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Identification and Evaluation of Long Noncoding RNAs in Response to Handling Stress in Red Cusk-Eel (Genypterus chilensis) via RNA-seq

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Abstract

The red cusk-eel (Genypterus chilensis) is a native species with strong potential to support Chilean aquaculture diversification. Under commercial conditions, fish are exposed to several stressors. To date, little is known about the mechanism involved in the stress response of red cusk-eel, and there is no information related to the regulation mediated by long noncoding RNAs (lncRNAs). The objective of this work was to identify for the first time the lncRNAs in the transcriptome of G. chilensis and to evaluate the differential expression levels of lncRNAs in the liver, head kidney, and skeletal muscle in response to handling stress. We used previously published transcriptome data to identify the lncRNAs by applying a series of filters based on annotation information in several databases to discard coding sequences. We identified a total of 14,614 putative lncRNAs in the transcriptome of red cusk-eel, providing a useful lncRNA reference resource to be used in future studies. We evaluated their differential expression in response to handling stress in the liver, head kidney, and skeletal muscle, identifying 112, 323, and 108 differentially expressed lncRNAs, respectively. The results suggest that handling stress in red cusk-eel generate an altered metabolic status in liver, altered immune response in head kidney, and skeletal muscle atrophy through an important coding and noncoding gene network. This is the first study that identifies lncRNAs in Genypterus genus and that evaluates the relation between handling stress and lncRNAs in teleost fish, thereby providing valuable information regarding noncoding responses to stress in Genypterus species.

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References

  • Aballai V, Aedo JE, Maldonado J, Bastias-Molina M, Silva H, Meneses C, Boltana S, Reyes A, Molina A, Valdes JA (2017) RNA-seq analysis of the head-kidney transcriptome response to handling-stress in the red cusk-eel (Genypterus chilensis). Comp Biochem Phys D 24:111–117

    CAS  Google Scholar 

  • Abdelmohsen K, Kuwano Y, Kim HH, Gorospe M (2008) Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biol Chem 389:243–255

    CAS  PubMed  Google Scholar 

  • Aedo JE, Maldonado J, Estrada JM, Fuentes EN, Silva H, Gallardo-Escarate C, Molina A, Valdes JA (2014) Sequencing and de novo assembly of the red cusk-eel (Genypterus chilensis) transcriptome. Mar Genomics 18 Pt B:105–107

    PubMed  Google Scholar 

  • Aedo JE, Maldonado J, Aballai V, Estrada JM, Bastias-Molina M, Meneses C, Gallardo-Escarate C, Silva H, Molina A, Valdes JA (2015) mRNA-seq reveals skeletal muscle atrophy in response to handling stress in a marine teleost, the red cusk-eel (Genypterus chilensis). BMC Genomics 16:1024

    PubMed  PubMed Central  Google Scholar 

  • Ali A, Al-Tobasei R, Kenney B, Leeds TD, Salem M (2018) Integrated analysis of lncRNA and mRNA expression in rainbow trout families showing variation in muscle growth and fillet quality traits. Sci Rep 8:12111

    PubMed  PubMed Central  Google Scholar 

  • Al-Tobasei R, Paneru B, Salem M (2016) Genome-wide discovery of long non-coding RNAs in rainbow trout. Plos One 11:e0148940

    PubMed  PubMed Central  Google Scholar 

  • Aluru N, Vijayan MM (2009) Stress transcriptomics in fish: a role for genomic cortisol signaling. Gen Comp Endocrinol 164:142–150

    CAS  PubMed  Google Scholar 

  • Amaral PP, Dinger ME, Mattick JS (2013) Non-coding RNAs in homeostasis, disease and stress responses: an evolutionary perspective. Brief Funct Genomics 12:254–278

    CAS  PubMed  Google Scholar 

  • Ayupe AC, Tahira AC, Camargo L, Beckedorff FC, Verjovski-Almeida S, Reis EM (2015) Global analysis of biogenesis, stability and sub-cellular localization of lncRNAs mapping to intragenic regions of the human genome. RNA Biol 12:877–892

    PubMed  PubMed Central  Google Scholar 

  • Basu S, Hadzhiev Y, Petrosino G, Nepal C, Gehrig J, Armant O, Ferg M, Strahle U, Sanges R, Muller F (2016) The Tetraodon nigroviridis reference transcriptome: developmental transition, length retention and microsynteny of long non-coding RNAs in a compact vertebrate genome. Sci Rep 6:33210

  • Bhat SA, Ahmad SM, Mumtaz PT, Malik AA, Dar MA, Urwat U, Shah RA, Ganai NA (2016) Long non-coding RNAs: mechanism of action and functional utility. Noncoding RNA Res 1:43–50

    PubMed  PubMed Central  Google Scholar 

  • Boltana S, Valenzuela-Miranda D, Aguilar A, Mackenzie S, Gallardo-Escarate C (2016) Long noncoding RNAs (lncRNAs) dynamics evidence immunomodulation during ISAV-infected Atlantic salmon (Salmo salar). Sci Rep 6:22698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bugeon J, Lefevre F, Cardinal M, Uyanik A, Davenel A, Haffray P (2010) Flesh quality in large rainbow trout with high or low fillet yield. J Muscle Foods 21:702–721

    Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    CAS  Google Scholar 

  • Cech TR, Steitz JA (2014) The noncoding RNA revolution-trashing old rules to forge new ones. Cell 157:77–94

    CAS  PubMed  Google Scholar 

  • Chong J, Gonzalez P (2009) Reproductive cycle and maturity mean size of the red cusk eel, Genypterus chilensis (Guichenot, 1881) in the coast off Talcahuano, Chile. Rev Biol Mar Oceanog 44:257–262

    Google Scholar 

  • Clark MB, Johnston RL, Inostroza-Ponta M, Fox AH, Fortini E, Moscato P, Dinger ME, Mattick JS (2012) Genome-wide analysis of long noncoding RNA stability. Genome Res 22:885–898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    CAS  Google Scholar 

  • Etebari K, Furlong MJ, Asgari S (2015) Genome wide discovery of long intergenic non-coding RNAs in diamondback moth (Plutella xylostella) and their expression in insecticide resistant strains. Sci Rep 5:14642

  • Fast MD, Hosoya S, Johnson SC, Afonso LOB (2008) Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish Immun 24:194–204

    CAS  Google Scholar 

  • Geven EJW, Klaren PHM (2017) The teleost head kidney: integrating thyroid and immune signalling. Dev Comp Immunol 66:73–83

    CAS  PubMed  Google Scholar 

  • Gonzalez P, Dettleff P, Valenzuela C, Estrada JM, Valdes JA, Meneses C, Molina A (2019) Evaluating the genetic structure of wild and commercial red cusk-eel (Genypterus chilensis) populations through the development of novel microsatellite markers from a reference transcriptome. Mol Biol Rep. https://doi.org/10.1007/s11033-019-05021-0

    PubMed  Google Scholar 

  • Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang XP, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477:295–U60

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu FZ, Xu K, Zhou YF, Wu C, Wang S, Xiao J, Wen M, Zhao RR, Luo KK, Tao M, Duan W, Liu SJ (2017) Different expression patterns of sperm motility-related genes in testis of diploid and tetraploid cyprinid fish. Biol Reprod 96:907–920

    PubMed  PubMed Central  Google Scholar 

  • Jiang LH, Liu W, Zhu AY, Zhang JS, Zhou JJ, Wu CW (2016) Transcriptome analysis demonstrate widespread differential expression of long noncoding RNAs involve in Larimichthys crocea immune response. Fish Shellfish Immun 51:1–8

    CAS  Google Scholar 

  • Jiang P, Hou Y, Fu W, Tao X, Luo J, Lu H, Xu Y, Han B, Zhang J (2018) Characterization of lncRNAs involved in cold acclimation of zebrafish ZF4 cells. PLoS One 13

  • Johnston IA (1982) Physiology of muscle in hatchery raised fish. Comp Biochem Phys B 73:105–124

    Google Scholar 

  • Kalvari I, Argasinska J, Quinones-Olvera N, Nawrocki EP, Rivas E, Eddy SR, Bateman A, Finn RD, Petrov AI (2018) Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res 46:D335–D342

    CAS  PubMed  Google Scholar 

  • Kim, C., Kang, D., Lee, E.K. & Lee, J.S. (2017). Long noncoding RNAs and RNA-binding proteins in oxidative stress, cellular senescence, and age-related diseases. Oxid Med Cell Longev 2017:2062384

  • Kour S, Rath PC (2016) Long noncoding RNAs in aging and age-related diseases. Ageing Res Rev 26:1–21

    CAS  PubMed  Google Scholar 

  • Krasnov A, Koskinen H, Pehkonen P, Rexroad CE, Afanasyev S, Molsa H (2005) Gene expression in the brain and kidney of rainbow trout in response to handling stress. BMC Genomics 6:3

    PubMed  PubMed Central  Google Scholar 

  • Li Y, Kong L, Deng M, Lian Z, Han Y, Sun B, Guo Y, Liu G, Liu D (2019) Heat stress-responsive Transcriptome analysis in the liver tissue of Hu sheep. Genes (Basel) 10.

  • Liao Q, Liu CN, Yuan XY, Kang SL, Miao RY, Xiao H, Zhao GG, Luo HT, Bu DC, Zhao HT, Skogerbo G, Wu ZD, Zhao Y (2011) Large-scale prediction of long non-coding RNA functions in a coding-non-coding gene co-expression network. Nucleic Acids Res 39:3864–3878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lopes CT, Franz M, Kazi F, Donaldson SL, Morris Q, Bader GD (2010) Cytoscape web: an interactive web-based network browser. Bioinformatics 26:2347–2348

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luo HL, Yang HZ, Lin Y, Zhang YD, Pan CY, Feng PF, Yu YL, Chen XH (2017) LncRNA and mRNA profiling during activation of tilapia macrophages by HSP70 and Streptococcus agalactiae antigen. Oncotarget 8:98455–98470

    PubMed  PubMed Central  Google Scholar 

  • Metz JR, Huising MO, Leon K, Verburg-Van Kemenade BML, Flik G (2006) Central and peripheral interleukin-1 beta and interieukin-1 receptor I expression and their role in the acute stress response of common carp, Cyprinus carpio L. J Endocrinol 191:25–35

    CAS  PubMed  Google Scholar 

  • Montes M, Lund AH (2016) Emerging roles of lncRNAs in senescence. FEBS J 283:2414–2426

    CAS  PubMed  Google Scholar 

  • Mu C, Wang RJ, Li TQ, Li YQ, Tian ML, Jiao WQ, Huang XT, Zhang LL, Hu XL, Wang S, Bao ZM (2016) Long non-coding RNAs (lncRNAs) of sea cucumber: large-scale prediction, expression profiling, non-coding network construction, and lncRNA-microRNA-gene interaction analysis of lncRNAs in Apostichopus japonicus and Holothuria glaberrima during LPS challenge and radial organ complex regeneration. Mar Biotechnol 18:485–499

    CAS  PubMed  Google Scholar 

  • Nakano T, Afonso LOB, Beckman BR, Iwama GK, Devlin RH (2013) Acute physiological stress down-regulates mRNA expressions of growth-related genes in Coho Salmon. Plos One 8:e71421

    PubMed  PubMed Central  Google Scholar 

  • Naour S, Espinoza BM, Aedo JE, Zuloaga R, Maldonado J, Bastias-Molina M, Silva H, Meneses C, Gallardo-Escarate C, Molina A, Valdes JA (2017) Transcriptomic analysis of the hepatic response to stress in the red cusk-eel (Genypterus chilensis): insights into lipid metabolism, oxidative stress and liver steatosis. Plos One 12:e0176447

    PubMed  PubMed Central  Google Scholar 

  • Olsvik PA, Vikesa V, Lie KK, Hevroy EM (2013) Transcriptional responses to temperature and low oxygen stress in Atlantic salmon studied with next-generation sequencing technology. BMC Genomics 14:817

    PubMed  PubMed Central  Google Scholar 

  • Paneru B, Ali A, Al-Tobasei R, Kenney B, Salem M (2018) Crosstalk among lncRNAs, microRNAs and mRNAs in the muscle 'degradome' of rainbow trout. Sci Rep 8:8416

    PubMed  PubMed Central  Google Scholar 

  • Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, Schier AF (2012) Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res 22:577–591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qian B, Xue L (2016) Liver transcriptome sequencing and de novo annotation of the large yellow croaker (Larimichthy crocea) under heat and cold stress. Mar Genomics 25:95–102

    PubMed  Google Scholar 

  • Rinn JL, Chang HY (2012) Genome regulation by long noncoding RNAs. Annu Rev Biochem 81:145–166

    CAS  PubMed  Google Scholar 

  • Salisbury JP, Sirbulescu RF, Moran BM, Auclair JR, Zupanc GKH, Agar JN (2015) The central nervous system transcriptome of the weakly electric brown ghost knifefish (Apteronotus leptorhynchus): de novo assembly, annotation, and proteomics validation. BMC Genomics 16:166

  • Sandri M (2013) Protein breakdown in muscle wasting: role of autophagy-lysosome and ubiquitin-proteasome. Int J Biochem Cell Biol 45:2121–2129

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun W, Feng J (2018) Differential lncRNA expression profiles reveal the potential roles of lncRNAs in antiviral immune response of Crassostrea gigas. Fish Shellfish Immunol 81:233–241

    CAS  PubMed  Google Scholar 

  • Tarifeno-Saldivia E, Valenzuela-Miranda D, Gallardo-Escarate 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

    CAS  PubMed  Google Scholar 

  • Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375

    CAS  PubMed  Google Scholar 

  • Valenzuela CA, Escobar D, Perez L, Zuloaga R, Estrada JM, Mercado L, Valdes JA, Molina A (2015) Transcriptional dynamics of immune, growth and stress related genes in skeletal muscle of the fine flounder (Paralichthys adpersus) during different nutritional statuses. Dev Comp Immunol 53:145–157

    CAS  PubMed  Google Scholar 

  • Valenzuela CA, Zuloaga R, Mercado L, Einarsdottir IE, Bjornsson BT, Valdes JA, Molina A (2018) Chronic stress inhibits growth and induces proteolytic mechanisms through two different nonoverlapping pathways in the skeletal muscle of a teleost fish. Am J Physiol-Reg I 314:R102–R113

    Google Scholar 

  • Valenzuela-Miranda D, Gallardo-Escarate 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 Immun 59:427–438

    CAS  Google Scholar 

  • Valenzuela-Munoz V, Valenzuela-Miranda D, Gallardo-Escarate 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

    CAS  PubMed  Google Scholar 

  • Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A. & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:RESEARCH0034

  • Vega R, Pradenas M, Estrada JM, Ramirez D, Valdebenito I, Mardones A, Dantagnan P, Alfaro D, Encina F, Pichara C (2012) Evaluation and comparison of the efficiency of two incubation systems for Genypterus chilensis (Guichenot, 1848) eggs. Lat Am J Aquat Res 40:187–200

    Google Scholar 

  • Vega R, Estrada JM, Ramirez D, Flores C, Zamorano J, Encina F, Mardones A, Valdebenito I, Dantagnan P (2015) Growth of cusk eel Genypterus chilensis juveniles in culture conditions. Lat Am J Aquat Res 43:344–350

    Google Scholar 

  • Wang, L., Park, H.J., Dasari, S., Wang, S.Q., Kocher, J.P. & Li, W. (2013). CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res 41:e74

  • Wang J, Fu LY, Koganti PP, Wang L, Hand JM, Ma H, Yao JB (2016) Identification and functional prediction of large Intergenic noncoding RNAs (lincRNAs) in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol 18:271–282

    CAS  PubMed  Google Scholar 

  • Wu YQ, Cheng TC, Liu C, Liu DL, Zhang Q, Long RW, Zhao P, Xia QY (2016) Systematic identification and characterization of long non-coding RNAs in the silkworm, Bombyx mori. Plos One 11:e0147147

    PubMed  PubMed Central  Google Scholar 

  • Xu H, Cao L, Sun B, Wei Y, Liang M (2019) Transcriptomic analysis of potential "lncRNA-mRNA" interactions in liver of the marine teleost Cynoglossus semilaevis fed diets with different DHA/EPA ratios. Front Physiol 10:331

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This study was supported by CONICYT/FONDAP/15110027 awarded to Juan Antonio Valdés and Alfredo Molina and CONICYT FONDECYT Postdoctorado 3180283 awarded to Phillip Dettleff.

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Authors and Affiliations

  1. Laboratory of Molecular Biotechnology, Faculty of Life Sciences, Andres Bello University, Republica 440, 8370186, Santiago, Chile

    Phillip Dettleff, Elizabeth Hormazabal, Jorge Aedo, Marcia Fuentes, Alfredo Molina & Juan Antonio Valdes

  2. Interdisciplinary Center for Aquaculture Research (INCAR), 4070386, Concepción, Chile

    Phillip Dettleff, Elizabeth Hormazabal, Jorge Aedo, Marcia Fuentes, Alfredo Molina & Juan Antonio Valdes

  3. Plant Biotechnology Center, Andres Bello University, 8370186, Santiago, Chile

    Claudio Meneses

  4. FONDAP Center for Genome Regulation, Andres Bello University, 8370186, Santiago, Chile

    Claudio Meneses

  5. CIMARQ, Andres Bello University, Quintay, Chile

    Alfredo Molina & Juan Antonio Valdes

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  1. Phillip Dettleff
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  2. Elizabeth Hormazabal
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  3. Jorge Aedo
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  6. Alfredo Molina
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  7. Juan Antonio Valdes
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Correspondence to Juan Antonio Valdes.

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Dettleff, P., Hormazabal, E., Aedo, J. et al. Identification and Evaluation of Long Noncoding RNAs in Response to Handling Stress in Red Cusk-Eel (Genypterus chilensis) via RNA-seq. Mar Biotechnol 22, 94–108 (2020). https://doi.org/10.1007/s10126-019-09934-6

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