Whole-Genome Transcript Expression Profiling Reveals Novel Insights into Transposon Genes and Non-Coding RNAs during Atlantic Salmon Seawater Adaptation
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Smoltification and Seawater Transfer
2.2. High-Throughput Transcriptome Sequencing
2.3. Whole-Genome Transcript Expression Analysis
2.4. RNA-Seq Data Analysis
2.5. Sequence Annotation and GO Enrichment Analysis
2.6. miRNA Annotation and Expression Analysis in Response to Salinity Changes
2.7. miRNA Target Prediction and Expression Correlation
2.8. RT-qPCR Validation Analysis
3. Results
3.1. Atlantic Salmon Performance during the Experimental Trial
3.2. Gill-Tissue-Transcription Modulation during Smoltification Process
3.3. Intestine Tissue-Transcription Modulation during Smoltification Process
3.4. Head-Kidney Transcriptome Modulation during Smoltification Process
3.5. Differential Expression Analysis of Atlantic Salmon during Seawater Transfer
3.6. miRNA Regulation in Atlantic Salmon during Smoltification
3.7. GO Enrichment of miRNA Target Genes
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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GSC Atlantic Salmon | SS Atlantic Salmon | ||
---|---|---|---|
Gill Tissue Biological Process | N° GO Term | Gill Tissue Biological Process | N° GO Term |
Cellular process | 269 | Pattern recognitio receptor signaling pathway | 126 |
Metabolic prosess | 259 | Regulation of Pattern recognitio receptor signaling pathway | 121 |
Response to stimilus | 243 | Truptophanil-tRNA aminoacylation | 59 |
Macromolecule metabolic process | 241 | Protein ADP-ribosylation | 53 |
Biological regulation | 239 | Regulation od protein ADP-ribosylation | 51 |
Regulation of biological process | 234 | Spindle assembly | 43 |
Cellular biosynthetic process | 233 | Mitotic spindle assembly | 32 |
Regulation of cellular process | 232 | Response to ATP | 30 |
Organic cyclic compound metabolic process | 229 | Regulation of meiotic cell cycle | 28 |
Celullar response to stimulus | 226 | Microtube nucleation | 23 |
Gene expression | 221 | Carbon utilization | 22 |
Regulation of metabolic process | 218 | Regulation of mitotic spindle assembly | 20 |
Localization | 215 | ||
Cell communication | 214 | ||
Transport | 212 | ||
Organic ciclyc compound biosynthetic process | 210 | ||
Regulation of cellular metabolic process | 210 | ||
Cellular component organization | 209 | ||
Cellular component organization or biogenesis | 209 | ||
Portein metabolic process | 209 | ||
Cellular macomolecule biosynthetic process | 208 | ||
Response to stress | 203 | ||
Immune system process | 202 | ||
Small molecules metabolic process | 202 | ||
Regulation of gene expression | 202 | ||
Intestine Tissue Biological Process | N° GO Term | Intestine Tissue Biological Process | N° GO Term |
Cellular process | 269 | Regulation of mononuclear cell proliferation | 8 |
Metabolic prosess | 259 | Regulation of lymphocyte proliferation | 8 |
Organic substance metabolic process | 256 | Antigen processing and presentation of peptide | 8 |
Cellular metabolic process | 255 | Hydrogen peroxide catabolic process | 7 |
Prymary metabolic process | 253 | Antigen processing and presentation of peptide antigen | 7 |
Response to stimilus | 243 | MCH class II | 6 |
Macromolecule metabolic process | 241 | Fertilization | 5 |
Biological regulation | 239 | Cell-cell recognition | 4 |
Organic substance biosynthetic process | 237 | Sperm-egg recognition | 3 |
Biosynthetic process | 237 | Lung epithelium development | 3 |
Regulation of biological process | 234 | Hemolysis in other organims | 3 |
Cellular macomolecule metabolic process | 233 | Microtubule polymerization | 3 |
Regulation of cellular process | 233 | Regulation of platelet activation | 3 |
Cellular response to stimulus | 232 | Forebrain neuron differentation | 3 |
Gene expression | 226 | Forebrain generation of neurons | 3 |
Nucleobase-containing compund metabolic process | 221 | ||
Regulation of metabolic process | 221 | ||
Cellular nitrogen compound bisynthetic process | 218 | ||
Localization | 215 | ||
Cell communication | 214 | ||
Transport | 212 | ||
Response to stress | 203 | ||
Immune system process | 202 | ||
Regulation of gene expression | 202 | ||
Head Kidney Tissue Biological Process | N° GO Term | Head Kidney Tissue Biological Process | N° GO Term |
Cellular process | 169 | DNA integration | 82 |
Metabolic prosess | 165 | Transposition | 55 |
Cellular metabolic process | 163 | Transposition, DNA-mediated | 55 |
Organic substance metabolic process | 163 | Macromolecule glycosylation | 42 |
Primary metabolic process | 158 | Protein glycosilation | 42 |
Nitrogen compund metabolic process | 154 | Pryrimidine nucleotide-sugar transmembrane transport | 19 |
Cellular biosynthetic process | 153 | Nucelotide-sugar transmembrane transport | 19 |
Biosyntetic process | 153 | ARF protein signal transduction | 10 |
Organic substance biosynthetic process | 152 | Regulation of ARF protein signal transduction | 10 |
Macromolecule metabolic process | 151 | ||
Biological regulation | 149 | ||
Organonitrogen compound metabolic process | 149 | ||
Response to stimilus | 147 | ||
Cellular macomolecule metabolic process | 147 | ||
Regulation of biological process | 146 | ||
Localization | 144 | ||
Cellular nitrogen compound metabolic process | 143 | ||
Regulation of cellular process | 143 | ||
Organic cyclic compound metabolic process | 143 | ||
Transport | 142 | ||
Establishment of localization | 142 | ||
Immune system process | 124 | ||
Immune response | 119 | ||
Defense response | 108 | ||
Response to biotic stimilus | 103 |
Tissue | miRNA | Fold Change GSC | Fold Change SS | De nodo Assembly Contig | Fold Change GSC | Fold Change SS | Delta G | Description |
---|---|---|---|---|---|---|---|---|
Gills | ssa-miR-204-5p | −2, 52 | 0 | contig_33389 | 2, 14 | 0 | −12.00 | PREDICTED: serine/threonine-protein kinase WNK2-like isoform X2 [Salmo salar] |
ssa-miR-19c-3-5p | 3, 04 | 0 | contig_41523 | −2, 29 | 0 | −12.00 | PREDICTED: heat shock 70 kDa protein 12B-like [Salmo salar] | |
ssa-miR-214-5p | −1, 51 | 0 | contig_50634 | 2, 59 | 0 | −12.00 | PREDICTED: creatine kinase S-type, mitochondrial isoform X1 [Salmo salar] | |
ssa-miR-214-5p | −1, 51 | 0 | contig_29197 | 2, 47 | 0 | −12.20 | PREDICTED: MAPK/MAK/MRK overlapping kinase-like isoform X1 [Salmo salar] | |
ssa-miR-199a-3p | −1, 52 | 0 | contig_12464 | 2, 54 | 0 | −12.00 | PREDICTED: interleukin-20 receptor subunit beta-like [Salmo salar] | |
ssa-miR-19c-3-5p | 3, 04 | 0 | contig_3735 | −2, 11 | 0 | −12.00 | PREDICTED: myosin light chain kinase, smooth muscle-like isoform X3 [Salmo salar] | |
ssa-miR-456-5p | 0 | 8, 79 | contig_63289 | 0 | −3, 32 | −12.00 | PREDICTED: fibroblast growth factor 10-like [Salmo salar] | |
ssa-miR-150-3p | 0 | −1, 6 | contig_15517 | 0 | 2, 02 | −12.10 | ATPase inhibitor, mitochondrial precursor [Salmo salar] | |
ssa-miR-19d-5p | 0 | −2, 68 | contig_13064 | 0 | 2, 07 | −12.00 | ATP-binding cassette sub-family F member 2 [Salmo salar] | |
ssa-miR-222b-5p | 0 | −1, 98 | contig_78633 | 0 | 3, 86 | −12.00 | transposase [Salmo salar] | |
ssa-miR-204-5p | −2, 52 | 0 | contig_66355 | 2, 96 | 0 | −12.00 | transposase [Salmo salar] | |
ssa-miR-18b-5p | 0 | 1, 56 | contig_19956 | 0 | −17, 31 | −12.00 | PREDICTED: haptoglobin-like [Salmo salar] | |
ssa-miR-456-5p | 0 | 8, 79 | contig_9077 | 0 | −3, 2 | −12.00 | SPATA5 [Salmo salar] | |
ssa-miR-456-5p | 0 | 8, 79 | contig_52147 | 0 | −2, 72 | −12.10 | PREDICTED: MAPK/MAK/MRK overlapping kinase-like isoform X3 [Salmo salar] | |
ssa-miR-456-5p | 0 | 8, 79 | contig_32835 | 0 | −2, 64 | −12.00 | interleukin-17A/F3 [Salmo salar] | |
Intestine | ssa-miR-25-3-5p | 4, 02 | 0 | contig_19100 | −2, 43 | 0 | −30.60 | PREDICTED: non-syndromic hearing impairment protein 5-like isoform X2 [Salmo salar] |
ssa-miR-30a-3-3p | 0 | 2, 28 | contig_58533 | −3, 12 | 0 | −30.50 | PREDICTED: kynureninase-like [Salmo salar] | |
ssa-miR-92b-3p | 0 | 1, 22 | contig_2303 | 2, 07 | 0 | −30.40 | PREDICTED: coronin-1B-like [Salmo salar] | |
ssa-miR-214-5p | 0 | 1, 35 | contig_3322 | 2, 75 | 0 | −30.10 | PREDICTED: fibroblast growth factor receptor substrate 2-like [Salmo salar] | |
ssa-miR-19c-5p | −2, 06 | 0 | contig_51580 | 3, 29 | 0 | −30.10 | PREDICTED: protein-tyrosine kinase 6-like [Salmo salar] | |
ssa-miR-92a-5p | 3, 72 | 0 | contig_4409 | −4, 12 | 0 | −30.00 | PREDICTED: dihydropyrimidinase-related protein 4-like [Salmo salar] | |
ssa-miR-125b-5p | 0 | 1, 26 | contig_4543 | 0 | −1, 97 | −29.80 | PREDICTED: low-density lipoprotein receptor-related protein 2-like [Salmo salar] | |
ssa-miR-30a-3-3p | 0 | 2, 28 | contig_3114 | 0 | −1, 94 | −29.00 | PREDICTED: free fatty acid receptor 3-like [Salmo salar] | |
ssa-miR-30a-3p | −1, 73 | 0 | contig_44524 | 2, 17 | 0 | −29.00 | PREDICTED: annexin A2-like [Salmo salar] | |
ssa-miR-92a-5p | 3, 72 | 0 | contig_51439 | −3, 15 | 0 | −28.90 | PREDICTED: myosin heavy chain, fast skeletal muscle-like [Salmo salar] | |
ssa-miR-15a-3p | 1, 72 | 0 | contig_9149 | −2, 1 | 0 | −28.40 | PREDICTED: annexin A2-like [Salmo salar] | |
ssa-miR-140-3p | −1, 53 | 0 | contig_25304 | 4, 52 | 0 | −28.40 | PREDICTED: leucine-rich repeat-containing protein 58-like [Salmo salar] | |
ssa-miR-456-3p | 3, 35 | 0 | contig_24874 | −1, 73 | 0 | −17.60 | PREDICTED: sialic acid-binding Ig-like lectin 5 [Salmo salar] | |
ssa-let-7i-5p | 0 | 5, 51 | contig_66659 | 0 | −1, 37 | −16.80 | PREDICTED: dedicator of cytokinesis protein 3-like, partial [Salmo salar] | |
ssa-let-7d-5p | 4 | 0 | contig_28976 | −5, 05 | 0 | −16.00 | PREDICTED: fibroblast growth factor receptor substrate 2-like [Salmo salar] | |
Head kidney | ssa-miR-8157-3p | 0 | −2, 18 | contig_122554 | 0 | 6, 77 | −30.20 | PREDICTED: E3 ubiquitin-protein ligase TRIP12-like isoform X1 [Salmo salar] |
ssa-miR-128-1-5p | −1, 57 | 0 | contig_72217 | 6, 3 | 0 | −29.60 | SPATA5 [Salmo salar] | |
ssa-miR-214-3p | 0 | 1, 8 | contig_21752 | 0 | −1, 47 | −29.50 | PREDICTED: BTB/POZ domain-containing adapter for CUL3-mediated RhoA degradation protein 2 isoform X1 [Salmo salar] | |
ssa-miR-8157-3p | 0 | −2, 18 | contig_46746 | 0 | 1, 67 | −29.50 | PREDICTED: phospholipid-transporting ATPase 11C-like isoform X1 [Salmo salar] | |
ssa-miR-205a-5p | 0 | 1, 99 | contig_45675 | 0 | −1, 03 | −29.40 | PREDICTED: von Willebrand factor A domain-containing protein 7-like [Salmo salar] | |
ssa-miR-214-3p | 0 | 1, 8 | contig_95191 | 0 | −1, 84 | −28.90 | PREDICTED: fibrinogen beta chain-like [Salmo salar] | |
ssa-miR-194a-3p | 7, 34 | 0 | contig_28663 | −3, 31 | 0 | −28.60 | PREDICTED: laminin subunit alpha-4-like isoform X1 [Salmo salar] | |
ssa-miR-462a-3p | −1, 86 | 0 | contig_22955 | 2, 08 | 0 | −34.50 | PREDICTED: 3-keto-steroid reductase-like isoform X2 [Salmo salar] | |
ssa-miR-122-5p | 0 | 3, 15 | contig_68369 | 0 | −1, 89 | −29.80 | PREDICTED: transcription factor E2F7-like [Salmo salar] | |
ssa-miR-125a-5p | 0 | 2, 32 | contig_31191 | 0 | −1, 03 | −27.70 | PREDICTED: tectonic-2 [Salmo salar] | |
ssa-miR-449a-5p | 21, 47 | 0 | contig_44769 | −2, 24 | 0 | −20.40 | PREDICTED: guanine nucleotide-binding protein G(I)/G(S)/G(T) subunit beta-3-like isoform X1 [Salmo salar] | |
ssa-miR-192b-5p | 13, 39 | 0 | contig_65873 | −2, 18 | 0 | −20.00 | PREDICTED: E3 ubiquitin-protein ligase RNF144A-like [Salmo salar] | |
ssa-miR-212a-5p | −1, 83 | 0 | contig_49183 | 2, 56 | 0 | PREDICTED: collagen EMF1-alpha-like [Salmo salar] |
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Valenzuela-Muñoz, V.; Gallardo-Escárate, C.; Benavente, B.P.; Valenzuela-Miranda, D.; Núñez-Acuña, G.; Escobar-Sepulveda, H.; Váldes, J.A. Whole-Genome Transcript Expression Profiling Reveals Novel Insights into Transposon Genes and Non-Coding RNAs during Atlantic Salmon Seawater Adaptation. Biology 2022, 11, 1. https://0-doi-org.brum.beds.ac.uk/10.3390/biology11010001
Valenzuela-Muñoz V, Gallardo-Escárate C, Benavente BP, Valenzuela-Miranda D, Núñez-Acuña G, Escobar-Sepulveda H, Váldes JA. Whole-Genome Transcript Expression Profiling Reveals Novel Insights into Transposon Genes and Non-Coding RNAs during Atlantic Salmon Seawater Adaptation. Biology. 2022; 11(1):1. https://0-doi-org.brum.beds.ac.uk/10.3390/biology11010001
Chicago/Turabian StyleValenzuela-Muñoz, Valentina, Cristian Gallardo-Escárate, Bárbara P. Benavente, Diego Valenzuela-Miranda, Gustavo Núñez-Acuña, Hugo Escobar-Sepulveda, and Juan Antonio Váldes. 2022. "Whole-Genome Transcript Expression Profiling Reveals Novel Insights into Transposon Genes and Non-Coding RNAs during Atlantic Salmon Seawater Adaptation" Biology 11, no. 1: 1. https://0-doi-org.brum.beds.ac.uk/10.3390/biology11010001