Spatially differentiated expression of quadruplicated green-sensitive RH2 opsin genes in zebrafish is determined by proximal regulatory regions and gene order to the locus control region

BMC Genetics

Shoji Kawamura²  Ryuichi Ashino²  Ryoko Masuda²  Taro Tsujimura¹ 

[1] Department of Advanced Nephrology and Regenerative Medicine, Division of Tissue Engineering, the University of Tokyo Hospital, Hongo 7-3-1, Bunkyo-ku 113-8655, Tokyo, Japan;Department of Integrated Biosciences, Graduate School of Frontier Sciences, the University of Tokyo, Kashiwanoha 5-1-5, Kashiwa 277-8562, Chiba, Japan

关键词: Gene order;    RH2-LCR;    Gene regulation;    Expression;    Subfunctionalization;    Gene duplication;    RH2;    opsin;    Zebrafish;   

Others  :  1230299
DOI  :  10.1186/s12863-015-0288-7

 received in 2015-08-19, accepted in 2015-10-27,  发布年份 2015

【 摘 要 】

Background

Fish are remarkably diverse in repertoires of visual opsins by gene duplications. Differentiation of their spatiotemporal expression patterns and absorption spectra enables fine-tuning of feature detection in spectrally distinct regions of the visual field during ontogeny. Zebrafish have quadruplicated green-sensitive (RH2) opsin genes in tandem (RH2-1, −2, −3, −4), which are expressed in the short member of the double cones (SDC). The shortest wavelength RH2 subtype (RH2-1) is expressed in the central to dorsal area of the adult retina. The second shortest wave subtype (RH2-2) is expressed overlapping with RH2-1 but extending outside of it. The second longest wave subtype (RH2-3) is expressed surrounding the RH2–2 area, and the longest wave subtype (RH2-4) is expressed outside of the RH2-3 area broadly occupying the ventral area. Expression of the four RH2 genes in SDC requires a single enhancer (RH2-LCR), but the mechanism of their spatial differentiation remains elusive.

Results

Functional comparison of the RH2-LCR with its counterpart in medaka revealed that the regulatory role of the RH2-LCR in SDC-specific expression is evolutionarily conserved. By combining the RH2-LCR and the proximal upstream region of each RH2 gene with fluorescent protein reporters, we show that the RH2-LCR and the RH2-3 proximal regulatory region confer no spatial selectivity of expression in the retina. But those of RH2-1, −2 and −4 are capable of inducing spatial differentiation of expression. Furthermore, by analyzing transgenic fish with a series of arrays consisting of the RH2-LCR and multiple upstream regions of the RH2 genes in different orders, we show that a gene expression pattern related to an upstream region is greatly influenced by another flanking upstream region in a relative position-dependent manner.

Conclusions

The zebrafish RH2 genes except RH2-3 acquired differential cis-elements in the proximal upstream regions to specify the differential expression patterns. The input from these proximal elements collectively dictates the actual gene expression pattern of the locus, context-dependently. Importantly, competition for the RH2-LCR activity among the replicates is critical in this collective regulation, facilitating differentiation of expression among them. This combination of specificity and generality enables seemingly complicated spatial differentiation of duplicated opsin genes characteristic in fish.

【 授权许可】

   
2015 Tsujimura et al.

【 图 表 】

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Fig. 5.

【 参考文献 】

• [1]Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res. 2000; 19(4):385-419.
• [2]Kawamura S. Evolutionary diversification of visual opsin genes in fish and primates. In: From genes to animal behavior: Social structures, personalities, communication by color. Inoue-Murayama M, Kawamura S, Weiss A, editors. Springer, Tokyo; 2011: p.329-349.
• [3]Chinen A, Hamaoka T, Yamada Y, Kawamura S. Gene duplication and spectral diversification of cone visual pigments of zebrafish. Genetics. 2003; 163(2):663-675.
• [4]Morrow JM, Lazic S, Chang BS. A novel rhodopsin-like gene expressed in zebrafish retina. Vis Neurosci. 2011; 28(4):325-335.
• [5]Matsumoto Y, Fukamachi S, Mitani H, Kawamura S. Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene. 2006; 371(2):268-278.
• [6]Carleton KL, Kocher TD. Cone opsin genes of African cichlid fishes: Tuning spectral sensitivity by differential gene expression. Mol Biol Evol. 2001; 18(8):1540-1550.
• [7]Spady TC, Parry JW, Robinson PR, Hunt DM, Bowmaker JK, Carleton KL. Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene arrays. Mol Biol Evol. 2006; 23(8):1538-1547.
• [8]Zhang J. Evolution by gene duplication: an update. Trends Ecol Evol. 2003; 18(6):292-298.
• [9]Carleton KL, Spady TC, Streelman JT, Kidd MR, McFarland WN, Loew ER. Visual sensitivities tuned by heterochronic shifts in opsin gene expression. BMC Biol. 2008; 6:22. BioMed Central Full Text
• [10]Hofmann CM, Carleton KL. Gene duplication and differential gene expression play an important role in the diversification of visual pigments in fish. Integr Comp Biol. 2009; 49(6):630-643.
• [11]Owens GL, Rennison DJ, Allison WT, Taylor JS. In the four-eyed fish (Anableps anableps), the regions of the retina exposed to aquatic and aerial light do not express the same set of opsin genes. Biol Lett. 2012; 8(1):86-89.
• [12]Rennison DJ, Owens GL, Allison WT, Taylor JS. Intra-retinal variation of opsin gene expression in the guppy (Poecilia reticulata). J Exp Biol. 2011; 214(Pt 19):3248-3254.
• [13]Takechi M, Kawamura S. Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. J Exp Biol. 2005; 208(Pt 7):1337-1345.
• [14]Davies WI, Collin SP, Hunt DM. Molecular ecology and adaptation of visual photopigments in craniates. Mol Ecol. 2012; 21(13):3121-3158.
• [15]Raymond PA, Barthel LK, Rounsifer ME, Sullivan SA, Knight JK. Expression of rod and cone visual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressed in cones. Neuron. 1993; 10(6):1161-1174.
• [16]Vihtelic TS, Doro CJ, Hyde DR. Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins. Vis Neurosci. 1999; 16(3):571-585.
• [17]Stenkamp DL. Neurogenesis in the fish retina. Int Rev Cytol. 2007; 259:173-224.
• [18]Tsujimura T, Chinen A, Kawamura S. Identification of a locus control region for quadruplicated green-sensitive opsin genes in zebrafish. Proc Natl Acad Sci U S A. 2007; 104(31):12813-12818.
• [19]Tsujimura T, Hosoya T, Kawamura S. A single enhancer regulating the differential expression of duplicated red-sensitive opsin genes in zebrafish. PLoS Genet. 2010; 6(12):e1001245.
• [20]Hisatomi O, Satoh T, Tokunaga F. The primary structure and distribution of killifish visual pigments. Vision Res. 1997; 37(22):3089-3096.
• [21]Gong Z, Ju B, Wang X, He J, Wan H, Sudha PM. Green fluorescent protein expression in germ-line transmitted transgenic zebrafish under a stratified epithelial promoter from keratin8. Dev Dyn. 2002; 223(2):204-215.
• [22]Parinov S, Kondrichin I, Korzh V, Emelyanov A. Tol2 transposon-mediated enhancer trap to identify developmentally regulated zebrafish genes in vivo. Dev Dyn. 2004; 231(2):449-459.
• [23]Fang W, Bonaffini S, Zou J, Wang X, Zhang C, Tsujimura T et al.. Characterization of transgenic zebrafish lines that express GFP in the retina, pineal gland, olfactory bulb, hatching gland, and optic tectum. Gene Expr Patterns. 2013; 13(5–6):150-159.
• [24]Montavon T, Soshnikova N, Mascrez B, Joye E, Thevenet L, Splinter E et al.. A regulatory archipelago controls Hox genes transcription in digits. Cell. 2011; 147(5):1132-1145.
• [25]Marinic M, Aktas T, Ruf S, Spitz F. An integrated holo-enhancer unit defines tissue and gene specificity of the Fgf8 regulatory landscape. Dev Cell. 2013; 24(5):530-542.
• [26]Ogawa Y, Shiraki T, Kojima D, Fukada Y. Homeobox transcription factor Six7 governs expression of green opsin genes in zebrafish. Proc Biol Sci. 2015; 282(1812):20150659.
• [27]Rennison DJ, Owens GL, Taylor JS. Opsin gene duplication and divergence in ray-finned fish. Mol Phylogenet Evol. 2012; 62(3):986-1008.
• [28]Mitchell DM, Stevens CB, Frey RA, Hunter SS, Ashino R, Kawamura S et al.. Retinoic Acid signaling regulates differential expression of the tandemly-duplicated long wavelength-sensitive cone opsin genes in zebrafish. PLoS Genet. 2015; 11(8):e1005483.
• [29]Smallwood PM, Wang Y, Nathans J. Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes. Proc Natl Acad Sci U S A. 2002; 99(2):1008-1011.
• [30]Hanscombe O, Whyatt D, Fraser P, Yannoutsos N, Greaves D, Dillon N et al.. Importance of globin gene order for correct developmental expression. Genes Dev. 1991; 5(8):1387-1394.
• [31]Tanimoto K, Liu Q, Bungert J, Engel JD. Effects of altered gene order or orientation of the locus control region on human beta-globin gene expression in mice. Nature. 1999; 398(6725):344-348.
• [32]Fuss SH, Omura M, Mombaerts P. Local and cis effects of the H element on expression of odorant receptor genes in mouse. Cell. 2007; 130:373-384.
• [33]Nishizumi H, Kumasaka K, Inoue N, Nakashima A, Sakano H. Deletion of the core-H region in mice abolishes the expression of three proximal odorant receptor genes in cis. Proc Natl Acad Sci U S A. 2007; 104:20067-20072.
• [34]Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, Yoshihara Y et al.. Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science. 2003; 302(5653):2088-2094.
• [35]Kaneko R, Abe M, Hirabayashi T, Uchimura A, Sakimura K, Yanagawa Y et al.. Expansion of stochastic expression repertoire by tandem duplication in mouse Protocadherin-alpha cluster. Sci Rep. 2014; 4:6263.
• [36]Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I. VISTA: Computational tools for comparative genomics. Nucleic Acids Res. 2004; 32(Web Server issue):W273-279.
• [37]Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA et al.. VISTA: Visualizing global DNA sequence alignments of arbitrary length. Bioinformatics. 2000; 16(11):1046-1047.
• [38]Bray N, Dubchak I, Pachter L. AVID: A global alignment program. Genome Res. 2003; 13(1):97-102.
• [39]Rauch G-J, Granato, M., and Haffter, P.: A polymorphic zebrafish line for genetic mapping using SSLPs on high-percentage agarose gels. Tech Tips Online 1997, T01208.
• [40]Haffter P, Odenthal J, Mullins MC, Lin S, Farrell MJ, Vogelsang E et al.. Mutations affecting pigmentation and shape of the adult zebrafish. Dev Genes Evol. 1996; 6(4):260-276.
• [41]Westerfield M. The zebrafish book: A guide for the laboratory use of zebrafish (Danio Rerio). University of Oregon Press, Eugene; 1995.
• [42]Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, Court DL et al.. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics. 2001; 73(1):56-65.
• [43]Thermes V, Grabher C, Ristoratore F, Bourrat F, Choulika A, Wittbrodt J et al.. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev. 2002; 118(1–2):91-98.
• [44]Urasaki A, Morvan G, Kawakami K. Functional dissection of the Tol2 transposable element identified the minimal cis-sequence and a highly repetitive sequence in the subterminal region essential for transposition. Genetics. 2006; 174(2):639-649.
• [45]Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell. 2004; 7(1):133-144.
• [46]Hamaoka T, Takechi M, Chinen A, Nishiwaki Y, Kawamura S. Visualization of rod photoreceptor development using GFP-transgenic zebrafish. Genesis. 2002; 34(3):215-220.
• [47]Luo W, Williams J, Smallwood PM, Touchman JW, Roman LM, Nathans J. Proximal and distal sequences control UV cone pigment gene expression in transgenic zebrafish. J Biol Chem. 2004; 279(18):19286-19293.