Genome Sequencing of the Perciform Fish Provides Insights into Molecular and Genetic Mechanisms of Stress Adaptation

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L. crocea is a temperate-water migratory fish that belongs to the order Perciformes and the family Sciaenidae. In China, the annual yield from L. crocea aquaculture exceeds that of any other net-cage-farmed marine fish species. L. crocea also exhibits peculiar behavioral and physiological characteristics and is especially sensitive to various environmental stresses. To understand the molecular and genetic mechanisms underlying the adaptation and response of L. crocea to environmental stress, we sequenced and assembled the genome of L. crocea. Further genomic analyses showed the significant expansion of several gene families, such as vision-related crystallins, olfactory receptors, and auditory sense-related genes, and provided a genetic basis for the peculiar physiological characteristics of L. crocea. Transcriptome analyses of the hypoxia-exposed L. crocea brain revealed new aspects of neuro-endocrine-immune/metabolism regulatory networks that may help the fish to avoid cerebral inflammatory injury and maintain energy balance under hypoxia. Proteomics data demonstrate that skin mucus of the air-exposed L. crocea had a complex composition, suggesting its multiple protective mechanisms involved in antioxidant functions, oxygen transport, immune defence, and osmotic and ionic regulation. These findings provide novel insights into the mechanisms of fish stress adaptation.

Vyšlo v časopise: Genome Sequencing of the Perciform Fish Provides Insights into Molecular and Genetic Mechanisms of Stress Adaptation. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005118
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005118

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Zdroje

1. Cossins AR, Crawford DL (2005) Fish as models for environmental genomics. Nat Rev Genet 6: 324–333. 15803200

2. van der Meer DL, van den Thillart GE, Witte F, de Bakker MA, Besser J, et al. (2005) Gene expression profiling of the long-term adaptive response to hypoxia in the gills of adult zebrafish. Am J Physiol Regul Integr Comp Physiol 289: R1512–1519. 15994372

3. Gracey AY, Troll JV, Somero GN (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci U S A 98: 1993–1998. 11172064

4. Chen S, Zhang G, Shao C, Huang Q, Liu G, et al. (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46: 253–260. doi: 10.1038/ng.2890 24487278

5. Star B, Nederbragt AJ, Jentoft S, Grimholt U, Malmstrom M, et al. (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477: 207–210. doi: 10.1038/nature10342 21832995

6. Schartl M, Walter RB, Shen Y, Garcia T, Catchen J, et al. (2013) The genome of the platyfish, Xiphophorus maculatus, provides insights into evolutionary adaptation and several complex traits. Nat Genet 45: 567–572. doi: 10.1038/ng.2604 23542700

7. Feng Z, Cao Q (1979) Ichthyology. Beijing: Agricultural Press House. 217 p.

8. ) Breeding and Farming of Pseudosciaena Crocea. Beijing: China Ocean Press. 329 p.

9. Liu YY, Cao MJ, Zhang ML, Hu JW, Zhang YX, et al. (2014) Purification, characterization and immunoreactivity of beta'-component, a major allergen from the roe of large yellow croaker (Pseudosciaena crocea). Food Chem Toxicol 72C: 111–121.

10. Liu XD, Zhao GT, Cai MY, Wang ZY (2013) Estimated genetic parameters for growth-related traits in large yellow croaker Larimichthys crocea using microsatellites to assign parentage. J Fish Biol 82: 34–41. doi: 10.1111/j.1095-8649.2012.03472.x 23331136

11. Ye H, Liu Y, Liu X, Wang X, Wang Z (2014) Genetic Mapping and QTL Analysis of Growth Traits in the Large Yellow Croaker Larimichthys crocea. Mar Biotechnol (NY) 16: 729–738. doi: 10.1007/s10126-014-9590-z 25070688

12. Ning Y, Liu X, Wang ZY, Guo W, Li Y, et al. (2007) A genetic map of large yellow croaker Pseudosciaena crocea. Aquaculture 264: 16–26.

13. Mu Y, Ding F, Cui P, Ao J, Hu S, et al. (2010) Transcriptome and expression profiling analysis revealed changes of multiple signaling pathways involved in immunity in the large yellow croaker during Aeromonas hydrophila infection. BMC Genomics 11: 506. doi: 10.1186/1471-2164-11-506 20858287

14. Zhou Y, Yan X, Xu S, Zhu P, He X, et al. (2011) Family structure and phylogenetic analysis of odorant receptor genes in the large yellow croaker (Larimichthys crocea). BMC Evol Biol 11: 237. doi: 10.1186/1471-2148-11-237 21834959

15. Gu X, Xu Z (2011) Effect of hypoxia on the blood of large yellow croaker (Pseudosciaena crocea). Chinese Journal of Oceanology and Limnology 29: 524.

16. Mu Y, Li M, Ding F, Ding Y, Ao J, et al. (2014) De Novo Characterization of the Spleen Transcriptome of the Large Yellow Croaker (Pseudosciaena crocea) and Analysis of the Immune Relevant Genes and Pathways Involved in the Antiviral Response. PLoS One 9: e97471. doi: 10.1371/journal.pone.0097471 24820969

17. Yu S, Mu Y, Ao J, Chen X (2010) Peroxiredoxin IV regulates pro-inflammatory responses in large yellow croaker (Pseudosciaena crocea) and protects against bacterial challenge. J Proteome Res 9: 1424–1436. doi: 10.1021/pr900961x 20099887

18. Luo R, Liu B, Xie Y, Li Z, Huang W, et al. (2012) SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Gigascience 1: 18. doi: 10.1186/2047-217X-1-18 23587118

19. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555–556. 9367129

20. Niimura Y (2009) On the origin and evolution of vertebrate olfactory receptor genes: comparative genome analysis among 23 chordate species. Genome Biol Evol 1: 34–44. doi: 10.1093/gbe/evp003 20333175

21. Li W, Sorensen PW, Gallaher DD (1995) The olfactory system of migratory adult sea lamprey (Petromyzon marinus) is specifically and acutely sensitive to unique bile acids released by conspecific larvae. J Gen Physiol 105: 569–587. 7658193

22. Eisen MD, Ryugo DK (2007) Hearing molecules: contributions from genetic deafness. Cell Mol Life Sci 64: 566–580. 17260086

23. Jiang L, Liu Q, Ni J (2010) In silico identification of the sea squirt selenoproteome. BMC Genomics 11: 289. doi: 10.1186/1471-2164-11-289 20459719

24. Vandermarliere E, Ghesquiere B, Jonckheere V, Gevaert K, Martens L (2014) Unraveling the specificities of the different human methionine sulfoxide reductases. Proteomics 14: 1990–1998. doi: 10.1002/pmic.201300357 24737740

25. Hansen JD, Vojtech LN, Laing KJ (2011) Sensing disease and danger: a survey of vertebrate PRRs and their origins. Dev Comp Immunol 35: 886–897. doi: 10.1016/j.dci.2011.01.008 21241729

26. Komuro A, Bamming D, Horvath CM (2008) Negative regulation of cytoplasmic RNA-mediated antiviral signaling. Cytokine 43: 350–358. doi: 10.1016/j.cyto.2008.07.011 18703349

27. Chang M, Collet B, Nie P, Lester K, Campbell S, et al. (2011) Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in Rainbow trout (Oncorhynchus mykiss). J Virol 85: 8403–8412. doi: 10.1128/JVI.00445-10 21680521

28. Castanier C, Zemirli N, Portier A, Garcin D, Bidere N, et al. (2012) MAVS ubiquitination by the E3 ligase TRIM25 and degradation by the proteasome is involved in type I interferon production after activation of the antiviral RIG-I-like receptors. BMC Biol 10: 44. doi: 10.1186/1741-7007-10-44 22626058

29. Gao D, Wu J, Wu YT, Du F, Aroh C, et al. (2013) Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341: 903–906. doi: 10.1126/science.1240933 23929945

30. Zhang Z, Yuan B, Bao M, Lu N, Kim T, et al. (2011) The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12: 959–965. doi: 10.1038/ni.2091 21892174

31. Zou J, Tafalla C, Truckle J, Secombes CJ (2007) Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol 179: 3859–3871. 17785823

32. Zhang L, Mo J, Swanson KV, Wen H, Petrucelli A, et al. (2014) NLRC3, a Member of the NLR Family of Proteins, Is a Negative Regulator of Innate Immune Signaling Induced by the DNA Sensor STING. Immunity 40:329–341. doi: 10.1016/j.immuni.2014.01.010 24560620

33. Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20: 78–84. 9023876

34. Yang N, Ray DW, Matthews LC (2012) Current concepts in glucocorticoid resistance. Steroids 77: 1041–1049. doi: 10.1016/j.steroids.2012.05.007 22728894

35. Lemos Vde A, dos Santos RV, Lira FS, Rodrigues B, Tufik S, et al. (2013) Can high altitude influence cytokines and sleep? Mediators Inflamm 2013: 279365. doi: 10.1155/2013/279365 23690660

36. Nadeau S, Rivest S (2003) Glucocorticoids play a fundamental role in protecting the brain during innate immune response. J Neurosci 23: 5536–5544. 12843254

37. Sorrells SF, Sapolsky RM (2007) An inflammatory review of glucocorticoid actions in the CNS. Brain Behav Immun 21: 259–272. 17194565

38. Hayashi R, Wada H, Ito K, Adcock IM (2004) Effects of glucocorticoids on gene transcription. Eur J Pharmacol 500: 51–62. 15464020

39. Takahashi K, Udono-Fujimori R, Totsune K, Murakami O, Shibahara S (2003) Suppression of cytokine-induced expression of adrenomedullin and endothelin-1 by dexamethasone in T98G human glioblastoma cells. Peptides 24: 1053–1062. 14499284

40. Mastorakos G, Chrousos GP, Weber JS (1993) Recombinant interleukin-6 activates the hypothalamic-pituitary-adrenal axis in humans. J Clin Endocrinol Metab 77: 1690–1694. 8263159

41. Kitamuro T, Takahashi K, Nakayama M, Murakami O, Hida W, et al. (2000) Induction of adrenomedullin during hypoxia in cultured human glioblastoma cells. J Neurochem 75: 1826–1833. 11032871

42. Earley S, Nelin LD, Chicoine LG, Walker BR (2002) Hypoxia-induced pulmonary endothelin-1 expression is unaltered by nitric oxide. J Appl Physiol (1985) 92: 1152–1158.

43. Hou TD, Du JZ (2005) Norepinephrine attenuates hypoxia-inhibited thyrotropin-releasing hormone release in median eminence and paraventricular nucleus of rat hypothalamus. Neuro Endocrinol Lett 26: 43–49. 15726019

44. Kenessey A, Ojamaa K (2006) Thyroid hormone stimulates protein synthesis in the cardiomyocyte by activating the Akt-mTOR and p70S6K pathways. J Biol Chem 281: 20666–20672. 16717100

45. Yen PM (2001) Physiological and molecular basis of thyroid hormone action. Physiol Rev 81: 1097–1142. 11427693

46. Sabell I, Morata P, Quesada J, Morell M (1985) Effect of thyroid hormones on the glycolytic enzyme activity in brain areas of the rat. Enzyme 34: 27–32. 2935391

47. Benita Y, Kikuchi H, Smith AD, Zhang MQ, Chung DC, et al. (2009) An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1)-target genes that form the core response to hypoxia. Nucleic Acids Res 37: 4587–4602. doi: 10.1093/nar/gkp425 19491311

48. Dayan F, Roux D, Brahimi-Horn MC, Pouyssegur J, Mazure NM (2006) The oxygen sensor factor-inhibiting hypoxia-inducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxia-inducible factor-1alpha. Cancer Res 66: 3688–3698. 16585195

49. Shephard KL (1994) Functions for fish mucus. Reviews in Fish Biology and Fisheries 4: 401–429.

50. Subramanian S, Ross NW, MacKinnon SL (2008) Comparison of antimicrobial activity in the epidermal mucus extracts of fish. Comp Biochem Physiol B Biochem Mol Biol 150: 85–92. doi: 10.1016/j.cbpb.2008.01.011 18342561

51. Pluta K, McGettigan PA, Reid CJ, Browne JA, Irwin JA, et al. (2012) Molecular aspects of mucin biosynthesis and mucus formation in the bovine cervix during the periestrous period. Physiol Genomics 44: 1165–1178. doi: 10.1152/physiolgenomics.00088.2012 23092952

52. Guzman-Aranguez A, Mantelli F, Argueso P (2009) Mucin-type O-glycans in tears of normal subjects and patients with non-Sjogren's dry eye. Invest Ophthalmol Vis Sci 50: 4581–4587. doi: 10.1167/iovs.09-3563 19407012

53. Cross CE, Halliwell B, Allen A (1984) Antioxidant protection: a function of tracheobronchial and gastrointestinal mucus. Lancet 1: 1328–1330. 6145029

54. Bona E, Andersson AL, Blomgren K, Gilland E, Puka-Sundvall M, et al. (1999) Chemokine and inflammatory cell response to hypoxia-ischemia in immature rats. Pediatr Res 45: 500–509. 10203141

55. Taylor MM, Bagley SL, Samson WK (2005) Intermedin/adrenomedullin-2 acts within central nervous system to elevate blood pressure and inhibit food and water intake. Am J Physiol Regul Integr Comp Physiol 288: R919–927. 15576658

56. Kaur C, Ling EA (2008) Blood brain barrier in hypoxic-ischemic conditions. Curr Neurovasc Res 5: 71–81. 18289024

57. Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214: 191–199. doi: 10.1242/jeb.047951 21177940

58. Lee DC, Hassan SS, Romero R, Tarca AL, Bhatti G, et al. (2011) Protein profiling underscores immunological functions of uterine cervical mucus plug in human pregnancy. J Proteomics 74: 817–828. doi: 10.1016/j.jprot.2011.02.025 21362502

59. Rodriguez-Pineiro AM, Bergstrom JH, Ermund A, Gustafsson JK, Schutte A, et al. (2013) Studies of mucus in mouse stomach, small intestine, and colon. II. Gastrointestinal mucus proteome reveals Muc2 and Muc5ac accompanied by a set of core proteins. Am J Physiol Gastrointest Liver Physiol 305: G348–356. doi: 10.1152/ajpgi.00047.2013 23832517

60. Li R, Yu C, Li Y, Lam TW, Yiu SM, et al. (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966–1967. doi: 10.1093/bioinformatics/btp336 19497933

61. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W (2011) Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 27: 578–579. doi: 10.1093/bioinformatics/btq683 21149342

62. Smit A, Hubley, R & Green, P. RepeatMasker Open-3.0 (1996–2010). http://www.repeatmasker.org.

63. Price AL, Jones NC, Pevzner PA (2005) De novo identification of repeat families in large genomes. Bioinformatics 21 Suppl 1: i351–358. 15961478

64. Birney E, Clamp M, Durbin R (2004) GeneWise and Genomewise. Genome Res 14: 988–995. 15123596

65. Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 33: W465–467. 15980513

66. Korf I (2004) Gene finding in novel genomes. BMC Bioinformatics 5: 59. 15144565

67. Burge C, Karlin S (1997) Prediction of complete gene structures in human genomic DNA. J Mol Biol 268: 78–94. 9149143

68. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111. doi: 10.1093/bioinformatics/btp120 19289445

69. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628. doi: 10.1038/nmeth.1226 18516045

70. Ruan J, Li H, Chen Z, Coghlan A, Coin LJ, et al. (2008) TreeFam: 2008 Update. Nucleic Acids Res 36: D735–740. 18056084

71. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797. 15034147

72. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552. 10742046

73. De Bie T, Cristianini N, Demuth JP, Hahn MW (2006) CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22: 1269–1271. 16543274

74. Zhang H, Gao S, Lercher MJ, Hu S, Chen WH (2012) EvolView, an online tool for visualizing, annotating and managing phylogenetic trees. Nucleic Acids Res 40: W569–572. doi: 10.1093/nar/gks576 22695796

75. Loytynoja A, Goldman N (2010) webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11: 579. doi: 10.1186/1471-2105-11-579 21110866

76. Zhang G, Fang X, Guo X, Li L, Luo R, et al. (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490: 49–54. doi: 10.1038/nature11413 22992520

77. Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7: 986–995. 9331369

78. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Annals of statistics: 1165–1188.

79. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. 11846609