse. Cell Mol Gastroenterol Hepatol 13(1):275–287. https://doi.org/10.1016/j.jcmgh.2021.08.012

    Article  CAS  PubMed  Google Scholar 

  9. Shi Z, He F, Wang L, Liang Y, Han H, Wang C, Zhao Q, Geng X (2008) Expression, refolding, and purification of a truncated human deltalike1, a ligand of Notch receptors. Protein Expres Purif 59:242–248. https://doi.org/10.1016/j.pep.2008.02.004

    Article  CAS  Google Scholar 

  10. LeComte M, Wesley UV, Mok L, Shepherd A, Wesley C (2006) Evidence for the involvement of dominant-negative Notch molecules in the normal course of Drosophila development. Dev Dynam 235:411. https://doi.org/10.1002/dvdy.20650

    Article  CAS  Google Scholar 

  11. Mok L, Qin T, Bardot B, LeComte M, Homayouni A, Ahimou F, Wesley C (2005) Delta activity independent of its activity as a ligand of notch. BMC Dev Biol 5(1):6. https://doi.org/10.1186/1471-213X-5-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kainz F, Ewen-Campen B, Akam M, Extavour CG (2011) Notch/delta signaling is not required for segment generation in the basally branching insect Gryllus bimaculatus. Development 138(22):5015–5026. https://doi.org/10.1242/dev.073395

    Article  CAS  PubMed  Google Scholar 

  13. Condorelli AG, El Hachem M, Zambruno G, Nystrom A, Candi E, Castiglia D (2021) Notching up knowledge on molecular mechanisms of skin fibrosis: focus on the multifaceted Notch signalling pathway. J Biomed Sci 28(1):36. https://doi.org/10.1186/s12929-021-00732-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhou H, Zhao W, Zheng Z, Aweya JJ, Zhang Y, Zhu J, Zhao Y, Chen X, Yao D (2021) The Notch receptor-ligand delta is involved in the immune response of Penaeus vannamei. Dev Comp Immunol 125:104147. https://doi.org/10.1016/j.dci.2021.104147

    Article  CAS  PubMed  Google Scholar 

  15. Deng S, Yan X, Liang L, Wang L, Liu Y, Duan J, Yang Z, Chang T, Ruan B, Zheng Q, Han H (2017) The Notch ligand delta-like 3 promotes tumor growth and inhibits Notch signaling in lung cancer cells in mice. Biochem Bioph Res Co 483:488–494. https://doi.org/10.1016/j.bbrc.2016.12.117

    Article  CAS  Google Scholar 

  16. Bardot B, Mok L, Thayer T, Ahimou F, Wesley C (2005) The Notch amino terminus regulates protein levels and Delta-induced clustering of Drosophila Notch receptors. Exp Cell Res 304:202–223. https://doi.org/10.1016/j.yexcr.2004.10.030

    Article  CAS  PubMed  Google Scholar 

  17. Chipman AD, Akam M (2008) The segmentation cascade in the centipede Strigamia maritima: involvement of the Notch pathway and pair-rule gene homologues. Dev Biol 319:160–169. https://doi.org/10.1016/j.ydbio.2008.02.038

    Article  CAS  PubMed  Google Scholar 

  18. Oda H, Nishimura O, Hirao Y, Tarui H, Agata K, Akiyama-Oda Y (2007) Progressive activation of Delta-Notch signalling from around the blastopore is required to set up a functional caudal lobe in the spider Achaearanea tepidariorum. Development 134:2195–2205. https://doi.org/10.1242/dev.004598

    Article  CAS  PubMed  Google Scholar 

  19. Chesebro JE, Pueyo JI, Couso JP (2012) Interplay between a Wnt-dependent organizer and the Notch segmentation clock regulates posterior development in Periplaneta americana. Biol Open 2:227–237. https://doi.org/10.1242/bio.20123699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Eriksson BJ, Ungerer P, Stollewerk A (2013) The function of Notch signalling in segment formation in the crustacean Daphnia magna (Branchiopoda). Dev Biol 383:321–330. https://doi.org/10.1016/j.ydbio.2013.09.021

    Article  CAS  PubMed  Google Scholar 

  21. Janssen R, Budd GE (2016) Gene expression analysis reveals that Delta/Notch signalling is not involved in onychophoran segmentation. Dev Genes Evol 226(2):69–77. https://doi.org/10.1007/s00427-016-0529-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Udolph G, Rath P, Tio M, Toh J, Fang W, Pandey R, Technau GM, Chia W (2009) On the roles of Notch, Delta, kuzbanian, and inscuteable during the development of Drosophila embryonic neuroblast lineages. Dev Biol 336:156–168. https://doi.org/10.1016/j.ydbio.2009.09.030

    Article  CAS  PubMed  Google Scholar 

  23. Lai X, Chen J, Liang S, Chen H, Liu S, Gao H (2023) Effects of the probiotic Psychrobacter sp. B6 on the growth, digestive enzymes, antioxidant capacity, immunity, and resistance of Exopalaemon carinicauda to Aeromonas hydrophila. Probiotics Antimicro 15:813–820. https://doi.org/10.1007/s12602-022-09919-3

    Article  CAS  Google Scholar 

  24. Shen S, Mi X, Shen Q, Chen J, Gao H, Lai X (2023) Isolation and characterization of the actinomycete, Nocardiopsis, from Haizhou Bay, and its application as a probiotic for Exopalaemon carinicauda (Holthuis, 1950) (Caridea, Palaemonidae). Crustaceana 96:55–72. https://doi.org/10.1163/15685403-bja10266

    Article  Google Scholar 

  25. Jiang H, Li Y, Li W, Duan C, Xu J, Baloch WA, Yu F, Gao H (2022) Analysis on the infecting ability of different concentrations of Enterocytozoon hepatopenaei (Microsporidia, Microsporea, Chytridiopsida) in Exopalaemon carinicauda (Decapoda, Caridea, Palaemonidae). Crustaceana 95:1231–1246. https://doi.org/10.1163/15685403-bja10257

    Article  Google Scholar 

  26. Jiang H, Li Y, Xu J, Li W, Baloch W, Yu F, Mu H, Gao H (2023) Effect of exogenous nitric oxide on Enterocytozoon hepatopenaei copy numbers and immunity of Exopalaemon carinicauda. Aquac Res Online First. https://doi.org/10.1155/2023/2250046

    Article  Google Scholar 

  27. Hu G, Wang W, Xu K, Wang C, Liu D, Xu J, Yan B, Ji N, Gao H (2023) Transcriptomic and metabolomic analyses of Palaemon carinicauda hepatopancreas in response to Enterocytozoon hepatopenaei (EHP) infection. Fishes 8(2):92. https://doi.org/10.3390/fishes8020092

    Article  Google Scholar 

  28. Hua S, Yu F, Li Y, Liu X, Shi T, Zhang P, Li W, Baloch WA, Yan B, Gao H (2023) The ubiquitin-like, containing PHD and RING finger domains 1 (uhrf1) gene promotes ovarian development in Exopalaemon carinicauda. Aquacult Repts 29:101492. https://doi.org/10.1016/j.aqrep.2023.101492

    Article  Google Scholar 

  29. Shen S, Hu J, Shen Q, Chen H, Gao H, Lai X (2023) Cloning of notch1 and its role in the growth and development of Exopalaemon carinicauda. Aquacult Rep 30:101537. https://doi.org/10.1016/j.aqrep.2023.101537

    Article  Google Scholar 

  30. Pang Z, Zhao Z, Li Y, Sun Y, Duan C, Yan B, Baloch WA, Zhou Q, Gao H (2022) Effects of different sex ratios on the growth and ovarian development of the ridgetail white shrimp Exopalaemon carinicauda. Aquacult Rep 27:101419. https://doi.org/10.1016/j.aqrep.2022.101419

    Article  Google Scholar 

  31. Liu S, Jiang H, Qin F, Hu J, Lai X, Zhang Q, Gao H (2022) Effects of different illumination on the growth, digestion, and nonspecific immune-related enzyme activities of Exopalaemon carinicauda. Marine Sci 46(4):114–122. https://doi.org/10.11759/hykx20210209001

    Article  Google Scholar 

  32. Wang LH, Shen NN, Jiang HY, Ouyang LF, Zhang QQ, Hu GW, Wang PP, Gao H (2022) Effects of live food combinations on the metamorphosis and larval development of Exopalaemon carinicauda. Prog Fish Sci 43(4):171–179. https://doi.org/10.19663/j.issn2095-9869.20210317003

    Article  CAS  Google Scholar 

  33. Fasoulakis Z, Daskalakis G, Theodora M, Antsaklis P, Sindos M, Diakosavvas M, Angelou K, Loutradis D, Kontomanolis E (2021) The relevance of Notch signaling in cancer progression. Adv Exp Med Biol 1287:169–181. https://doi.org/10.1007/978-3-030-55031-8_11

    Article  CAS  PubMed  Google Scholar 

  34. Khait I, Orsher Y, Golan O, Binshtok U, Gordon-Bar N, Amir-Zilberstein L, Sprinzak D (2016) Quantitative analysis of Delta-like 1 membrane dynamics elucidates the role of contact geometry on Notch Signaling. Cell Rep 14:225–233. https://doi.org/10.1016/j.celrep.2015.12.040

    Article  CAS  PubMed  Google Scholar 

  35. Bland CE, Kimberly P, Rand MD (2003) Notch-induced proteolysis and nuclear localization of the Delta ligand. J Biol Chem 278(16):13607–13610. https://doi.org/10.1074/jbc.C300016200

    Article  CAS  PubMed  Google Scholar 

  36. Ferreira A, Lamy M, Rocha MM, Silva G, Bandeiras TM, Barbas A (2018) Production and characterization of a novel Delta-like 1 functional unit as a tool for Notch pathway activation and generation of a specific antibody. Protein Expres Purif 146:8–16. https://doi.org/10.1016/j.pep.2018.01.008

    Article  CAS  Google Scholar 

  37. Fontana JR, Posakony JW (2009) Both inhibition and activation of Notch signaling rely on a conserved Neuralized-binding motif in Bearded proteins and the Notch ligand Delta. Dev Biol 333(2):373–385. https://doi.org/10.1016/j.ydbio.2009.06.039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Wesley CS, Saez L (2000) Notch responds differently to Delta and Wingless in cultured Drosophila cells. J Biol Chem 275(13):9099–9101. https://doi.org/10.1074/jbc.275.13.9099

    Article  CAS  PubMed  Google Scholar 

  39. Thamm K, Seaver EC (2008) Notch signaling during larval and juvenile development in the polychaete annelid Capitella sp. I Dev Biol 320(1):304–318. https://doi.org/10.1016/j.ydbio.2008.04.015

    Article  CAS  PubMed  Google Scholar 

  40. Jiang YH, Yan SF (2004) Cytochemical studies on oogenesis of Penaeus vannamei. Chin J Zool 9(2):116–121. https://doi.org/10.1007/s00427-016-0529-4

    Article  CAS  Google Scholar 

  41. Bordonaro M, Tewari S, Atamna W, Lazarova DL (2011) The Notch ligand Delta-like 1 integrates inputs from TGFbeta/Activin and Wnt pathways. Exp Cell Res 317:1368–1381. https://doi.org/10.1016/j.yexcr.2011.03.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Stupnikov MR, Yang Y, Mori M, Lu J, Cardoso WV (2019) Jagged and Delta-like ligands control distinct events during airway progenitor cell differentiation. Elife 8:50487. https://doi.org/10.7554/eLife.50487

    Article  Google Scholar 

  43. Hirano KI, Suganami A, Tamura Y, Yagita H, Habu S, Kitagawa M, Sato T, Hozumi K (2020) Delta-like 1 and Delta-like 4 differently require their extracellular domains for triggering Notch signaling in mice. Elife 9:50979. https://doi.org/10.7554/eLife.50979

    Article  Google Scholar 

  44. Lai XF, Shi TT, Chen H, Shen SR, Gao H, Wu GT (2022) Identification and functional characterization of WNT5 in ovarian maturation of Exopalaemon carinicauda (Holthuis, 1950) (Caridea, Palaemonidae). Crustaceana 95:943–960. https://doi.org/10.1163/15685403-bja10228

    Article  Google Scholar 

  45. Zhang P, Hua S, Li Y, Zhang S, Liu X, Shi T, Wang P, Yan B, Li J, Gao H (2022) Expression of the cyclin-dependent kinase 2 gene (cdk2) influences ovarian development in the ridgetail white prawn Exopalaemon carinicauda. Aquacult Rep 25:101265. https://doi.org/10.1016/j.aqrep.2022.101265

    Article  Google Scholar 

  46. Janpoom S, Kaewduang M, Prasertlux S, Rongmung P, Ratdee O, Lirdwitayaprasit T, Klinbunga S, Khamnamtong B (2020) A SNP of the hemocyanin gene (LvHc) is a marker for high growth and ammonia-tolerance in Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 106:491–501. https://doi.org/10.1016/j.fsi.2020.07.058

    Article  CAS  PubMed  Google Scholar 

  47. Lander ES (1996) The new genomics: global views of biology. Science 274(5287):536–539. https://doi.org/10.1126/science.274.5287.536

    Article  CAS  PubMed  Google Scholar 

  48. Liu H, Zhang W, Wang M, Xu S, Zhong L, Bian W, Zhang S, Chen X (2023) Characterization of rrp44 gene in channel catfish (Ictalurus punctatus): molecular cloning, tissue distribution, and single nucleotide polymorphisms (SNPs) association analysis with growth traits. Aquacult Rep 30:101613. https://doi.org/10.1016/j.aqrep.2023.101613

    Article  Google Scholar 

  49. Hartley DA, Xu TA, Artavanis-Tsakonas S (1987) The embryonic expression of the Notch locus of Drosophila melanogaster and the implications of point mutations in the extracellular EGF-like domain of the predicted protein. EMBO J 6(11):3407–3417. https://doi.org/10.1002/j.1460-2075.1987.tb02664.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ekaterina S, Thomas K (2021) The role of ligand endocytosis in notch signaling. Biol Cell 113(10):401–418. https://doi.org/10.1111/BOC.202100009

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Jiangsu Ocean University, Jiangsu Key Laboratory of Marine Bioresources and Environment, Co-Innovation Center of Jiangsu Marine Bio-industry Technology, and The Jiangsu Provincial Platform for Conservation and Utilization of Agricultural Germplasm for their support in experiment instruments and funds.

Funding

This work was supported by Project of Seed-industry Revitalization from the Department of Agriculture and Rural Affairs of Jiangsu Province (JBGS(2021)124), Industry-University-Research Collaboration Fund (JOUH23147), Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by XL, SS, FJ, FY, HC and HG. The first draft of the manuscript was written by XL and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Xiaofang Lai.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethical approval

This article contains no studies with human participants performed by any authors.

Additional information

Publisher's Note

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

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

Lai, X., Ji, F., Yu, F. et al. Delta of Exopalaemon carinicauda: molecular characterization, expression in different tissues and developmental stages, and its SNPs association analysis with development. Mol Biol Rep 50, 10083–10095 (2023). https://doi.org/10.1007/s11033-023-08840-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-023-08840-4

Keywords

Navigation