Transcriptome analysis of food habit transition from carnivory to herbivory in a typical vertebrate herbivore, grass carp Ctenopharyngodon idella

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• 作者：Shan He (1)
  Xu-Fang Liang (1)
  Ling Li (1)
  Jian Sun (1)
  Zheng-Yong Wen (1)
  Xiao-Yan Cheng (1)
  Ai-Xuan Li (1)
  Wen-Jing Cai (1)
  Yu-Hui He (1)
  Ya-Ping Wang (2)
  Ya-Xiong Tao (3)
  Xiao-Chen Yuan (1)
  
  1. Key Laboratory of Freshwater Animal Breeding ; Ministry of Agriculture ; College of Fisheries ; Huazhong Agricultural University ; Hubei Collaborative Innovation Center for Freshwater Aquaculture ; 430070 ; Wuhan ; China
  2. State Key Laboratory of Freshwater Ecology and Biotechnology ; Institute of Hydrobiology ; Chinese Academy of Sciences ; 430072 ; Wuhan ; China
  3. Department of Anatomy ; Physiology ; and Pharmacology ; College of Veterinary Medicine ; Auburn University ; Auburn ; AL ; 36849-5519 ; USA
  
• 关键词：Food habit transition ; Carnivory ; Herbivory ; Grass carp ; Transcriptome sequencing
• 刊名：BMC Genomics
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：16
• 期：1
• 全文大小：3,243 KB
• 参考文献：1. Van Soest PJ. Nutritional Ecology of the Ruminant. 2nd ed. Ithaca, NY: Cornell University Press; 1994.
  2. Bryant MP. Introduction to gastrointestinal microbial ecology. In: Mackie RI, White BA, editors. Gastrointestinal Microbiology. Vol. 1: Gastrointestinal Ecosystems and Fermentations. New York: Chapman and Hall; 1997. p. 3鈥?2. CrossRef
  3. Mackie RI. Gut environment and evolution of mutualistic fermentative digestion. In: Mackie RI, White BA, editors. Gastrointestinal Microbiology. Vol. 1: Gastrointestinal Ecosystems and Fermentations. New York: Chapman and Hall; 1997. p. 156鈥?8.
  4. Sullam KE, Essinger SD, Lozupone CA, O鈥檆onnor MP, Rosen GL, Knight R. Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis. Mol Ecol. 2012;21:3363鈥?8. CrossRef
  5. Choat JH, Clements KD. Vertebrate herbivores in marine and terrestrial environments: a nutritional ecology perspective. Annu Rev Ecol System. 1998;29:375鈥?03. CrossRef
  6. Hickling CF. On the feeding process in the White Amur, / Ctenopharyngodon idella. J Zool. 1966;148:408鈥?9. CrossRef
  7. Van Dyke JM, Sutton DL. Digestion of duckweed ( / Lemna spp.) by the grass carp ( / Ctenopharyngodon idella). J Fish Biol. 1977;11:273鈥?. CrossRef
  8. Lindsay GJH, Harris JE. Carboxymethylcellulase activity and the digestive tracts of fish. J Fish Biol. 1980;16:219鈥?3. CrossRef
  9. Lesel R, Fromageot C, Lesel M. Cellulose digestibility in grass carp, / Ctenopharyngodon idella and in goldfish, / Carassius auratus. Aquaculture. 1986;54:11鈥?. CrossRef
  10. Watkins CE, Shireman JV, Rottmann RW, Colle DE. Food habits of fingerling grass carp. Prog Fish-Culturist. 1981;43:95鈥?. CrossRef
  11. Wu S, Wang G, Angert ER, Wang W, Li W, Zou H. Composition, diversity, and origin of the bacterial community in grass carp intestine. PLoS ONE. 2012;7:e30440. CrossRef
  12. Martin MM. Cellulose digestion in insects. Comp Biochem Physiol. 1983;75:313鈥?4. CrossRef
  13. Zinkler D, Gotze M. Cellulose digestion by the firebrat / Thermobia domestica. Comp Biochem Physiol B. 1987;88:661鈥?.
  14. Goodenough S, Goodenough P. Who needs cellulase? J Biol Educ. 1993;27:97鈥?02. CrossRef
  15. Zhou Y, Yuan X, Liang XF, Fang L, Li J, Guo X, et al. Enhancement of growth and intestinal flora in grass carp: the effect of exogenous cellulase. Aquaculture. 2013;416鈥?17:1鈥?. CrossRef
  16. Ni DS, Wang JG. Biology and Diseases of Grass Carp. Beijing, China: Science Press; 1999.
  17. Li SF, Yang HQ, Lu WM. Preliminary research on diurnal feeding rhythm and the daily ration for silver carp, bighead carp and grass carp. J Fish China. 1980;4:275鈥?3 (In Chinese).
  18. Cui YB, Chen SL, Wang SM, Liu XF. Laboratory observations on the circadian feeding patterns in the grass carp (Ctenopharyngodon idella Val.) fed three different diets. Aquaculture. 1993;113:57鈥?4. CrossRef
  19. He S, Liang XF, Li L, Sun J, Shen D. Differential gut growth, gene expression and digestive enzyme activities in young grass carp ( / Ctenopharyngodon idella) fed with plant and animal diets. Aquaculture. 2013;410:18鈥?4. CrossRef
  20. Modrek B, Lee C. A genomic view of alternative splicing. Nat Genet. 2002;30:13鈥?. CrossRef
  21. McGuire AM, Pearson MD, Neafsey DE, Galagan JE. Cross-kingdom patterns of alternative splicing and splice recognition. Genome Biol. 2008;9:R50. CrossRef
  22. Johnson LR. Physiology of the Gastrointestinal Tract. New York: Raven; 1994.
  23. Hofer R, Schiemer F. Proteolytic activity in the digestive tract of several species of fish with different feeding habits. Oecologia. 1981;48:342鈥?. CrossRef
  24. Sotiropoulos A, Perrot-Applanat M, Dinerstein H, Pallier A, Postel-Vinay MC, Finidori J, et al. Distinct cytoplasmic regions of the growth hormone receptor are required for activation of JAK2, mitogen-activated protein kinase, and transcription. Endocrinology. 1994;135:1292鈥?.
  25. Argetsinger LS, Hsu GW, Myers MG, Billestrup N, White MF, Carter-Su C. Growth hormone, interferon-纬, and leukemia inhibitory factor promoted tyrosyl phosphorylation of insulin receptor substrate-1. J Biol Chem. 1995;270:14685鈥?2. CrossRef
  26. Ridderstrale M, Degerman E, Tornqvist H. Growth hormone stimulates the tyrosine phosphorylation of the insulin receptor substrate-1 and its association with phosphatidylinositol 3-kinase in primary adipocytes. J Biol Chem. 1995;270:3471鈥?. CrossRef
  27. Argetsinger LS, Carter-Su C. Mechanism of signaling by growth hormone receptor. Physiol Rev. 1996;76:1089鈥?07.
  28. Playford RJ, Marchbank T, Mandir N, Higham A, Meeran K, Ghatei MA, et al. Effects of keratinocyte growth factor (KGF) on gut growth and repair. J Pathol. 1998;184:316鈥?2. CrossRef
  29. Tassi E, Al-Attar A, Aigner A, Swift MR, McDonnell K, Karavanov A, et al. Enhancement of fibroblast growth factor (FGF) activity by an FGF-binding protein. J Biol Chem. 2001;276:40247鈥?3. CrossRef
  30. Brubaker PL, Drucker DJ. Minireview: glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system. Endocrinology. 2004;145:2653鈥?. CrossRef
  31. Washizawa N, Gu LH, Gu L, Openo KP, Jones DP, Ziegler TR. Comparative effects of glucagon-like peptide-2 (GLP-2), growth hormone (GH), and keratinocyte growth factor (KGF) on markers of gut adaptation after massive small bowel resection in rats. JPEN-Parenter Enter. 2004;28:399鈥?09. CrossRef
  32. Shulman DI, Hu CS, Duckett G, Lavallee-Grey M. Effects of short-term growth hormone therapy in rats undergoing 75% small intestinal resection. J Pediatr Gastroenterol Nutr. 1992;14:3鈥?1. CrossRef
  33. Delehaye-Zervas MC, Mertani H, Martini JF, Nihoul-Fekete C, Morel G, Postel-Vinay MC. Expression of the growth hormone receptor gene in human digestive tissues. J Clin Endocrinol Meta. 1994;78:1473鈥?0.
  34. Ulshen MH, Dowling RH, Fuller CR, Zimmermann EM, Lund PK. Enhanced growth of small bowel in transgenic mice overexpressing bovine growth hormone. Gastroenterology. 1993;104:973鈥?0.
  35. Pillai SB, Hinman CE, Luquette MH, Nowicki PT, Besner GE. Heparin-binding epidermal growth factor-like growth factor protects rat intestine from ischemia/reperfusion injury. J Surg Res. 1999;87:225鈥?1. CrossRef
  36. Cove FL, Evans GS. The use of an intestinal epithelial cellline as a biological assay system for growth factor activity. Biochem Soc Trans. 1992;20:175S.
  37. Hernell O, Olivecrona T. Human milk lipases. II. Bile salt-stimulated lipase. Biochim Biophys Acta. 1974;369:234鈥?4. CrossRef
  38. Hamosh M, Hamosh P. Development of digestive enzyme secretion. Development of the gastrointestinal tract. Sanderson IR, Walker WA, Decker Hamilton, Ontario, Chap. 16. 1999. p. 261-277.
  39. Whitcomb DC, Lowe ME. Human pancreatic digestive enzymes. Digest Dis Sci. 2007;52:1鈥?7. CrossRef
  40. Verrey F, Singer D, Ramadan T, Vuille-dit-Bille RN, Mariotta L, Camargo SMR. Kidney amino acid transport. Pflugers Arch-Eur J Physiol. 2009;458:53鈥?0. CrossRef
  41. Arrese M, Trauner M. Molecular aspects of bile formation and cholestasis. Trends Mol Med. 2003;9:558鈥?4. CrossRef
  42. Hersey SJ, Sachs G. Gastric acid secretion. Physiol Rev. 1995;75:155鈥?9.
  43. Reddy JK, Hashimoto T. Peroxisomal-oxidation and peroxisome proliferator-activated receptor: an adaptive metabolic system. Annu Rev Nutr. 2001;21:193鈥?30. CrossRef
  44. Tao YX, Yuan ZH, Xie J. G protein-coupled receptors as regulators of energy homeostasis. Prog Mol Biol Transl Sci. 2013;114:1鈥?3. CrossRef
  45. Morley JE. Appetite regulation by gut peptides. Annu Rev Nutr. 1990;10:383鈥?5. CrossRef
  46. Terry P, Gilbert DB, Cooper SJ. Dopamine receptor subtype agonists and feeding behavior. Obesity Res. 1995;3:515S鈥?3. CrossRef
  47. Stratford TR, Kelley AE. GABA in the nucleus accumbens shell participates in the central regulation of feeding behavior. J Neurosci. 1997;17:4434鈥?0.
  48. Lin X, Taguchi A, Park S, Kushner JA, Li F, Li Y, et al. Dysregulation of insulin receptor substrate 2 in beta cells and brain causes obesity and diabetes. J Clin Invest. 2004;114:908鈥?6. CrossRef
  49. Chaudhri O, Small C, Bloom S. Gastrointestinal hormones regulating appetite. Philos T Roy Soc B. 2006;361:1187鈥?09. CrossRef
  50. Wilding JP. Neuropeptides and appetite control. Diabetic Med. 2002;19:619鈥?7. CrossRef
  51. Alavi K, Schwartz MZ, Prasad R, O'connor D, Funanage V. Leptin: a new growth factor for the small intestine. J Pediatr Surg. 2002;37:327鈥?0. CrossRef
  52. Al-Hussaini AH. On the functional morphology of the alimentary tract of some fish in relation to differences in their feeding habits: cytology and physiology. Q J Microsco Sci. 1949;s3-90:323鈥?4.
  53. Kapoor BG, Smit H, Verighina IA. The alimentary canal and digestion in teleosts. Adv Mar Biol. 1976;13:109鈥?39. CrossRef
  54. He S, Liang XF, Sun J, Li L, Yu Y, Huang W, et al. Insights into food preference in hybrid F1 of / Siniperca chuatsi (鈾€)鈥壝椻€?em class="a-plus-plus">Siniperca scherzeri (鈾? mandarin fish through transcriptome analysis. BMC Genomics. 2013;14:601. CrossRef
  55. Wang Y, Newton DC, Marsden PA. Neuronal NOS: gene structure, mRNA diversity, and functional relevance. Crit Rev Neurobiol. 1999;13:21鈥?3.
  56. Shigeri Y, Seal RP, Shimamoto K. Molecular pharmacology of glutamate transporters, EAATs and VGLUTs. Brain Res Rev. 2004;45:250鈥?5. CrossRef
  57. Cahill GM. Clock mechanisms in zebrafish. Cell Tissue Res. 2002;309:27鈥?4. CrossRef
  58. Falvey E, Fleury-Olela F, Schibler U. The rat hepatic leukemia factor (HLF) gene encodes two transcriptional activators with distinct circadian rhythms, tissue distributions and target preferences. EMBO J. 1995;14:4307鈥?7.
  59. Zylka MJ, Shearman LP, Weaver DR, Reppert SM. Three period homologs in mammals: differential light responses in the suprachiasmatic circadian clock and oscillating transcripts outside of brain. Neuron. 1998;20:1103鈥?0. CrossRef
  60. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature. 2002;418:935鈥?1. CrossRef
  61. Green CB, Douris N, Kojima S, Strayer CA, Fogerty J, Lourim D, et al. Loss of Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proc Natl Acad Sci U S A. 2007;104:9888鈥?3. CrossRef
  62. Busino L, Bassermann F, Maiolica A, Lee C, Nolan PM, Godinho SI, et al. SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science. 2007;316:900鈥?. science.1141194" target="_blank" title="It opens in new window">CrossRef
  63. Shi J, Wittke-Thompson JK, Badner JA, Hattori E, Potash JB, Willour VL, et al. Clock genes may influence bipolar disorder susceptibility and dysfunctional circadian rhythm. Am J Med Genet B Neuropsychiatr Genet. 2008;147B:1047鈥?5. CrossRef
  64. Hidalgo MC, Urea E, Sanz A. Comparative study of digestive enzymes in fish with different nutritional habits: proteolytic and amylase activities. Aquaculture. 1999;170:267鈥?3. CrossRef
  65. Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics. 2009;25:1966鈥?. CrossRef
  66. Huang S, Zhang J, Li R, Zhang W, He Z, Lam TW, et al. SOAPsplice: genome-wide ab initio detection of splice junctions from RNA-Seq data. Front Genet. 2011;2:46. CrossRef
  67. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5:621鈥?. CrossRef
  
• 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
• 出版者：BioMed Central
• ISSN：1471-2164

文摘

Background Although feeding behavior and food habit are ecologically and economically important properties, little is known about formation and evolution of herbivory. Grass carp (Ctenopharyngodon idella) is an ecologically appealing model of vertebrate herbivore, widely cultivated in the world as edible fish or as biological control agents for aquatic weeds. Grass carp exhibits food habit transition from carnivory to herbivory during development. However, currently little is known about the genes regulating the unique food habit transition and the formation of herbivory, and how they could achieve higher growth rates on plant materials, which have a relatively poor nutritional quality. Results We showed that grass carp fed with duckweed (modeling fish after food habit transition) had significantly higher relative length of gut than fish before food habit transition or those fed with chironomid larvae (fish without transition). Using transcriptome sequencing, we identified 10,184 differentially expressed genes between grass carp before and after transition in brain, liver and gut. By eliminating genes potentially involved in development (via comparing fish with or without food habit transition), we identified changes in expression of genes involved in cell proliferation and differentiation, appetite control, circadian rhythm, and digestion and metabolism between fish before and after food habit transition. Up-regulation of GHRb, Egfr, Fgf, Fgfbp1, Insra, Irs2, Jak, STAT, PKC, PI3K expression in fish fed with duckweed, consistent with faster gut growth, could promote the food habit transition. Grass carp after food habit transition had increased appetite signal in brain. Altered expressions of Per, Cry, Clock, Bmal2, Pdp, Dec and Fbxl3 might reset circadian phase of fish after food habit transition. Expression of genes involved in digestion and metabolism were significantly different between fish before and after the transition. Conclusions We suggest that the food habit transition from carnivory to herbivory in grass carp might be due to enhanced gut growth, increased appetite, resetting of circadian phase and enhanced digestion and metabolism. We also found extensive alternative splicing and novel transcript accompanying food habit transition. These differences together might account for the food habit transition and the formation of herbivory in grass carp.