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RNA-seq Analysis Reveals Alternative Splicing Under Heat Stress in Rainbow Trout (Oncorhynchus mykiss)

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Abstract

Rainbow trout (Oncorhynchus mykiss) is one of the most economically important cold-water farmed species in the world, and transcriptomic studies in response to heat stress have been conducted and will be studied in depth. Alternative splicing (AS), a post-transcriptional regulatory process that regulates gene expression and increases proteomic diversity, is still poorly understood in rainbow trout under heat stress. In the present study, 18,623 alternative splicing events were identified from 9936 genes using RNA transcriptome sequencing technology (RNA-Seq) and genomic information. A total of 2731 differential alternative splicing (DAS) events were found among 2179 differentially expressed genes (DEGs). Gene ontology analysis revealed that the DEGs were mainly enriched in cellular metabolic process, cell part, and organic cyclic compound binding under heat stress. Kyoto Encyclopedia of Genes and Genomes pathway enrichment analysis displayed that the DEGs were enriched for 39 pathways, and some key pathways, such as lysine degradation, are involved in the regulation of heat stress in liver tissues of rainbow trout. The results were validated by qRT-PCR, confirming reliability of our bioinformatics analysis.

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References

  • Andrews S (2010) FastQC: a quality control tool for high throughput sequence data, Babraham bioinformatics, Babraham Institute, Cambridge, United Kingdom

  • Baird NA, Douglas PM, Simic MS, Grant AR, Moresco JJ, Wolff SC, Yates JR, Manning G, Dillin A (2014) HSF-1-mediated cytoskeletal integrity determines thermotolerance and life span. Science 346:360–363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbazuk WB, Fu Y, McGinnis KM (2008) Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res 18:1381–1392

    Article  CAS  PubMed  Google Scholar 

  • Barta A, Kalyna M, Lorkovic ZJ (2008) Plant SR proteins and their functions. Curr Top Microbiol Immunol 326:83–102

    CAS  PubMed  Google Scholar 

  • Barta A, Kalyna M, Reddy AS (2010) Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell 22:2926–2929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basu N, Todgham AE, Ackerman PA, Bibeau MR, Nakano K, Schulte PM, Iwama GK (2002) Heat shock protein genes and their functional significance in fish. Gene 295:173–183

    Article  CAS  PubMed  Google Scholar 

  • Berget SM, Moore C, Sharp PA (2000) Spliced segments at the 5’ terminus of adenovirus 2 late mRNA. 1977. Rev Med Virol 10:356–362

    CAS  PubMed  Google Scholar 

  • Bessa C, Matos P, Jordan P, Gonçalves V (2020) Alternative splicing: expanding the landscape of cancer biomarkers and therapeutics. Int J Mol Sci 21:9032

    Article  CAS  PubMed Central  Google Scholar 

  • Biamonti G, Caceres JF (2009) Cellular stress and RNA splicing. Trends Biochem Sci 34:146–153

    Article  CAS  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chacko E, Ranganathan S (2009) Comprehensive splicing graph analysis of alternative splicing patterns in chicken, compared to human and mouse. BMC Genomics 10:S5

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang CY, Lin WD, Tu SL (2014) Genome-wide analysis of heat sensitive alternative splicing in Physcomitrella patens. Plant Physiol 165:826–840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang YW, Wang YC, Zhang XX, Iqbal J, Lu MX, Du YZ (2021) Transcriptional regulation of small heat shock protein genes by heat shock factor 1 (HSF1) in Liriomyza trifolii under heat stress. Cell Stress Chaperones 26:835–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cossins AR, Crawford DL (2005) Fish as models for environmental genomics. Nat Rev Genet 6:324–333

    Article  CAS  PubMed  Google Scholar 

  • De AL, Alper S (2013) Limiting of the innate immune response by SF3A-dependent control of MyD88 alternative mRNA splicing. PLoS Genet 9:e1003855

  • De AL, Seng A, Lackford B, Keikhaee MR, Bowerman B, Freedman JH, Schwartz DA, Alper S (2013) An evolutionarily conserved innate immunity protein interaction network. J Biol Chem 288:1967–1978

    Article  Google Scholar 

  • Elliott DJ, Grellscheld SN (2006) Alternative RNA splicing regulation in the testis. Reproduction 132:811–819

    Article  CAS  PubMed  Google Scholar 

  • Foissac S, Sammeth M (2015) Analysis of alternative splicing events in custom gene datasets by AStalavista. Methods Mol Biol 1269:379–392

    Article  CAS  PubMed  Google Scholar 

  • Fujikake N, Nagai Y, Popiel HA, Kano H, Yamaguchi M, Toda T (2005) Alternative splicing regulates the transcriptional activity of Drosophila heat shock transcription factor in response to heat/cold stress. FEBS Lett 579:3842–3848

    Article  CAS  PubMed  Google Scholar 

  • Ge Y, Schuster MB, Pundhir S et al (2019) The splicing factor RBM25 controls MYC activity in acute myeloid leukemia. Nat Commun 10:172

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong NP, Björnsson BT (2014) Leptin signaling in the rainbow trout central nervous system is modulated by a truncated leptin receptor isoform. Endocrinology 155:2445–2455

    Article  PubMed  Google Scholar 

  • Grczynski SF, Cattaneo AM, Walker WB (2019) Alternative splicing of the cpomOR53 gene produces three transcripts expressed in Codling Moth (Lepidoptera: Tortricidae) Antennae. J Econ Entomol 112:991–996

    Article  Google Scholar 

  • Hansen KD, Brenner SE, Dudoit S (2010) Biases in Illumina transcriptome sequencing caused by random hexamer priming. Nucleic Acids Res 38:e131

  • Hao Y, Feng YJ, Yang P, Cui YJ, Liu J, Yang CH, Gu XH (2016) Transcriptome analysis reveals that constant heat stress modifies the metabolism and structure of the porcine longissimus dorsi skeletal muscle. Mol Genet Genomics 291:2101–2115

    Article  CAS  PubMed  Google Scholar 

  • Hartl FU, Hayer-HM (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science (New York, N.Y.) 295:1852–1858

  • Hartmuth K, Barta A (1986) In vitro processing of a plant pre-mRNA in a HeLa cell nuclear extract. Nucleic Acids Res 14:7513–7528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He ZS, Xie R, Zou HS, Wang YZ, Zhu JB, Yu GQ (2007) Structure and alternative splicing of a heat shocktranscription factor gene, MsHSF1, in Medicago sativa. Biochem Bioph Res Co 364:1056–1061

    Article  CAS  Google Scholar 

  • Healy TM, Schulte PM (2019) Patterns of alternative splicing in response to cold acclimation in fish. J Exp Biol 222:jeb193516

  • Hentze N, Le BL, Wiesner J, Kempf G, Mayer MP (2016) Molecular mechanism of thermosensory function of human heat shock transcription factor Hsf1. Elife 5:e11576

  • Huang BY, Zhang LL, Tang XY, Zhang GF, Li L (2016) Genome-wide analysis of alternative splicing provides insights into stress adaptation of the Pacific Oyster. Mar Biotechnol (NY) 18:598–609

    Article  CAS  Google Scholar 

  • Iwama GK, Afonso LOB, Todgham A, Ackerman PNK (2004) Are hsps suitable for indicating stressed states in fish? J Exp Biol 207:15–19

    Article  CAS  PubMed  Google Scholar 

  • Iwata H, Gotoh O (2011) Comparative analysis of information contents relevant to recognition of introns in many species. BMC Genomics 12:45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jaksic AM, Schlotterer C (2016) The interplay of temperature and genotype on patterns of alternative splicing in Drosophila melanogaster. Genetics 204:315–325

    Article  PubMed  PubMed Central  Google Scholar 

  • Jurica MS, Moore MJ (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12:5–14

    Article  CAS  PubMed  Google Scholar 

  • Kalsotra A, Cooper TA (2011) Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 12:715–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kannan S, Halter G, Renner T, Waters ER (2018) Patterns of alternative splicing vary between species during heat stress. AoB Plants 10:ply013

  • Kelemen O, Convertini P, Zhang ZY, Wen Y, Shen M, Falaleeva M, Stamm S (2013) Function of alternative splicing. Gene 514:1–30

    Article  CAS  PubMed  Google Scholar 

  • Keller M, Hu YJ, Mesihovic A, Fragkostefanakis S, Schleiff E, Simm S (2017) Alternative splicing in tomato pollen in response to heat stress(aEuro). DNA Res 24:205–217

    CAS  PubMed  Google Scholar 

  • Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

    Article  PubMed  PubMed Central  Google Scholar 

  • Krone PH, Lele Z, Sass JB (1997) Heat shock genes and the heat shock response in zebrafish embryos. Biochem Cell Biol 75:487–497

    Article  CAS  PubMed  Google Scholar 

  • Lan DL, Xiong XR, Wei YL, Xu T, Zhong JC, Zhi XD, Wang Y, Li J (2014) RNA-Seq analysis of yak ovary: improving yak gene structure information and mining reproduction-related genes. Sci China Life Sci 57:925–935

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Rio DC (2015) Mechanisms and regulation of alternative pre-mRNA splicing. Annu Rev Biochem 84:291–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ling Y, Serrano N, Gao G, Atia M, Mokhtar M, Woo YH, Bazin J, Veluchamy A, Benhamed M, Crespi M, Gehring C, Reddy ASN, Mahfouz MM (2018) Thermopriming triggers splicing memory in Arabidopsis. J Exp Bot 69:2659–2675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XX, Shi HN, Liu Z, Kang YJ, Huang JQ (2019) Effect of heat stress on heat shock protein 30 (Hp30) mRNA expression in rainbow trout (Oncorhynchus mykiss). Turk J Fish Aquat Sc 19:681–688

    Google Scholar 

  • Marquez Y, Brown JW, Simpson C, Barta A, Kalyna M (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22:1184–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Modrek B, Lee CJ (2003) Alternative splicing in the human, mouse and rat genomes is associated with an increased frequency of exon creation and/or loss. Nat Genet 34:177–180

    Article  CAS  PubMed  Google Scholar 

  • Mottola G, Nikinmaa M, Anttila K (2020) Hsp70s transcription-translation relationship depends on the heat shock temperature in zebrafish. Comp Biochem Phys A 240:110629

  • Munoz MJ, Perez Santangelo MS, Paronetto MP, de la Mata M, Pelisch F, Boireau S, Glover-Cutter K, Ben-Dov C, Blaustein M, Lozano JJ, Bird G, Bentley D, Bertrand E, Kornblihtt AR (2009) DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation. Cell 137:708–720

    Article  CAS  PubMed  Google Scholar 

  • Nakai A, Morimoto RI (1993) Characterization of a novel chicken heat shock transcription factor, heat shock factor 3, suggests a new regulatory pathway. Mol Cell Biol 13:1983–1997

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neef DW, Jaeger AM, Thiele DJ (2013) Genetic selection for constitutively trimerized human HSF1 mutants identifies a role for coiled-coil motifs in DNA binding. G3-Genes Genom Genet 3:1315–1324

  • Neudegger T, Verghese J, Hayer-Hartl M, Hartl FU, Bracher A (2016) Structure of human heat-shock transcription factor 1 in complex with DNA. Nat Struct Mol Biol 23:140–146

    Article  CAS  PubMed  Google Scholar 

  • Neueder A, Achilli F, Moussaoui S, Bates GP (2014) Novel isoforms of heat shock transcription factor 1, HSF1γα and HSF1γβ, regulate chaperone protein gene transcription. J Biol Chem 289:19894–19906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsen TW, Graveley BR (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature 463:457–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ojima N, Yamashita M (2004) Cloning and characterization of two distinct isoforms of rainbow trout heat shock factor 1. Evidence for heterotrimer formation. Eur J Biochem 271:703–712

    Article  CAS  PubMed  Google Scholar 

  • Palusa SG, Ali GS, Reddy ASN (2007) Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses. Plant J 49:1091–1107

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ (2008) Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40:1413–1415

    Article  CAS  PubMed  Google Scholar 

  • Panter PE, Knight H, Nimmo HG, Zhang R, Brown JWS (2018) Rapid and dynamic alternative splicing impacts the Arabidopsis cold response transcriptome. Plant Cell 30:1424–1444

    Article  PubMed  PubMed Central  Google Scholar 

  • Pérez-Casanova JC, Rise ML, Dixon B, Afonso LOB, Hall JR, Johnson SC, Gamperl AK (2008) The immune and stress responses of Atlantic cod to long-term increases in water temperature. Fish Shellfish Immunol 24:600–609

    Article  PubMed  Google Scholar 

  • Pirkkala L, Nykänen P, Sistonen LEA (2001) Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15:1118–1131

    Article  CAS  PubMed  Google Scholar 

  • Purohit GK, Mahanty A, Suar M, Sharma AP, Mohanty BP, Mohanty S (2014) Investigating hsp gene expression in liver of Channa striatus under heat stress for understanding the upper thermal acclimation. Biomed Res Int 2014:381719

  • Quan JQ, Kang YJ, Luo ZC, Zhao GY, Ma F, Li LL, Liu Z (2020) Identification and characterization of long noncoding RNAs provide insight into the regulation of gene expression in response to heat stress in rainbow trout (Oncorhynchus mykiss). Comp Biochem Phys D 36:100707

  • Rabergh CMI, Airaksinen S, Soitamo A, Bjo¨ rklund HV, Johansson T, Nikinmaa M, Sistonen L, (2000) Tissue-specific expression of zebrafish (Danio rerio) heat shock factor 1 mRNAs in response to heat stress. J Exp Biol 203:1817–1824

    Article  CAS  PubMed  Google Scholar 

  • Rabindran SK, Giorgi G, Clos J, Wu C (1991) Molecular cloning and expression of a human heat shock factor, HSF1. P Natl Acad Sci USA 88:6906–6910

    Article  CAS  Google Scholar 

  • Rappsilber J, Ryder U, Lamond AI, Matthias M (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res 12:1231–1245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossner P, Vrbova K, Strapacova S, Rossnerova A, Ambroz A, Brzicova T, Libalova H, Javorkova E, Kulich P, Vecera Z, Mikuska P, Coufalik P, Krumal K, Capka L, Docekal B, Moravec P, Sery O, Misek I, Fictum P, Fiser K, Machala M, Topinka J (2019) Inhalation of ZnO nanoparticles: splice junction expression and alternative splicing in mice. Toxicol Sci 168:190–200

    Article  CAS  PubMed  Google Scholar 

  • Sammeth M, Foissac S, Guigó R (2008) A general definition and nomenclature for alternative splicing events. PLoS Comput Biol 4:e1000147

  • Sarge KD, Zimarino V, Holm K, Wu C, Morimoto RI (1991) Cloning and characterization of two mouse heat shock factors with distinct inducible and constitutive DNA-binding ability. Genes Dev 5:1902–1911

    Article  CAS  PubMed  Google Scholar 

  • Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (HSF) family: structure, function and evolution. BBA-Gene Regul Mech 1819:104–119

    CAS  Google Scholar 

  • Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL (2000) Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101:671–684

    Article  CAS  PubMed  Google Scholar 

  • Shen SH, Park JW, Lu ZX, LL, Henry MD, Wu YN, ZQ, Xing Y, (2014) rMATS: robust and flexible detection of differential alternative splicing from replicate RNA-Seq data. Proc Natl Acad Sci USA 111:E5593–E5601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi HN, Liu Z, Zhang JP, Kang YJ, Wang JF, Huang JQ, Wang WM (2015) Effect of heat stress on heat-shock protein (Hsp60) mRNA expression in rainbow trout Oncorhynchus mykiss. Genet Mol Res 14:5280–5286

    Article  CAS  PubMed  Google Scholar 

  • Song L, Pan ZZ, Chen L, Dai Y, Wan JR, Ye H, Nguyen HT, Zhang GZ, Chen HT (2020) Analysis of whole transcriptome RNA-seq data reveals many alternative splicing events in soybean roots under drought stress conditions. Genes 11:1520

    Article  CAS  PubMed Central  Google Scholar 

  • Staiger D, Brown JWS (2013) Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25:3640–3656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan SX, Wang WW, Tian CG, Niu DH, Zhou T, Yang YJ, Gao DY, Liu ZJ (2019a) Post-transcriptional regulation through alternative splicing after infection with Flavobacterium columnare in channel catfish (Ictalurus punctatus). Fish Shellfish Immunol 91:188–193

    Article  CAS  PubMed  Google Scholar 

  • Tan SX, Wang WW, Tian CX, Niu DH, Zhou T, Jin YL, Yang YJ, Gao DY, Dunham R, Liu ZJ (2019b) Heat stress induced alternative splicing in catfish as determined by transcriptome analysis. Comp Biochem Phys D 29:166–172

    CAS  Google Scholar 

  • Tan SX, Wang WW, Zhong XX, Tian CG, Niu DH, Bao LS, Zhou T, Jin YL, Yang YJ, Yuan ZH, Gao DY, Dunham R, Liu ZJ (2018) Increased alternative splicing as a host response to Edwardsiella ictaluri infection in catfish. Mar Biotechnol 20:729–738

    Article  CAS  Google Scholar 

  • Tanabe M, Sasai N, Nagata K, Liu XD, Liu PCC, Thiele DJ, Nakai A (1999) The Mammalian HSF4 gene generates both an activator and a repressor of heat shock genes by alternative splicing. J Biol Chem 274:27845–27856

    Article  CAS  PubMed  Google Scholar 

  • Tian J, Liu YP, Zhu BB, Tian Y, Zhong R, Chen W, Lu XG, Zou L, Shen N, Qian JM, Li H, Miao XP, Wang L (2015) SF3A1 and pancreatic cancer: new evidence for the association of the spliceosome and cancer. Oncotarget 6:37750–37757

    Article  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treutlein B, Gokce O, Quake SR, Südhof TC (2014) Cartography of neurexin alternative splicing mapped by single-molecule long-read mRNA sequencing. Proc Natl Acad Sci USA 111:E1291–E1299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker NR, Middleton RC, Le QP, Shelden EA (2011) HSF1 is essential for the resistance of zebrafish eye and brain to hypoxia/reperfusion injury. PLoS One 6:e22268

  • Vitulo N, Forcato C, Carpinelli EC, Telatin A, Campagna D, D’Angelo M, Zimbello R, Corso M, Vannozzi A, Bonghi C, Lucchin M, Valle G (2014) A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biol 14:99

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang ET, Sandberg R, Luo SJ, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456:470–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XY, Du LY, Wei H, Zhang AY, Yang K, Zhou H (2018) Identification of two Stat3 variants lacking a transactivation domain in grass carp: new insights into alternative splicing in the modification of teleost Stat3 signaling. Fish Shellfish Immunol 77:13–21

    Article  PubMed  Google Scholar 

  • Wang ZJ, Ji HT, Yuan BJ, Wang SF, Su C, Yao B, Zhao HT, Li X (2015) ABA signalling is fine-tuned by antagonistic HAB1 variants. Nat Commun 6:8138

    Article  PubMed  Google Scholar 

  • Werner I, Linares-Casenave J, Eenennaam J, Doroshov SI (2007) The effect of temperature stress on developmentand heat-shock protein expression in larval green sturgeon (acipenser mirostris). Environ Bio Fish 79:191–200

    Article  Google Scholar 

  • Wiseman S, Osachoff H, Bassett E, Malhotra J, Bruno J, Vanaggelen G, Mommsen TP, Vijayan MM (2007) Gene expression pattern in the liver during recovery from an acute stressor in rainbow trout. Comp Biochem Phys D 2:234–244

    Google Scholar 

  • Wong WK, Mockler TC (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 20:45–58

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu Z, Liang JH, Wang CP, Ding LP, Zhao X, Cao X, Xu SJ, Teng NJ, Yi MF (2019) Alternative splicing provides a mechanism to regulate LlHSFA3 function in response to heat stress in lily. Plant Physiol 181:1651–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia JH, Li HL, Li BJ, Gu XH, Lin HR (2018) Acute hypoxia stress induced abundant differential expression genes and alternative splicing events in heart of tilapia. Gene 639:52–61

    Article  CAS  PubMed  Google Scholar 

  • Xu ZX, Gan L, Li TY, Xu C, Chen K, Wang XD, Qin JG, Chen LQ, Li ER (2015) Transcriptome profiling and molecular pathway analysis of genes in association with salinity adaptation in nile tilapia oreochromis niloticus. PLoS One 10:e0136506

  • Yabas M, Elliott H, Hoyne GF (2015) The role of alternative splicing in the control of immune homeostasis and cellular differentiation. Int J Mol Sci 17:3

    Article  PubMed Central  Google Scholar 

  • Yan K, Liu P, Wu CA, Yang GD, Xu R, Guo QH, Huang JG, Zheng CC (2012) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48:521–531

    Article  CAS  PubMed  Google Scholar 

  • Yang YC, Guo WX, Shen X, Li JF, Yang SH, Chen SF, He ZW, Zhou RC, Shi SH (2018) Identification and characterization of evolutionarily conserved alternative splicing events in a mangrove genus Sonneratia. Sci Rep 8:4425

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang XX, Yuan JB, Zhang XJ, Liu CZ, Xiang JH, Li FH (2019) Genome-wide analysis of alternative splicing provides insights into stress response of the pacific white shrimp Litopenaeus vannamei. Front Genet 10:845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Cai Q, Shu XO (2015) Whole-exome sequencing identifies novel somatic mutations in chinese breast cancer patients. J Mol Genet Med 9

  • Zhou A, Ou AC, Cho A (2008) Novel splicing factor RBM25 modulates Bcl-x pre-mRNA 5’ splice site selection. Mol Cell Biol 28:5924–5936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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The study was supported by the National Natural Science Foundation of China (31960727). The funding bodies had no role in the design of the study; the collection, analysis, and interpretation of the data; or the writing of the manuscript.

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Sun, J., Liu, Z., Quan, J. et al. RNA-seq Analysis Reveals Alternative Splicing Under Heat Stress in Rainbow Trout (Oncorhynchus mykiss). Mar Biotechnol 24, 5–17 (2022). https://doi.org/10.1007/s10126-021-10082-z

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