Skip to main content

Advertisement

SpringerLink
Log in

Transcriptome Profiling of Long Non-coding RNAs During the Atlantic Salmon Smoltification Process

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

Abstract

For salmon aquaculture, one of the most critical phase is the parr-smolt transformation. Studies around this process have mainly focused on physiological changes and the Na+/K+-ATPase activity during the osmoregulatory activity. However, understanding how the salmon genome regulates the parr-smolt transformation, specifically the molecular mechanisms involved, remains uncovered. This study aimed to explore the transcriptional modulation of long non-coding RNAs (lncRNAs), as key molecular regulators, during the freshwater (FW) to seawater (SW) transfer in Atlantic salmon. Transcriptome sequencing was performed from gill samples of Atlantic salmon adapted from FW to SW through gradual salinity changes from 0 to 30 PSU. The results showed that most transcripts differently modulated were downregulated in all salinity conditions. Relevant biological processes were associated with growth, collagen formation, immune response, metabolism, and heme transport. Notably, 2864 putative lncRNAs were identified in Atlantic salmon gills differently expressed during fish smoltification. The highest number of lncRNAs differently modulated was observed at 30 PSU. Correlation expression analysis suggests putative regulatory roles of lncRNAs with smoltification-related genes. Herein, co-localization of Na+/K+-ATPase, growth hormone receptor, and thyroid hormone receptor genes with lncRNAs differentially expressed suggest putative regulatory mechanisms in the Atlantic salmon genome. The lncRNAs can be used as novel biomarkers for the fish smoltification process. Here, the lncRNA_145326 and lncRNA_18762 are putatively related to the parr-smolt transfer in Atlantic salmon. This study is the first description of lncRNAs with putative regulatory roles in Atlantic salmon during the SW adaptation.

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

  • Björnsson BT, Bradley TM (2007) Epilogue: past successes, present misconceptions and future milestones in salmon smoltification research. Aquaculture 273:384–391

    Article  Google Scholar 

  • Boltaña S, Valenzuela-Miranda D, Aguilar A, Mackenzie S, Gallardo-Escárate C (2016) Long noncoding RNAs (lncRNAs) dynamics evidence immunomodulation during ISAV-Infected Atlantic salmon (Salmo salar). Sci Rep 6

  • Ebbesson LOE, Ekström P, Ebbesson SOE, Stefansson SO, Holmqvist B (2003) Neural circuits and their structural and chemical reorganization in the light–brain–pituitary axis during parr–smolt transformation in salmon. Aquaculture 222:59–70

    Article  CAS  Google Scholar 

  • Hezroni H, Koppstein D, Schwartz MG, Avrutin A, Bartel DP, Ulitsky I (2015) Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species. Cell Rep 11:1110–1122

    Article  CAS  Google Scholar 

  • Higgins P (1985) Metabolic differences between Atlantic salmon (Salmo salar) parr and smolts. Aquaculture 45:33–53

    Article  Google Scholar 

  • Johansson LH, Timmerhaus G, Afanasyev S, Jørgensen SM, Krasnov A (2016) Smoltification and seawater transfer of Atlantic salmon (Salmo salar L.) is associated with systemic repression of the immune transcriptome. Fish Shellfish Immunol 58:33–41

    Article  CAS  Google Scholar 

  • Kapusta A, Kronenberg Z, Lynch VJ, Zhuo X, Ramsay L, Bourque G, Yandell M,  Feschotte C (2013) Transposable elements are major contributors to the origin, diversification, and regulation of vertebrate long noncoding RNAs. PLoS Genet 9

  • Karlik E, Gözükırmızı N (2018) Evaluation of barley lncRNAs expression analysis in salinity stress. Russ J Genet 54:198–204

    Article  CAS  Google Scholar 

  • Krasnov A, Koskinen H, Afanasyev S, Mölsä H (2005) Transcribed Tc1-like transposons in salmonid fish. BMC Genomics 6:107

    Article  Google Scholar 

  • Lien S, Koop BF, Sandve SR, Miller JR, Kent MP, Nome T, Hvidsten TR, Leong JS, Minkley DR, Zimin A (2016) The Atlantic salmon genome provides insights into rediploidization. Nature 533:200

  • Marshall WS (2002) Na+, Cl−, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283

    Article  CAS  Google Scholar 

  • Maryoung LA, Lavado R, Bammler TK, Gallagher EP, Stapleton PL, Beyer RP, Farin FM, Hardiman G, Schlenk D (2015) Differential gene expression in liver, gill, and olfactory rosettes of coho salmon (Oncorhynchus kisutch) after acclimation to salinity. Mar Biotechnol 17:703–717

    Article  CAS  Google Scholar 

  • Mccormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity. Can J Fish Aquat Sci 50:656–658

    Article  CAS  Google Scholar 

  • Mccormick SD, Björnsson BT (1994) Physiological and hormonal differences among Atlantic salmon parr and smolts reared in the wild, and hatchery smolts. Aquaculture 121:235–244

    Article  CAS  Google Scholar 

  • Mccormick SD, Hansen LP, Quinn TP, Saunders RL (1998) Movement, migration, and smolting of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55:77–92

    Article  Google Scholar 

  • Mccormick SD, Lerner DT, Monette MY, Nieves-Puigdoller K, Kelly JT, Björnsson BT (2009) Taking it with you when you go: How perturbations to the freshwater environment, including temperature, dams, and contaminants, affect marine survival of salmon. Am Fish Soc Symp, Citeseer

    Google Scholar 

  • Mccormick SD, O’dea MF, Moeckel Björnsson AMBT (2003) Endocrine and physiological changes in Atlantic salmon smolts following hatchery release. Aquaculture 222:45–57

    Article  CAS  Google Scholar 

  • Muthusamy M, Uma S, Backiyarani S, Saraswathi M (2015) Genome-wide screening for novel, drought stress-responsive long non-coding RNAs in drought-stressed leaf transcriptome of drought-tolerant and-susceptible banana (Musa spp) cultivars using Illumina high-throughput sequencing. Plant Biotechnol Rep 9:279–286

    Article  Google Scholar 

  • Norman JD, Ferguson MM, Danzmann RG (2014) An integrated transcriptomic and comparative genomic analysis of differential gene expression in Arctic charr (Salvelinus alpinus) following seawater exposure. J Exp Biol. https://doi.org/10.1242/jeb.107441

    Article  PubMed  Google Scholar 

  • Núñez-Acuña G, Détrée C, Gallardo-Escárate C, Gonçalves AT (2017) Functional diets modulate lncRNA-coding RNAs and gene interactions in the intestine of rainbow trout Oncorhynchus mykiss. Mar Biotechnol 19:287–300

    Article  Google Scholar 

  • Place RF, Noonan EJ (2014) Non-coding RNAs turn up the heat: an emerging layer of novel regulators in the mammalian heat shock response. Cell Stress Chaperones 19:159–172

    Article  CAS  Google Scholar 

  • Renaut S, Nolte AW, Bernatchez L (2010) Mining transcriptome sequences towards identifying adaptive single nucleotide polymorphisms in lake whitefish species pairs (Coregonus spp. Salmonidae). Mol Ecol 19:115–131

    Article  CAS  Google Scholar 

  • Robertson LS, Mccormick SD (2012) Transcriptional profiling of the parr–smolt transformation in Atlantic salmon. Comp Biochem Physiol D: Genomics Proteomics 7:351–360

    CAS  PubMed  Google Scholar 

  • Seear PJ, Carmichael SN, Talbot R, Taggart JB, Bron JE, Sweeney GE (2010) Differential gene expression during smoltification of Atlantic salmon (Salmo salar L.): a first large-scale microarray study. Mar Biotechnol 12:126–140

    Article  CAS  Google Scholar 

  • Stefansson S, Bjürnsson BT, Ebbesson L, Mccormic S (2008) Smoltification. In: Fish larval physiology (Finn RN, Kapor BG Eds.) Science Publishers, Inc. Enfield (NH) and IBN Publishing Co. Pvt.

  • Sullivan CV, Dickhoff WW, Mahnken C, Hershberger W (1985) Changes in the hemoglobin system of the coho salmon (Oncorhynchus kisutch) during smoltification and triiodothyronine and propylthiouracil treatment. Comp Biochem Physiol, A: Comp Physiol 81:807–813

    Article  CAS  Google Scholar 

  • Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6:e21800

    Article  CAS  Google Scholar 

  • Sweeting R, Wagner G, Mckeown B (1985) Changes in plasma glucose, amino acid nitrogen and growth hormone during smoltification and seawater adaptation in coho salmon, (Oncorhynchus kisutch). Aquaculture 45:185–197

    Article  CAS  Google Scholar 

  • Tarifeño-Saldivia E, Valenzuela-Miranda D, Gallardo-Escárate C (2017) In the shadow: The emerging role of long non-coding RNAs in the immune response of Atlantic salmon. Dev Comp Immunol 73:193–205

    Article  Google Scholar 

  • Tipsmark CK, Sørensen KJ, Madsen SS (2010) Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation. J Exp Biol 213:368–379

    Article  CAS  Google Scholar 

  • Valenzuela-Miranda D, Gallardo-Escárate C (2016) Novel insights into the response of Atlantic salmon (Salmo salar) to Piscirickettsia salmonis: interplay of coding genes and lncRNAs during bacterial infection. Fish Shellfish Immunol 59:427–438

    Article  CAS  Google Scholar 

  • Valenzuela-Muñoz V, Novoa B, Figueras A, Gallardo-Escárate C (2017) Modulation of Atlantic salmon miRNome response to sea louse infestation. Dev Comp Immunol 76:380–391

    Article  Google Scholar 

  • Valenzuela-Muñoz V, Valenzuela-Miranda D, Gallardo-Escárate C (2018) Comparative analysis of long non-coding RNAs in Atlantic and Coho salmon reveals divergent transcriptome responses associated with immunity and tissue repair during sea lice infestation. Dev Comp Immunol 87:36–50

    Article  Google Scholar 

  • Xu Q, Song Z, Zhu C, Tao C, Kang L, Liu W, He F, Yan J, Sang T (2017) Systematic comparison of lncRNAs with protein coding mRNAs in population expression and their response to environmental change. BMC Plant Biol 17:42

    Article  Google Scholar 

Download references

Funding

ANID-Chile funded this study through Postdoctoral grant FONDECYT (#3190320), FONDECYT (#1180867 and # 1201498), and FONDAP (#15110027).

Author information

Authors and Affiliations

  1. Interdisciplinary Center for Aquaculture Research (INCAR), University of Concepción, Concepción, Chile

    Valentina Valenzuela-Muñoz, Juan Antonio Váldes & Cristian Gallardo-Escárate

  2. Laboratorio de Biotecnología Molecular, Universidad Andrés Bello, Facultad de Ciencias de la Vida, Santiago, Chile

    Valentina Valenzuela-Muñoz & Juan Antonio Váldes

  3. Laboratory of Biotechnology and Aquatic Genomics, Department of Oceanography, University of Concepción, Concepción, Chile

    Valentina Valenzuela-Muñoz & Cristian Gallardo-Escárate

Authors
  1. Valentina Valenzuela-Muñoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Antonio Váldes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristian Gallardo-Escárate
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valentina Valenzuela-Muñoz.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

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

Valenzuela-Muñoz, V., Váldes, J.A. & Gallardo-Escárate, C. Transcriptome Profiling of Long Non-coding RNAs During the Atlantic Salmon Smoltification Process. Mar Biotechnol 23, 308–320 (2021). https://doi.org/10.1007/s10126-021-10024-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-021-10024-9

Keywords

Search

Navigation