Heat stress induced alternative splicing in catfish as determined by transcriptome analysis

Suxu Tan1, Wenwen Wang1, Changxu Tian1, Donghong Niu1,2, Tao Zhou1, Yulin Jin1, Yujia Yang1, Dongya Gao1, Rex Dunham1, Zhanjiang Liu3
1The Fish Molecular Genetics and Biotechnology Laboratory, School of Fisheries, Aquaculture and Aquatic Sciences, Auburn University, Auburn, AL 36849, USA
2College of Life Sciences, Shanghai Ocean University, Shanghai, China
3Department of Biology, College of Art and Sciences, Syracuse University, Syracuse, NY, 13244, USA

Tài liệu tham khảo

Ali, 2008, Regulation of alternative splicing of pre-mRNAs by stresses, vol. 326, 257 Aluru, 2009, Stress transcriptomics in fish: a role for genomic cortisol signaling, Gen. Comp. Endocrinol., 164, 142, 10.1016/j.ygcen.2009.03.020 Argue, 2003, Dress-out and fillet yields of channel catfish, Ictalurus punctatus, blue catfish, Ictalurus furcatus, and their F1, F2 and backcross hybrids, Aquaculture, 228, 81, 10.1016/S0044-8486(03)00245-X Barat, 2016, Transcriptional response to heat shock in liver of snow trout (Schizothorax richardsonii)—a vulnerable Himalayan Cyprinid fish, Funct. Integr. Genomics, 16, 203, 10.1007/s10142-016-0477-0 Basu, 2002, Heat shock protein genes and their functional significance in fish, Gene, 295, 173, 10.1016/S0378-1119(02)00687-X Ben-Dov, 2008, Genome-wide analysis of alternative pre-mRNA splicing, J. Biol. Chem., 283, 1229, 10.1074/jbc.R700033200 Bennett, 1997, Temperature tolerance of the sheepshead minnow, Cyprinodon variegatus, Copeia, 1997, 77, 10.2307/1447842 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 Bourgeois, 2003, Broad specificity of SR (serine/arginine) proteins in the regulation of alternative splicing of pre-messenger RNA, Prog. Nucleic Acid Res. Mol. Biol., 78, 37, 10.1016/S0079-6603(04)78002-2 Brander, 2010, Impacts of climate change on fisheries, J. Mar. Syst., 79, 389, 10.1016/j.jmarsys.2008.12.015 Buckley, 2006, The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis, J. Exp. Biol., 209, 2660, 10.1242/jeb.02292 Chang, 2007, The nonsense-mediated decay RNA surveillance pathway, Annu. Rev. Biochem., 76, 51, 10.1146/annurev.biochem.76.050106.093909 Cho, 2000, Transcription, genomes, function, Trends Genet., 16, 409, 10.1016/S0168-9525(00)02065-5 Cossins, 2005, Fish as models for environmental genomics, Nat. Rev. Genet., 6, 324, 10.1038/nrg1590 Dang, 2012, Influence of elevated temperatures on the immune response of abalone, Haliotis rubra, Fish Shellfish Immunol., 32, 732, 10.1016/j.fsi.2012.01.022 Dunham, 2018, Catfish biology and farming, Annu. Rev. Anim. Biosci., 6, 305, 10.1146/annurev-animal-030117-014646 Dunham, 1983, Relative tolerance of channel x blue hybrid and channel catfish to low oxygen concentrations, Prog. Fish Cult., 45, 55, 10.1577/1548-8659(1983)45[55:RTOCXB]2.0.CO;2 Dunham, 1987, Comparison of mass selection, crossbreeding, and hybridization for improving growth of channel catfish, Prog. Fish Cult., 49, 293, 10.1577/1548-8640(1987)49<293:COMSCA>2.0.CO;2 Dunham, 2008, Comparison of production traits of NWAC103 channel catfish, NWAC103 channel catfish × blue catfish hybrids, Kansas Select 21 channel catfish, and blue catfish grown at commercial densities and exposed to natural bacterial epizootics, N. Am. J. Aquac., 70, 98, 10.1577/A07-006.1 Fabregat, 2016, The reactome pathway knowledgebase, Nucleic Acids Res., 44, D481, 10.1093/nar/gkv1351 Ficke, 2007, Potential impacts of global climate change on freshwater fisheries, Rev. Fish Biol. Fish., 17, 581, 10.1007/s11160-007-9059-5 Foissac, 2007, ASTALAVISTA: dynamic and flexible analysis of alternative splicing events in custom gene datasets, Nucleic Acids Res., 35, W297, 10.1093/nar/gkm311 Fujikake, 2005, Alternative splicing regulates the transcriptional activity of Drosophila heat shock transcription factor in response to heat/cold stress, FEBS Lett., 579, 3842, 10.1016/j.febslet.2005.05.074 Goodson, 1995, Regulated expression of heat shock factor 1 isoforms with distinct leucine zipper arrays via tissue-dependent alternative splicing, Biochem. Biophys. Res. Commun., 211, 943, 10.1006/bbrc.1995.1903 Graveley, 2001, Alternative splicing: increasing diversity in the proteomic world, Trends Genet., 17, 100, 10.1016/S0168-9525(00)02176-4 Graveley, 2005, Mutually exclusive splicing of the insect Dscam pre-mRNA directed by competing intronic RNA secondary structures, Cell, 123, 65, 10.1016/j.cell.2005.07.028 Hentze, 2016, Molecular mechanism of thermosensory function of human heat shock transcription factor Hsf1, elife, 5, 10.7554/eLife.11576 Hori, 2010, Heat-shock responsive genes identified and validated in Atlantic cod (Gadus morhua) liver, head kidney and skeletal muscle using genomic techniques, BMC Genomics, 11, 72, 10.1186/1471-2164-11-72 Huang, 2015, Comparative transcriptomics uncovers alternative splicing changes and signatures of selection from maize improvement, BMC Genomics, 16, 363, 10.1186/s12864-015-1582-5 Huang, 2017, Recently amplified arctic warming has contributed to a continual global warming trend, Nat. Clim. Chang., 7, 875, 10.1038/s41558-017-0009-5 Iida, 2004, Genome-wide analysis of alternative pre-mRNA splicing in Arabidopsis thaliana based on full-length cDNA sequences, Nucleic Acids Res., 32, 5096, 10.1093/nar/gkh845 Jin, 2017, A genome-wide association study of heat stress-associated SNPs in catfish, Anim. Genet., 48, 233, 10.1111/age.12482 Kassahn, 2007, Heterologous microarray experiments used to identify the early gene response to heat stress in a coral reef fish, Mol. Ecol., 16, 1749, 10.1111/j.1365-294X.2006.03178.x Kelemen, 2013, Function of alternative splicing, Gene, 514, 1, 10.1016/j.gene.2012.07.083 Kew, 1970, Liver damage in heatstroke, Am. J. Med., 49, 192, 10.1016/S0002-9343(70)80075-4 Kim, 2013, TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions, Genome Biol., 14, R36, 10.1186/gb-2013-14-4-r36 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Lee, 2015, Mechanisms and regulation of alternative pre-mRNA splicing, Annu. Rev. Biochem., 84, 291, 10.1146/annurev-biochem-060614-034316 Lejeune, 2005, Mechanistic links between nonsense-mediated mRNA decay and pre-mRNA splicing in mammalian cells, Curr. Opin. Cell Biol., 17, 309, 10.1016/j.ceb.2005.03.002 Lewis, 2003, Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans, Proc. Natl. Acad. Sci., 100, 189, 10.1073/pnas.0136770100 Lewis, 2010, Transcriptome responses to heat stress in the nucleated red blood cells of the rainbow trout (Oncorhynchus mykiss), Physiol. Genomics, 42, 361, 10.1152/physiolgenomics.00067.2010 Li, 2004, Comparison of the channel catfish, Ictalurus punctatus (NWAC103 strain) and the channel × blue catfish, I. punctatus × I. furcatus, F1 hybrid for growth, feed efficiency, processing yield, and body composition, J. Appl. Aquac., 15, 63, 10.1300/J028v15n03_05 Lin, 2009, Alternative splicing and differential expression of two transcripts of nicotine adenine dinucleotide phosphate oxidase B gene from Zea mays, J. Integr. Plant Biol., 51, 287, 10.1111/j.1744-7909.2008.00808.x Lindquist, 1988, The heat-shock proteins, Annu. Rev. Genet., 22, 631, 10.1146/annurev.ge.22.120188.003215 Liu, 2013, An autoregulatory loop controlling Arabidopsis HsfA2 expression: role of heat shock-induced alternative splicing, Plant Physiol., 162, 512, 10.1104/pp.112.205864 Liu, 2013, RNA-Seq reveals expression signatures of genes involved in oxygen transport, protein synthesis, folding, and degradation in response to heat stress in catfish, Physiol. Genomics, 45, 462, 10.1152/physiolgenomics.00026.2013 Long, 2009, The SR protein family of splicing factors: master regulators of gene expression, Biochem. J., 417, 15, 10.1042/BJ20081501 Maquat, 2004, Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics, Nat. Rev. Mol. Cell Biol., 5, 89, 10.1038/nrm1310 Mastrangelo, 2012, Alternative splicing: enhancing ability to cope with stress via transcriptome plasticity, Plant Sci., 185, 40, 10.1016/j.plantsci.2011.09.006 Mehla, 2014, Genome-wide analysis of the heat stress response in Zebu (Sahiwal) cattle, Gene, 533, 500, 10.1016/j.gene.2013.09.051 Narum, 2013, Thermal adaptation and acclimation of ectotherms from differing aquatic climates, Mol. Ecol., 22, 3090, 10.1111/mec.12240 Neef, 2013, Genetic selection for constitutively trimerized human HSF1 mutants identifies a role for coiled-coil motifs in DNA binding, G3 (Bethesda), 3, 1315, 10.1534/g3.113.006692 Neudegger, 2016, Structure of human heat-shock transcription factor 1 in complex with DNA, Nat. Struct. Mol. Biol., 23, 140, 10.1038/nsmb.3149 Neueder, 2014, Novel isoforms of heat shock transcription factor 1, HSF1γα and HSF1γβ, regulate chaperone protein gene transcription, J. Biol. Chem., 289, 19894, 10.1074/jbc.M114.570739 Nikinmaa, 2013, Transcription and redox enzyme activities: comparison of equilibrium and disequilibrium levels in the three-spined stickleback, Proc. R. Soc. B, 280, 10.1098/rspb.2012.2974 Nilsen, 2010, Expansion of the eukaryotic proteome by alternative splicing, Nature, 463, 457, 10.1038/nature08909 Palusa, 2007, Alternative splicing of pre-mRNAs of Arabidopsis serine/arginine-rich proteins: regulation by hormones and stresses, Plant J., 49, 1091, 10.1111/j.1365-313X.2006.03020.x Pan, 2008, Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing, Nat. Genet., 40, 1413, 10.1038/ng.259 Pérez-Casanova, 2008, The immune and stress responses of Atlantic cod to long-term increases in water temperature, Fish Shellfish Immunol., 24, 600, 10.1016/j.fsi.2008.01.012 Pirkkala, 2001, Roles of the heat shock transcription factors in regulation of the heat shock response and beyond, FASEB J., 15, 1118, 10.1096/fj00-0294rev Podrabsky, 2004, Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus, J. Exp. Biol., 207, 2237, 10.1242/jeb.01016 Prunet, 2008, Functional genomics of stress responses in fish, Rev. Fish. Sci., 16, 157, 10.1080/10641260802341838 Purohit, 2014, Investigating hsp gene expression in liver of Channa striatus under heat stress for understanding the upper thermal acclimation, Biomed. Res. Int., 2014, 10.1155/2014/381719 Rabergh, 2000, Tissue-specific expression of zebrafish (Danio rerio) heat shock factor 1 mRNAs in response to heat stress, J. Exp. Biol., 203, 1817, 10.1242/jeb.203.12.1817 Salamov, 2000, Ab initio gene finding in Drosophila genomic DNA, Genome Res., 10, 516, 10.1101/gr.10.4.516 Sammeth, 2008, A general definition and nomenclature for alternative splicing events, PLoS Comput. Biol., 4, 10.1371/journal.pcbi.1000147 Shen, 2014, rMATS: robust and flexible detection of differential alternative splicing from replicate RNA-Seq data, Proc. Natl. Acad. Sci., 111, E5593, 10.1073/pnas.1419161111 Sievers, 2014, Clustal Omega, accurate alignment of very large numbers of sequences, vol. 1079, 105 Smith, 2013, RNA-seq analysis reveals extensive transcriptional plasticity to temperature stress in a freshwater fish species, BMC Genomics, 14, 375, 10.1186/1471-2164-14-375 Smitherman, 1985, Genetics and breeding, 283 Song, 2014, Genome-wide identification of Hsp40 genes in channel catfish and their regulated expression after bacterial infection, PLoS One, 9, 10.1371/journal.pone.0115752 Staiger, 2013, Alternative splicing at the intersection of biological timing, development, and stress responses, Plant Cell, 25, 3640, 10.1105/tpc.113.113803 Stamm, 2005, Function of alternative splicing, Gene, 344, 1, 10.1016/j.gene.2004.10.022 Tan, 2018, Increased alternative splicing as a host response to Edwardsiella ictaluri infection in catfish, Mar. Biotechnol., 10.1007/s10126-018-9844-2 Trapnell, 2012, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks, Nat. Protoc., 7, 562, 10.1038/nprot.2012.016 Wang, 2008, Alternative isoform regulation in human tissue transcriptomes, Nature, 456, 470, 10.1038/nature07509 Werner, 2007, The effect of temperature stress on development and heat-shock protein expression in larval green sturgeon (Acipenser mirostris), Environ. Biol. Fish, 79, 191, 10.1007/s10641-006-9070-z Wiseman, 2007, Gene expression pattern in the liver during recovery from an acute stressor in rainbow trout, Comp. Biochem. Physiol. D, 2, 234 Wollerton, 2004, Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay, Mol. Cell, 13, 91, 10.1016/S1097-2765(03)00502-1 Xie, 2015, Hsp90, Hsp60 and sHsp families of heat shock protein genes in channel catfish and their expression after bacterial infections, Fish Shellfish Immunol., 44, 642, 10.1016/j.fsi.2015.03.027 Yabas, 2015, The role of alternative splicing in the control of immune homeostasis and cellular differentiation, Int. J. Mol. Sci., 17, 3, 10.3390/ijms17010003 Zuo, 1994, Activation of the DNA-binding ability of human heat shock transcription factor 1 may involve the transition from an intramolecular to an intermolecular triple-stranded coiled-coil structure, Mol. Cell. Biol., 14, 7557, 10.1128/MCB.14.11.7557