Gene expression during different periods of the handlingstress response in <i>Pampus argenteus</i> -- Journal of Oceanology and Limnology,2018,36(4):1349-1359

	Cite this paper:
	SUN Peng, TANG Baojun, YIN Fei. Gene expression during different periods of the handlingstress response in Pampus argenteus[J]. Journal of Oceanology and Limnology, 2018, 36(4): 1349-1359

Gene expression during different periods of the handlingstress response in Pampus argenteus

SUN Peng, TANG Baojun, YIN Fei

Key Laboratory of East China Sea Fishery Resources Exploitation, Ministry of Agriculture;East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai 200090, China

Abstract:

Common aquaculture practices subject fish to a variety of acute and chronic stressors. Such stressors are inherent in aquaculture production but can adversely affect survival, growth, immune response, reproductive capacity, and behavior. Understanding the biological mechanisms underlying stress responses helps with methods to alleviate the negative effects through better aquaculture practices, resulting in improved animal welfare and production efficiency. In the present study, transcriptome sequencing of liver and kidney was performed in silver pomfret (Pampus argenteus) subjected to handling stress versus controls. A total of 162.19 million clean reads were assembled to 30 339 unigenes. The quality of the assembly was high, with an N50 length of 2 472 bases. For function classification and pathway assignment, the unigenes were categorized into three GO (gene ontology) categories, twenty-six clusters of eggNOG (evolutionary genealogy of genes:non-supervised orthologous groups) function categories, and thirty-eight KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways. Stress affected different functional groups of genes in the tissues studied. Differentially expressed genes were mainly involved in metabolic pathways (carbohydrate metabolism, lipid metabolism, amino-acid metabolism, uptake of cofactors and vitamins, and biosynthesis of other secondary metabolites), environmental information processing (signaling molecules and their interactions), organismal systems (endocrine system, digestive system), and disease (immune, neurodegenerative, endocrine and metabolic diseases). This is the first reported analysis of genome-wide transcriptome in P. argenteus, and the findings expand our understanding of the silver pomfret genome and gene expression in association with stress. The results will be useful to future analyses of functional genes and studies of healthy artificial breeding in P. argenteus and other related fish species.

Key words: gene ontology|immune system|next-generation sequencing|transcriptome|unigenes

Received: 2017-01-13 Revised:

Tools

PDF (489 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by SUN Peng

Articles by TANG Baojun

Articles by YIN Fei

References:
Almatar S M, Lone K P, Abu-Rezq T S, Yousef A A. 2004.Spawning frequency, fecundity, egg weight and spawning type of silver pomfret, Pampus argenteus (Euphrasen)(Stromateidae), in Kuwait waters. J. Appl. Ichthy., 20(3):176-188.
Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Gen. Biol., 11:R106.
Bolasina S N. 2011. Stress response of juvenile flounder(Paralichthys orbignyanus, Valenciennes 1839), to acute and chronic stressors. Aquaculture, 313(1-4):140-143.
Bonga S E W. 1997. The stress response in fish. Physiol. Rev., 77(3):591-625.
Cairns M T, Johnson M C, Talbot A T, Pemmasani J K, McNeill R E, Houeix B, Sangrador-Vegas A, Pottinger T G. 2008.
A cDNA microarray assessment of gene expression in the liver of rainbow trout (Oncorhynchus mykiss) in response to a handling and confinement stressor. Comp. Biochem.Physiol. D, 3(1):51-66.
Campbell P M, Pottinger T G, Sumpter J P. 1992. Stress reduces the quality of gametes produced by rainbow trout.Biol. Reprod., 47(6):1 140-1 150.
Cara J B, Aluru N, Moyano F J, Vijayan M M. 2005. Fooddeprivation induces HSP70 and HSP90 protein expression in larval gilthead sea bream and rainbow trout. Comp.Biochem. Physiol. B, 142(4):426-431.
Castanheira M F, Herrera M, Costas B, Conceição L E C, Martins C I M. 2013. Linking cortisol responsiveness and aggressive behaviour in gilthead seabream Sparus aurata:Indication of divergent coping styles. Appl. Anim. Behav.Sci., 143(1):75-81.
Chen F F, Lin H B, Li J C, Wang Y, Li J, Zhang D G, Yu W Y. 2017. Grass carp (Ctenopharyngodon idellus) invariant chain of the MHC class Ⅱ chaperone protein associates with the class I molecule. Fish Shellfish Immunol., 63:1-8.
Davis K B. 2006. Management of physiological stress in finfish aquaculture. North Am. J. Aquac., 68(2):116-121.
Don Wickramaarachchi W, Wan Q, Lee Y, Lim B S, De Zoysa M, Oh M J, Jung S J, Kim H C, Whang I, Lee J. 2012.Genomic characterization and expression analysis of complement component 9 in rock bream (Oplegnathus fasciatus). Fish Shellfish Immunol., 33(4):707-717.
Fiol D F, Chan S Y, Kültz D. 2006. Identification and pathway analysis of immediate hyperosmotic stress responsive molecular mechanisms in tilapia (Oreochromis mossambicus) gill. Comp. Biochem. Physiol. D, 1(3):344-356.
Gao Q X, Gao Q, Min M H, Zhang C J, Peng S M, Shi Z H.2016. Ability of Lactobacillus plantarum lipoteichoic acid to inhibit Vibrio anguillarum-induced inflammation and apoptosis in silvery pomfret (Pampus argenteus) intestinal epithelial cells. Fish Shellfish Immunol., 54:573-579.
Geiger J H, Jin X S. 2006. The structure and mechanism of myo-inositol 1-phosphate synthase. In Subcellular Biochemistry, Vol. 39 (ed. A. L. Majumder and B. B.Biswas), Springer. p.157-180.
Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q D, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome.Nat. Biotechnol., 29(7):644-652.
Grimholt U, Larsen S, Nordmo R, Midtlyng P, Kjoeglum S, Storset A, Saebø S, Stet R J M. 2003. MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar);facing pathogens with single expressed major histocompatibility class I and class Ⅱ loci.Immunogenetics, 55(4):210-219.
Guo B Y, Wu C W, Lv Z M, Liu C L. 2016. Characterisation and expression analysis of two terminal complement components:C7 and C9 from large yellow croaker, Larimichthys crocea. Fish Shellfish Immunol., 51:211-219.
Haas B J, Papanicolaou A, Yassour M, Grabherr M, Blood P D, Bowden J, Couger M B, Eccles D, Li B, Lieber M, MacManes M D, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey C N, Henschel R, LeDuc R D, Friedman N, Regev A. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis.Nat. Protoc., 8(8):1 494-1 512.
Harmon T S. 2009. Methods for reducing stressors and maintaining water quality associated with live fish transport in tanks:a review of the basics. Rev. Aquac., 1(1):58-66.
Heratha H M L P B, Elvitigalaa D A S, Godahewa G I, Umasuthana N, Whang I, Nohc J K, Lee J. 2016.Molecular characterization and comparative expression analysis of two teleostean pro-inflammatory cytokines, IL-1β and IL-8, from Sebastes schlegeli. Gene, 575(2):732-742.
Hoskonen P, Pirhonen J. 2006. Effects of repeated handling, with or without anaesthesia, on feed intake and growth in juvenile rainbow trout, Oncorhynchus mykiss (Walbaum).Aqua. Res., 37(4):409-415.
Huang X X, Yin Y Q, Shi Z H, Li W W, Zhou H Q, Lv W Q. 2010. Lipid content and fatty acid composition in wildcaught silver pomfret (Pampus argenteus) broodstocks:effects on gonad development. Aquaculture, 310(1-2):192-199.
Jia R, Liu B L, Feng W R, Han C, Huang B, Lei J L. 2016.Stress and immune responses in skin of turbot(Scophthalmus maximus) under different stocking densities. Fish Shellfish Immunol., 55:131-139, https://doi.org/10.1016/j.fsi.2016.05.032.
Kajimura S, Kawaguchi N, Kaneko T, Kawazoe I, Hirano T, Visitacion N, Grau E G, Aida K. 2004. Identification of the growth hormone receptor in an advanced teleost, the tilapia (Oreochromis mossambicus) with special reference to its distinct expression pattern in the ovary. J.Endocrinol., 181(1):65-76.
Krasnov A, Koskinen H, Pehkonen P, Rexroad C, Afanasyev S, Mölsä H. 2005. Gene expression in the brain and kidney of rainbow trout in response to handling stress.BMC Genomics, 6:3.
Lefèvre F, Bugeon J, Aupérin B, Aubin J. 2008. Rearing oxygen level and slaughter stress effects on rainbow trout flesh quality. Aquaculture, 284(1-4):81-89.
Li Y J, Huang J Q, Liu Z, Zhou Y J, Xia B P, Wang Y J, Kang Y J, Wang J F. 2017. Transcriptome analysis provides insights into hepatic responses to moderate heat stress in the rainbow trout (Oncorhynchus mykiss). Gene, 619:1-9.
Liu J, Li C S, Ning P. 2013. Identity of silver pomfret Pampus argenteus (Euphrasen, 1788) based on specimens from its type locality, with a neotype designation (Teleostei, Stromateidae). Acta Zootaxonomica Sinica, 38(1):171-177.
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetJ, 17(1):10-12.
Momoda T S, Schwindt A R, Feist G W, Gerwick L, Bayne C J, Schreck C B. 2007. Gene expression in the liver of rainbow trout, Oncorhynchus mykiss, during the stress response. Comp. Biochem. Physiol. D, 2(4):303-315.
Morozova O, Marra M A. 2008. Applications of nextgeneration sequencing technologies in functional genomics. Genomics, 92(5):255-264.
Mortazavi A, Williams B A, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods, 5(7):621-628.
Nakano T, Afonso L O B, Beckman B R, Iwama G K, Devlin R H. 2013. Acute physiological stress down-regulates mRNA expression of growth-related genes in Coho salmon. PloS One, 8(8):e71421, https://doi.org/10.1371/journal.pone.0071421.
Olsen R E, Sundell K, Mayhew T M, Myklebust R, Ring E. 2005. Acute stress alters intestinal function of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture, 250(1-2):480-495.
Øverli O, Winberg S, Pottinger T G. 2005. Behavioral and neuroendocrine correlates of selection for stress responsiveness in rainbow trout-a review. Integr. Comp.Biol., 45(3):463-474.
Ozsolak F, Milos P M. 2011. RNA sequencing:advances, challenges and opportunities. Nat. Rev. Genet., 12(2):87-98.
Parma L, Candela M, Soverini M, Turroni S, Consolandi C, Brigidi P, Mandrioli L, Sirri R, Fontanillas R, Gatta P P, Bonaldo A. 2016. Next-generation sequencing characterization of the gut bacterial community of gilthead sea bream (Sparus aurata, L.) fed low fishmeal based diets with increasing soybean meal levels. Anim.Feed Sci. Tech., 222:204-216.
Peters M B, Turner T F. 2008. Genetic variation of the major histocompatibility complex (MHC class Ⅱ β gene) in the threatened Gila trout, Oncorhynchus gilae gilae. Conserv.Genet., 9(2):257-270.
Pierce A L, Fox B K, Davis L K, Visitacion N, Kitahashi T, Hirano T, Grau E G. 2005. Prolactin receptor, growth hormone receptor, and putative somatolactin receptor in Mozambique tilapia:tissue specific expression and differential regulation by salinity and fasting. Gen. Comp.Endocrinol., 154(1-3):31-40.
Qian B Y, Xue L Y. 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.
Reindl K M, Kittilson J D, Sheridan M A. 2009. Differential ligand binding and agonist-induced regulation characteristics of the two rainbow trout GH receptors, Ghr1 and Ghr2, in transfected cells. J. Endocrinol., 202(3):463-471.
Sahin K, Yazlak H, Orhan C, Tuzcu M, Akdemir F, Sahin N. 2014. The effect of lycopene on antioxidant status in rainbow trout (Oncorhynchus mykiss) reared under high stocking density. Aquaculture, 418-419:132-138.
Sánchez C C, Weber G M, Gao G T, Cleveland B M, Yao J B, Rexroad Ⅲ C E. 2011. Generation of a reference transcriptome for evaluating rainbow trout responses to various stressors. BMC Genomics, 12:626.
Smith S, Bernatchez L, Beheregaray L B. 2013. RNA-seq analysis reveals extensive transcriptional plasticity to temperature stress in a freshwater fish species. BMC Genomics, 14:375.
Sun P, Shi Z H, Yin F, Peng S M. 2012. Population genetic structure and demographic history of Pampus argenteus in the Indo-west Pacific inferred from mitochondrial cytochrome b sequences. Biochem. Syst. Ecol., 43:54-63.
Sun P, Yin F, Shi Z, Peng S. 2013. Genetic structure of silver pomfret (Pampus argenteus (Euphrasen, 1788)) in the Arabian Sea, Bay of Bengal, and South China Sea as indicated by mitochondrial COI gene sequences. J. Appl.Ichthyol., 29(4):733-737.
Sun P, Yin F, Tang B J. 2017. Effects of acute handling stress on expression of growth-related genes in Pampus argenteus. J. World Aquacult. SOC., 48(1):166-179.
Wang Y, Xu S S, Su Y H, Ye B P, Hua Z C. 2013. Molecular characterization and expression analysis of complement component C9 gene in the whitespotted bambooshark, Chiloscyllium plagiosum. Fish Shellfish Immunol., 35(2):599-606.
Wang Z, Gerstein M, Snyder M. 2009. RNA-Seq:a revolutionary tool for transcriptomics. Nat. Rev. Genet., 10(1):57-63.
Wu C X, Zhao F Y, Zhang Y, Zhu Y J, Ma M S, Mao H L, Hu C Y. 2012. Overexpression of Hsp90 from grass carp(Ctenopharyngodon idella) increases thermal protection against heat stress. Fish Shellfish Immunol., 33(1):42-47.
Wu X M, Hu Y W, Xue N N, Ren S S, Chen S N, Nie P, Chang M X. 2017. Role of zebrafish NLRC5 in antiviral response and transcriptional regulation of MHC related genes. Dev.Comp. Immunol., 68:58-68.
Xie Y J, Song L, Weng Z H, Liu S K, Liu Z J. 2015. Hsp90, Hsp60 and sHsp families of heat shock protein genes in channel catfish and their expression after bacterial infections. Fish Shellfish Immunol., 44(2):642-651.
Zhang C N, Tian H Y, Li X F, Zhu J, Cai D S, Xu C, Wang F, Zhang D D, Liu W B. 2014. The effects of fructooligosaccharide on the immune response, antioxidant capability and HSP70 and HSP90 expressions in blunt snout bream (Megalobrama amblycephala Yih)under high heat stress. Aquaculture, 433:458-466.
Zhao F, Dong Y H, Zhuang P, Zhang T, Zhang L Z, Shi Z H. 2011. Genetic diversity of silver pomfret (Pampus argenteus) in the Southern Yellow and East China Seas.Biochem. Syst. Ecol., 39(2):145-150.
Zizza M, Di Lorenzo M, Laforgia V, Furia E, Sindona G, Canonaco M, Facciolo R M. 2017. HSP90 and pCREB alterations are linked to mancozeb-dependent behavioral and neurodegenerative effects in a marine teleost. Toxicol.Appl. Pharmacol., 323:26-35.