Genome-wide identification of nuclear receptor (NR) superfamily genes in the copepod Tigriopus japonicus

BMC Genomics

Jae-Seong Lee²  Jae-Sung Rhee¹  Ae-Son Om⁴  Do-Hyun Kyung³  Min Chul Lee⁴  Hui-Su Kim²  Bo-Young Lee²  Dae-Sik Hwang² 

[1] Department of Marine Science, College of Natural Science, Incheon National University, Incheon 406-772, South Korea;Department of Biological Science, College of Science, Sungkyunkwan University, Suwon 440-746, South Korea;Department of Chemistry, College of Natural Sciences, Hanyang University, Seoul 133-791 South Korea;Department of Food and Nutrition, College of Human Ecology, Hanyang University, Seoul 133-791, South Korea

关键词: Ecdysone signaling;    Copepod;    Nuclear receptor;   

Others  :  1092233
DOI  :  10.1186/1471-2164-15-993

 received in 2014-06-20, accepted in 2014-11-04,  发布年份 2014

【 摘 要 】

Background

Nuclear receptors (NRs) are a large superfamily of proteins defined by a DNA-binding domain (DBD) and a ligand-binding domain (LBD). They function as transcriptional regulators to control expression of genes involved in development, homeostasis, and metabolism. The number of NRs differs from species to species, because of gene duplications and/or lineage-specific gene losses during metazoan evolution. Many NRs in arthropods interact with the ecdysteroid hormone and are involved in ecdysone-mediated signaling in arthropods. The nuclear receptor superfamily complement has been reported in several arthropods, including crustaceans, but not in copepods. We identified the entire NR repertoire of the copepod Tigriopus japonicus, which is an important marine model species for ecotoxicology and environmental genomics.

Results

Using whole genome and transcriptome sequences, we identified a total of 31 nuclear receptors in the genome of T. japonicus. Nomenclature of the nuclear receptors was determined based on the sequence similarities of the DNA-binding domain (DBD) and ligand-binding domain (LBD). The 7 subfamilies of NRs separate into five major clades (subfamilies NR1, NR2, NR3, NR4, and NR5/6). Although the repertoire of NR members in, T. japonicus was similar to that reported for other arthropods, there was an expansion of the NR1 subfamily in Tigriopus japonicus. The twelve unique nuclear receptors identified in T. japonicus are members of NR1L. This expansion may be a unique lineage-specific feature of crustaceans. Interestingly, E78 and HR83, which are present in other arthropods, were absent from the genomes of T. japonicus and two congeneric copepod species (T. japonicus and Tigriopus californicus), suggesting copepod lineage-specific gene loss.

Conclusions

We identified all NR receptors present in the copepod, T. japonicus. Knowledge of the copepod nuclear receptor repertoire will contribute to a better understanding of copepod- and crustacean-specific NR evolution.

【 授权许可】

   
2014 Hwang et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Laudet V, Gronemeyer H: The Nuclear Receptors Factsbook. London: Academic Press; 2002.
• [2]Laudet V: Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. J Mol Endocrinol 1997, 19(3):207-226.
• [3]Escriva H, Delaunay F, Laudet V: Ligand binding and nuclear receptor evolution. BioEssays 2000, 22(8):717-727.
• [4]Bonneton F, Chaumot A, Laudet V: Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Insect Biochem Mol Biol 2008, 38(4):416-429.
• [5]Giguere V: Orphan nuclear receptors: from gene to function. Endocr Rev 1999, 20(5):689-725.
• [6]Bassett MH, Suzuki T, Sasano H, De Vries CJ, Jimenez PT, Carr BR, Rainey WE: The orphan nuclear receptor NGFIB regulates transcription of 3beta-hydroxysteroid dehydrogenase. implications for the control of adrenal functional zonation. J Biol Chem 2004, 279(36):37622-37630.
• [7]Bassett MH, Suzuki T, Sasano H, White PC, Rainey WE: The orphan nuclear receptors NURR1 and NGFIB regulate adrenal aldosterone production. Mol Endocrinol 2004, 18(2):279-290.
• [8]Sluder AE, Maina CV: Nuclear receptors in nematodes: themes and variations. Trends Genet 2001, 17(4):206-213.
• [9]Ayer S, Walker N, Mosammaparast M, Nelson JP, Shilo BZ, Benyajati C: Activation and repression of Drosophila alcohol dehydrogenase distal transcription by two steroid hormone receptor superfamily members binding to a common response element. Nucleic Acids Res 1993, 21(7):1619-1627.
• [10]Horner MA, Chen T, Thummel CS: Ecdysteroid regulation and DNA binding properties of Drosophila nuclear hormone receptor superfamily members. Dev Biol 1995, 168(2):490-502.
• [11]Lavorgna G, Karim FD, Thummel CS, Wu C: Potential role for a FTZ-F1 steroid receptor superfamily member in the control of Drosophila metamorphosis. Proc Natl Acad Sci U S A 1993, 90(7):3004-3008.
• [12]Bertrand S, Brunet FG, Escriva H, Parmentier G, Laudet V, Robinson-Rechavi M: Evolutionary genomics of nuclear receptors: from twenty-five ancestral genes to derived endocrine systems. Mol Biol Evol 2004, 21(10):1923-1937.
• [13]Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, et al.: The genome sequence of Drosophila melanogaster. Science 2000, 287(5461):2185-2195.
• [14]Gissendanner CR, Crossgrove K, Kraus KA, Maina CV, Sluder AE: Expression and function of conserved nuclear receptor genes in Caenorhabditis elegans. Dev Biol 2004, 266(2):399-416.
• [15]Robinson-Rechavi M, Carpentier AS, Duffraisse M, Laudet V: How many nuclear hormone receptors are there in the human genome? Trends Genet 2001, 17(10):554-556.
• [16]Tan A, Palli SR: Identification and characterization of nuclear receptors from the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 2008, 38(4):430-439.
• [17]Thomson SA, Baldwin WS, Wang YH, Kwon G, Leblanc GA: Annotation, phylogenetics, and expression of the nuclear receptors in Daphnia pulex. BMC Genomics 2009, 10:500. BioMed Central Full Text
• [18]Raisuddin S, Kwok KW, Leung KM, Schlenk D, Lee JS: The copepod Tigriopus: a promising marine model organism for ecotoxicology and environmental genomics. Aquat Toxicol 2007, 83(3):161-173.
• [19]Thummel CS: Dueling orphans–interacting nuclear receptors coordinate Drosophila metamorphosis. BioEssays 1997, 19(8):669-672.
• [20]Truman JW, Riddiford LM: The origins of insect metamorphosis. Nature 1999, 401(6752):447-452.
• [21]Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD, McKeown M, Cherbas P, Evans RM: Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 1993, 366(6454):476-479.
• [22]Segraves WA, Hogness DS: The E75 ecdysone-inducible gene responsible for the 75B early puff in Drosophila encodes two new members of the steroid receptor superfamily. Genes Dev 1990, 4(2):204-219.
• [23]Stone BL, Thummel CS: The Drosophila 78C early late puff contains E78, an ecdysone-inducible gene that encodes a novel member of the nuclear hormone receptor superfamily. Cell 1993, 75(2):307-320.
• [24]Woodard CT, Baehrecke EH, Thummel CS: A molecular mechanism for the stage specificity of the Drosophila prepupal genetic response to ecdysone. Cell 1994, 79(4):607-615.
• [25]Sutherland JD, Kozlova T, Tzertzinis G, Kafatos FC: Drosophila hormone receptor 38: a second partner for Drosophila USP suggests an unexpected role for nuclear receptors of the nerve growth factor-induced protein B type. Proc Natl Acad Sci U S A 1995, 92(17):7966-7970.
• [26]Zelhof AC, Yao TP, Evans RM, McKeown M: Identification and characterization of a Drosophila nuclear receptor with the ability to inhibit the ecdysone response. Proc Natl Acad Sci U S A 1995, 92(23):10477-10481.
• [27]Tennessen JM, Baker KD, Lam G, Evans J, Thummel CS: The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth. Cell Metab 2011, 13(2):139-148.
• [28]Huys R, Boxshall GA: Copepod Evolution. London: Ray Soc; 1991.
• [29]Wells PG: Ecotoxicological Testing for the Marine Environment. Volume 1. Edited by Persoone G, Jaspers E, Claus C. Bredene: Inst. Mar. Sci. Res; 1984::215-256.
• [30]Lee JS, Rhee JS, Kim RO, Hwang DS, Han J, Choi BS, Park GS, Kim IC, Park HG, Lee YM: The copepod Tigriopus japonicus genomic DNA information (574Mb) and molecular anatomy. Mar Environ Res 2010, 69(Suppl):S21-S23.
• [31]Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH: CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 2011, 39(suppl 1):D225-D229.
• [32]Bertrand S, Belgacem MR, Escriva H: Nuclear hormone receptors in chordates. Mol Cell Endocrinol 2011, 334(1–2):67-75.
• [33]King-Jones K, Thummel CS: Nuclear receptors–a perspective from Drosophila. Nat Rev Genet 2005, 6(4):311-323.
• [34]Bonneton F, Laudet V: Chapter 6. Evolution of Nuclear Receptors in Insects. In Insect Endocrinology. Edited by Gilbert LI. San Diego, CA, USA: Academic Press; 2011:219-252.
• [35]Li Y, Ginjupalli GK, Baldwin WS: The HR97 (NR1L) group of nuclear receptors: a new group of nuclear receptors discovered in Daphnia species. Gen Comp Endocrinol 2014, 206C:30-42.
• [36]Owen GI, Zelent A: Origins and evolutionary diversification of the nuclear receptor superfamily. Cell Mol Life Sci 2000, 57(5):809-827.
• [37]Eick GN, Thornton JW: Evolution of steroid receptors from an estrogen-sensitive ancestral receptor. Mol Cell Endocrinol 2011, 334(1–2):31-38.
• [38]Thummel CS: From embryogenesis to metamorphosis: the regulation and function of Drosophila nuclear receptor superfamily members. Cell 1995, 83(6):871-877.
• [39]Giguere V, Yang N, Segui P, Evans RM: Identification of a new class of steroid hormone receptors. Nature 1988, 331(6151):91-94.
• [40]Baker ME: Steroid receptor phylogeny and vertebrate origins. Mol Cell Endocrinol 1997, 135(2):101-107.
• [41]Lecroisey C, Laudet V, Schubert M: The cephalochordate amphioxus: a key to reveal the secrets of nuclear receptor evolution. Brief Funct Genomics 2012, 11(2):156-166.
• [42]Robinson-Rechavi M, Maina C, Gissendanner C, Laudet V, Sluder A: Explosive lineage-specific expansion of the orphan nuclear receptor HNF4 in nematodes. J Mol Evol 2005, 60(5):577-586.
• [43]Vogeler S, Galloway TS, Lyons BP, Bean TP: The nuclear receptor gene family in the Pacific oyster, Crassostrea gigas, contains a novel subfamily group. BMC Genomics 2014, 15:369. BioMed Central Full Text
• [44]Weber K, Alvaro C, Baer G, Reinert K, Cheng G, Clever S, Wightman B: Analysis of C. elegans NR2E nuclear receptors defines three conserved clades and ligand-independent functions. BMC Evol Biol 2012, 12(1):81. BioMed Central Full Text
• [45]Jung S-O, Lee Y-M, Park T-J, Park HG, Hagiwara A, Leung KMY, Dahms H-U, Lee W, Lee J-S: The complete mitochondrial genome of the intertidal copepod Tigriopus sp. (Copepoda, Harpactidae) from Korea and phylogenetic considerations. J Exp Marine Biol Ecol 2006, 333(2):251-262.
• [46]Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A: Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011, 29(7):644-652.
• [47]Nuclear Receptors Nomenclature C: A unified nomenclature system for the nuclear receptor superfamily. Cell 1999, 97(2):161-163.
• [48]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
• [49]Schwarz G: Estimating the Dimension of a Model. 1978, 461-464.
• [50]Hurvich CM, Tsai C-L: Regression and time series model selection in small samples. Biometrika 1989, 76(2):297-307.
• [51]Posada D, Buckley TR: Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 2004, 53(5):793-808.
• [52]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
• [53]Schwarz R, Dayhoff M: Matrices for Detecting Distant Relationships. In Atlas of Protein Sequences. Edited by Dayhoff M. National Biomedical Research Foundation; 1979:353-358.