BMC Genomics | |
Differences in brain gene transcription profiles advocate for an important role of cognitive function in upstream migration and water obstacles crossing in European eel | |
Francoise Daverat2  Fabien Pierron3  Eric De Oliveira5  Luca Bargelloni1  Gregory E Maes4  Jose Marti Pujolar6  Massimo Milan1  Tomasz Podgorniak2  | |
[1] University of Padova, Viale dell’Università 16, Legnaro 35020, PD, Italy;Irstea Bordeaux, UR EABX, HYNES (Irstea – EDF R&D), 50 avenue de Verdun, Cestas 33612, Cedex, France;CNRS, EPOC, UMR 5805, Talence F-33400, France;Laboratory of Biodiversity and Evolutionary Genomics, University of Leuven (KU Leuven), Leuven B-3000, Belgium;EDF R&D LNHE, HYNES (Irstea-EDF R&D), 6, quai Watier, Bat Q, Chatou 78400, France;Department of Bioscience, Aarhus University, Ny Munkegade 114, Aarhus C DK-8000, Denmark | |
关键词: Fish brain; Synaptic plasticity; Microarray; Water dams; European eel; Transcripomics; | |
Others : 1203967 DOI : 10.1186/s12864-015-1589-y |
|
received in 2014-12-05, accepted in 2015-04-27, 发布年份 2015 | |
【 摘 要 】
Background
European eel is a panmictic species, whose decline has been recorded since the last 20 years. Among human-induced environmental factors of decline, the impact of water dams during species migration is questioned. The main issue of this study was to pinpoint phenotypic traits that predisposed glass eels to successful passage by water barriers. The approach of the study was individual-centred and without any a priori hypothesis on traits involved in the putative obstacles selective pressure. We analyzed the transcription level of 14,913 genes.
Results
Transcriptome analysis of three tissues (brain, liver and muscle) from individuals sampled on three successive forebays separated by water obstacles indicated different gene transcription profiles in brain between the two upstream forebays. No differences in gene transcription levels were observed in liver and muscle samples among segments. A total of 26 genes were differentially transcribed in brain. These genes encode for, among others, keratins, cytokeratins, calcium binding proteins (S100 family), cofilin, calmodulin, claudin and thy-1 membrane glycoprotein. The functional analysis of these genes highlighted a putative role of cytoskeletal dynamics and synaptic plasticity in fish upstream migration.
Conclusion
Synaptic connections in brain are solicited while eels are climbing the obstacles with poorly designed fishways. Successful passage by such barriers can be related to spatial learning and spatial orientation abilities when fish is out of the water.
【 授权许可】
2015 Podgorniak et al.; licensee BioMed Central.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150523033349685.pdf | 576KB | download | |
Figure 1. | 29KB | Image | download |
【 图 表 】
Figure 1.
【 参考文献 】
- [1]Fischer J, Lindenmayer DB. Landscape modification and habitat fragmentation: A synthesis. Glob Ecol Biogeogr. 2007; 16:265-80.
- [2]Soule ME. Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, Mass; 1986.
- [3]Beneteau CL, Mandrak NE, Heath DD. The effects of river barriers and range expansion of the population genetic structure and stability in Greenside Darter (Etheostoma blennioides) populations. Conserv Genet. 2009; 10:477-87.
- [4]Bunn SE, Arthington AH. Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity. Environ Manage. 2002; 30:492-507.
- [5]Hauer FR, Stanford JA, Ward JV. Serial discontinuities in a Rocky Mountain river. II distribution and abundance of trichoptera. Regul Rivers: Res Manag. 1989; 3:177-82.
- [6]Araújo FG, Pinto BCT, Teixeira TP. Longitudinal patterns of fish assemblages in a large tropical river in southeastern Brazil: Evaluating environmental influences and some concepts in river ecology. Hydrobiologia. 2009; 618:89-107.
- [7]Mueller M, Pander J, Geist J. The effects of weirs on structural stream habitat and biological communities. J Appl Ecol. 2011; 48:1450-61.
- [8]Wofford JEB, Gresswell RE, Banks MA. Influence of barriers to movement on within-watershed genetic variation of coastal cutthroat trout. Ecol Appl. 2005; 15:628-37.
- [9]Freeman MC, Pringle CM, Jackson CR. Hydrologic connectivity and the contribution of stream headwaters to ecological integrity at regional scales. J Am Water Resour Assoc. 2007; 43:5-14.
- [10]Liermann CR, Nilsson C, Robertson J, Ng RY. Implications of dam obstruction for global freshwater fish diversity. BioScience. 2012; 62:539-48.
- [11]Funk WC, Greene AE, Corn PS, Allendorf FW. High dispersal in a frog species suggests that it is vulnerable to habitat fragmentation. Biol Lett. 2005; 1:13-6.
- [12]Postel S. Rivers for life : managing water for people and nature/Sandra Postel and Brian Richter. Island Press, Washington; 2003.
- [13]Kleckner RC, McCleave JD. The northern limit of spawning by Atlantic eels (Anguilla spp.) in the Sargasso Sea in relation to thermal fronts and surface water masses. J Mar Res. 1988; 46:647-67.
- [14]Kettle AJ, Asbjørn Vøllestad L, Wibig J. Where once the eel and the elephant were together: Decline of the European eel because of changing hydrology in southwest Europe and northwest Africa? Fish Fish. 2011; 12:380-411.
- [15]Tesch F-W, Thorpe JE. The eel. Oxford: UK: Blackwell Science: The Fisheries society of the British isles; 2003.
- [16]Cooke SJ, Hinch SG. Improving the reliability of fishway attraction and passage efficiency estimates to inform fishway engineering, science, and practice. Ecol Eng. 2013; 58:123-32.
- [17]Kemp PS, O’Hanley JR. Procedures for evaluating and prioritising the removal of fish passage barriers: A synthesis. Fish Manag Ecol. 2010; 17:297-322.
- [18]Edeline E, Dufour S, Elie P. Proximate and Ultimate Control of Eel Continental Dispersal. In: Spawning Migration of the European Eel. Volume 30. Thillart G, Dufour S, Rankin JC, editors. Springer, Netherlands; 2009: p.433-61. Fish & Fisheries Series
- [19]Fontaine M, Callamand O. Sur certains facteurs des migrations de l’anguille. Bulletin de la Société Zoologique de France. 1941; 66:68-76.
- [20]Piper AT, Wright RM, Kemp PS. The influence of attraction flow on upstream passage of European eel (Anguilla anguilla) at intertidal barriers. Ecol Eng. 2012; 44:329-36.
- [21]Kemp PS, Anderson JJ, Vowles AS. Quantifying behaviour of migratory fish: Application of signal detection theory to fisheries engineering. Ecol Eng. 2012; 41:22-31.
- [22]Edeline E, Bardonnet A, Bolliet V, Dufour S, Elie P. Endocrine control of Anguilla anguilla glass eel dispersal: Effect of thyroid hormones on locomotor activity and rheotactic behavior. Horm Behav. 2005; 48:53-63.
- [23]Bolliet V, Lambert P, Bardonnet A. Energy and migratory behaviour in glass eels (Anguilla anguilla). Physiol Behav. 2007; 92:684-90.
- [24]Fontaine M. Physiological Mechanisms in the Migration of Marine and Amphihaline Fish. Advances in Marine Biology. 1976; 13:241-355.
- [25]Woodhead AD. Endocrine physiology of fish migration. G. Allen and Ungin; 1975.
- [26]Castonguay M, Dutil J-D, Audet C, Miller R. Locomotor Activity and Concentration of Thyroid Hormones in Migratory and Sedentary Juvenile American Eels. Trans Am Fish Soc. 1990; 119:946-56.
- [27]Coppe A, Pujolar JM, Maes GE, Larsen PF, Hansen MM, Bernatchez L et al.. Sequencing, de novo annotation and analysis of the first Anguilla anguilla transcriptome: EeelBase opens new perspectives for the study of the critically endangered european eel. BMC Genomics. 2010; 11:635.
- [28]Sébert P, Mortelette H, Nicolas J, Amérand A, Belhomme M, Moisan C. In vitro aerobic and anaerobic muscle capacities in the European eel, Anguilla anguilla: Effects of a swimming session. Respir Physiol Neurobiol. 2011; 176:118-22.
- [29]Larsson Å, Lewander K. Metabolic effects of starvation in the eel, Anguilla anguilla L. Comp Biochem Physiol A Physiol. 1973; 44:367-74.
- [30]Cren L. The Length-Weight Relationship and Seasonal Cycle in Gonad Weight and Condition in the Perch (Perca fluviatilis). J Anim Ecol. 1951; 20:201.
- [31]Pujolar JM, Marino IAM, Milan M, Coppe A, Maes GE, Capoccioni F et al.. Surviving in a toxic world: transcriptomics and gene expression profiling in response to environmental pollution in the critically endangered European eel. BMC Genomics. 2012; 13:507.
- [32]Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001; 98:5116-21.
- [33]Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 2007; 35:W71-4.
- [34]Imbert H, Arrowsmith R, Dufour S, Elie P. Relationships between locomotor behavior, morphometric characters and thyroid hormone levels give evidence of stage-dependent mechanisms in European eel upstream migration. Horm Behav. 2008; 53:69-81.
- [35]Cui Y, Wootton RJ. Effects of ration, temperature and body size on the body composition, energy content and condition of the minnow, Phoxinus phoxinus (L.). J Fish Biol. 1988; 32:749-64.
- [36]Edeline E, Lambert P, Rigaud C, Elie P. Effects of body condition and water temperature on Anguilla anguilla glass eel migratory behavior. J Exp Mar Biol Ecol. 2006; 331:217-25.
- [37]Lambert P, Bardonnet A. Is feeding behaviour related to glass eel propensity to migrate? Estuar Coast Shelf Sci. 2008; 80:323-9.
- [38]Zimmer DB, Eubanks JO, Ramakrishnan D, Criscitiello MF. Evolution of the S100 family of calcium sensor proteins. Cell Calcium. 2013; 53:170-9.
- [39]Shang X, Cheng H, Zhou R. Chromosomal mapping, differential origin and evolution of the S100 gene family. Genet Sel Evol. 2008; 40:449-64.
- [40]Andressen C, Blumcke I, Celio MR. Calcium-binding proteins: Selective markers of nerve cells. Cell Tissue Res. 1993; 271:181-208.
- [41]Donato R. Perspectives in S-100 protein biology. Cell Calcium. 1991; 12:713-26.
- [42]Donato R. S100: A multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol. 2001; 33:637-68.
- [43]Di Donato V, Auer TO, Duroure K, Del Bene F. Characterization of the Calcium Binding Protein Family in Zebrafish. PLoS One. 2013; 8:1.
- [44]Hermann A, Donato R, Weiger TM, Chazin WJ. S100 calcium binding proteins and ion channels. Front Pharmacol. 2012; 3:67.
- [45]Berridge MJ. Neuronal calcium signaling. Neuron. 1998; 21:13-26.
- [46]Heizmann CW. Calcium signaling in the brain. Acta Neurobiol Exp. 1993; 53:15-23.
- [47]Jastrzebska B, Filipek A, Nowicka D, Kaczmarek L, Kuznicki J. Calcyclin (S100A6) binding protein (CacyBP) is highly expressed in brain neurons. J Histochem Cytochem. 2000; 48:1195-202.
- [48]Nowotny M, Bhattacharya S, Filipek A, Krezel AM, Chazin W, Kuznicki J. Characterization of the interaction of calcyclin (S100A6) and calcyclin-binding protein. J Biol Chem. 2000; 275:31178-82.
- [49]Schneider G, Filipek A. S100A6 binding protein and Siah-1 interacting protein (CacyBP/SIP): Spotlight on properties and cellular function. Amino Acids. 2011; 41:773-80.
- [50]Leśniak W, Słomnicki ŁP, Filipek A. S100A6 - New facts and features. Biochem Biophys Res Commun. 2009; 390:1087-92.
- [51]Li H, Guan HW. Research progress on calcium-binding protein S100A6. J Dalian Med Univ. 2012; 34:194-9.
- [52]Gruden MA, Storozheva ZI, Sewell RDE, Kolobov VV, Sherstnev VV. Distinct functional brain regional integration of Casp3, Ascl1 and S100a6 gene expression in spatial memory. Behav Brain Res. 2013; 252:230-8.
- [53]He H, Li J, Weng S, Li M, Yu Y. S100A11: Diverse Function and Pathology Corresponding to Different Target Proteins. Etats-Unis: Cell biochemistry and biophysics, Totowa, NJ; 2009.
- [54]Sakaguchi M, Sonegawa H, Murata H, Kitazoe M, Futami J, Kataoka K et al.. S100A11, an dual mediator for growth regulation of human keratinocytes. Mol Biol Cell. 2008; 19:78-85.
- [55]Deloulme JC, Assard N, Mbele GO, Mangin C, Kuwano R, Baudier J. S100A6 and S100A11 are specific targets of the calcium- and zinc-binding S100B protein in vivo. J Biol Chem. 2000; 275:35302-10.
- [56]Nishiyama H, Knopfel T, Endo S, Itohara S. Glial protein S100B modulates long-term neuronal synaptic plasticity. Proc Natl Acad Sci U S A. 2002; 99(6):4037-42.
- [57]Benfenati F, Ferrari R, Onofri F, Arcuri C, Giambanco I, Donato R. S100A1 codistributes with synapsin I in discrete brain areas and inhibits the F-actin-bundling activity of synapsin I. J Neurochem. 2004; 89:1260-70.
- [58]Ackermann GE, Marenholz I, Wolfer DP, Chan WY, Schäfer B, Erne P et al.. S100A1-deficient male mice exhibit increased exploratory activity and reduced anxiety-related responses. Biochim Biophys Acta, Mol Cell Res. 2006; 1763:1307-19.
- [59]Tóthová V, Gibadulinová A. S100P, a peculiar member of S100 family of calcium-binding proteins implicated in cancer. Acta Virol. 2013; 57:238-46.
- [60]Arumugam T, Simeone DM, Schmidt AM, Logsdon CD. S100P Stimulates Cell Proliferation and Survival via Receptor for Activated Glycation End Products (RAGE). J Biol Chem. 2004; 279:5059-65.
- [61]Mizuno K. Signaling mechanisms and functional roles of cofilin phosphorylation and dephosphorylation. Cell Signal. 2013; 25:457-69.
- [62]Garvalov BK, Flynn KC, Neukirchen D, Meyn L, Teusch N, Wu XW et al.. Cdc42 regulates cofilin during the establishment of neuronal polarity. J Neurosci. 2007; 27:13117-29.
- [63]Bradke F, Dotti CG. Differentiated neurons retain the capacity to generate axons from dendrites. Curr Biol. 2000; 10:1467-70.
- [64]Sarmiere PD, Bamburg JR. Regulation of the Neuronal Actin Cytoskeleton by ADF/Cofilin. J Neurobiol. 2004; 58:103-17.
- [65]Racz B, Weinberg RJ. Spatial organization of cofilin in dendritic spines. Neuroscience. 2006; 138:447-56.
- [66]Rust MB, Gurniak CB, Renner M, Vara H, Morando L, Görlich A et al.. Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. EMBO J. 2010; 29:1889-902.
- [67]Yuen EY, Liu W, Kafri T, van Praag H, Yan Z. Regulation of AMPA receptor channels and synaptic plasticity by cofilin phosphatase Slingshot in cortical neurons. J Physiol. 2010; 588:2361-71.
- [68]Gu J, Lee CW, Fan Y, Komlos D, Tang X, Sun C et al.. ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci. 2010; 13:1208-15.
- [69]Eckelhoefer HA, Rajapaksa TE, Wang J, Hamer M, Appleby NC, Ling J, Lo DD. Claudin-4: Functional studies beyond the tight junction. Methods in Molecular Biology. 2011; 762:115-128.
- [70]Chua KL, Lim TM. Type I and type II cytokeratin cDNAs from the zebrafish (Danio rerio) and expression patterns during early development. Differentiation. 2000; 66:31-41.
- [71]Iwatsuki H, Suda M. Transient expression of keratin during neuronal development in the adult rabbit spinal ganglion. Anat Sci Int. 2010; 85:46-55.
- [72]Gnegy ME. Ca2+/calmodulin signaling in NMDA-induced synaptic plasticity. Crit Rev Neurobiol. 2000; 14:91-129.
- [73]Delorenzo RJ. Calmodulin in neurotransmitter release and synaptic function. Fed Proc. 1982; 41:2265-72.
- [74]Greenberg ME, Thompson MA, Sheng M. Calcium regulation of immediate early gene transcription. J Physiol Paris. 1992; 86:99-108.
- [75]Zheng F, Luo Y, Wang H. Regulation of brain-derived neurotrophic factor-mediated transcription of the immediate early gene Arc by intracellular calcium and calmodulin. J Neurosci Res. 2009; 87:380-92.
- [76]Davis S, Bozon B, Laroche S. How necessary is the activation of the immediate early gene zif 268 in synaptic plasticity and learning? Behav Brain Res. 2003; 142:17-30.
- [77]Ghosh A, Ginty DD, Bading H, Greenberg ME. Calcium regulation of gene expression in neuronal cells. J Neurobiol. 1994; 25:294-303.
- [78]Igaz LM, Bekinschtein P, Vianna MMR, Izquierdo I, Medina JH. Gene expression during memory formation. Neurotox Res. 2004; 6:189-203.
- [79]Miyashita T, Kubik S, Lewandowski G, Guzowski JF. Networks of neurons, networks of genes: An integrated view of memory consolidation. Neurobiol Learn Mem. 2008; 89:269-84.
- [80]Lanahan A, Worley P. Immediate-Early Genes and Synaptic Function. Neurobiol Learn Mem. 1998; 70:37-43.
- [81]Xue GP, Rivero BP, Morris RJ. The surface glycoprotein Thy-1 is excluded from growing axons during development - a study of the expression of Thy-1 during axogenesis in hippocampus and hindbrain. Development. 1991; 112:161-76.
- [82]Xue GP, Calvert RA, Morris RJ. Expression of the neuronal syrface glycoprotein Thy-1 is under posttranscirptional control, and is spatially regulated in the developping olfactory system. Development. 1990; 109:851-4.
- [83]Moullé VS, Cansell C, Luquet S, Cruciani-Guglielmacci C. The multiple roles of Fatty Acid Handling Proteins in brain. Front Physiol. 2012; 3:385.
- [84]Edeline E, Dufour S, Briand C, Fatin D, Elie P. Thyroid status is related to migratory behavior in Anguilla anguilla glass eels. Mar Ecol Prog Ser. 2004; 282:261-70.
- [85]Tomoda H, Uematsu K. Morphogenesis of the Brain in Larval and Juvenile Japanese Eels, Anguilla japonica. Brain Behav Evol. 1996; 47:33-41.
- [86]Gonda A, Herczeg G, Merilä J. Population variation in brain size of nine-spined sticklebacks (Pungitius pungitius) - Local adaptation or environmentally induced variation? BMC Evol Biol. 2011; 11:75.
- [87]Kihslinger RL, Lema SC, Nevitt GA. Environmental rearing conditions produce forebrain differences in wild Chinook salmon Oncorhynchus tshawytscha. Comp Biochem Physiol A Mol Integr Physiol. 2006; 145:145-51.
- [88]von Krogh K, Sørensen C, Nilsson GE, Øverli Ø. Forebrain cell proliferation, behavior, and physiology of zebrafish, Danio rerio, kept in enriched or barren environments. Physiol Behav. 2010; 101:32-9.
- [89]Gonda A, Välimäki K, Herczeg G, Merila J. Brain development and predation: Plastic responses depend on evolutionary history. Biol Lett. 2012; 8:249-52.
- [90]Salvanes AGV, Moberg O, Ebbesson LOE, Nilsen TO, Jensen KH, Braithwaite VA. Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc R Soc B Biol Sci. 2013; 280:13.
- [91]Sorensen C, Johansen IB, Overli O. Neural plasticity and stress coping in teleost fishes. Gen Comp Endocrinol. 2013; 181:25-34.
- [92]Fay JC, Wittkopp PJ. Evaluating the role of natural selection in the evolution of gene regulation. Heredity. 2008; 100:191-9.
- [93]Giger T, Excoffier L, Day PJR, Champigneulle A, Hansen MM, Powell R et al.. Life history shapes gene expression in salmonids. Curr Biol. 2006; 16:R281-2.
- [94]Aubin-Horth N, Renn SCP. Genomic reaction norms: Using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol Ecol. 2009; 18:3763-80.
- [95]Derome N, Duchesne P, Bernatchez L. Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol Ecol. 2006; 15:1239-49.
- [96]Larsen PF, Nielsen EE, Williams TD, Hemmer-Hansen J, Chipman JK, Kruhøffer M et al.. Adaptive differences in gene expression in European flounder (Platichthys flesus). Mol Ecol. 2007; 16:4674-83.
- [97]Pacariz S, Westerberg H, Björk G. Climate change and passive transport of European eel larvae. Ecol Freshw Fish. 2014; 23:86-94.
- [98]Dannewitz J, Maes GE, Johansson L, Wickström H, Volckaert FAM, Järvi T. Panmixia in the European eel: A matter of time. Proc R Soc B Biol Sci. 2005; 272:1129-37.
- [99]Lenormand T. Gene flow and the limits to natural selection. Trends Ecol Evol. 2002; 17:183-9.
- [100]Sultan SE, Spencer HG. Metapopulation structure favors plasticity over local adaptation. Am Nat. 2002; 160:271-83.
- [101]Edeline E. Adaptive phenotypic plasticity of eel diadromy. Mar Ecol Prog Ser. 2007; 341:229-32.
- [102]Côté CL, Castonguay M, Kalujnaia MS, Cramb G, Bernatchez L. In absence of local adaptation, plasticity and spatially varying selection rule: A view from genomic reaction norms in a panmictic species (Anguilla rostrata). BMC Genomics. 2014; 15:403.
- [103]Ebbesson LOE, Braithwaite VA. Environmental effects on fish neural plasticity and cognition. J Fish Biol. 2012; 81:2151-74.
- [104]Oliveira RF. Social plasticity in fish: integrating mechanisms and function. J Fish Biol. 2012; 81:2127-50.