BMC Evolutionary Biology | |
Molecular adaptation and resilience of the insect’s nuclear receptor USP | |
François Bonneton4  Vincent Laudet4  Xavier Belles3  Frederic Brunet4  Thomas Iwema1  David Martin3  Oscar Maestro3  Jean-Luc Da Lage2  Arnaud Chaumot5  | |
[1] Groupe de recherche "immunopathologie et maladies infectieuses (GRI), Universite de la Réunion, Centre CYROI, Cyclotron Réunion Ocean Indien, Sainte Clotilde Ile de la Réunion, 97491, France;UPR9034, Laboratoire Evolution, génomes et spéciation (LEGS), CNRS, Gif sur Yvette, 91198, France;Institute of Evolutionary Biology (CSIC-UPF), Passeig Marítim de la Barceloneta 37, Barcelona, 08003, Spain;Institut de Génomique Fonctionnelle de Lyon (IGFL), Université de Lyon, Université Lyon 1; CNRS; INRA; Ecole Normale Supérieure de Lyon, 32-34 avenue Tony Garnier, Lyon, 69007, France;Irstea, UR MALY, Lyon, F-69336, France | |
关键词: Selection; Mecopterida; USP; ECR; Ecdysone receptor; Nuclear receptors; | |
Others : 1140170 DOI : 10.1186/1471-2148-12-199 |
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received in 2012-06-04, accepted in 2012-09-25, 发布年份 2012 | |
【 摘 要 】
Background
The maintenance of biological systems requires plasticity and robustness. The function of the ecdysone receptor, a heterodimer composed of the nuclear receptors ECR (NR1H1) and USP (NR2B4), was maintained in insects despite a dramatic divergence that occurred during the emergence of Mecopterida. This receptor is therefore a good model to study the evolution of plasticity. We tested the hypothesis that selection has shaped the Ligand-Binding Domain (LBD) of USP during evolution of Mecopterida.
Results
We isolated usp and cox1 in several species of Drosophilidae, Tenebrionidae and Blattaria and estimated non-synonymous/synonymous rate ratios using maximum-likelihood methods and codon-based substitution models. Although the usp sequences were mainly under negative selection, we detected relaxation at residues located on the surface of the LBD within Mecopterida families. Using branch-site models, we also detected changes in selective constraints along three successive branches of the Mecopterida evolution. Residues located at the bottom of the ligand-binding pocket (LBP) underwent strong positive selection during the emergence of Mecopterida. This change is correlated with the acquisition of a large LBP filled by phospholipids that probably allowed the stabilisation of the new Mecopterida structure. Later, when the two subgroups of Mecopterida (Amphiesmenoptera: Lepidoptera, Trichoptera; Antliophora: Diptera, Mecoptera, Siphonaptera) diverged, the same positions became under purifying selection. Similarly, several positions of the heterodimerisation interface experienced positive selection during the emergence of Mecopterida, rapidly followed by a phase of constrained evolution. An enlargement of the heterodimerisation surface is specific for Mecopterida and was associated with a reinforcement of the obligatory partnership between ECR and USP, at the expense of homodimerisation.
Conclusions
In order to explain the episodic mode of evolution of USP, we propose a model in which the molecular adaptation of this protein is seen as a process of resilience for the maintenance of the ecdysone receptor functionality.
【 授权许可】
2012 Chaumot et al.; licensee BioMed Central Ltd.
【 预 览 】
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Figure 1. | 159KB | Image | download |
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【 参考文献 】
- [1]Wagner A: Robustness, evolvability, and neutrality. FEBS Lett 2005, 579(8):1772-1778.
- [2]Henrich VC: The ecdysteroid receptor. In Comprehensive Molecular Insect Science. Edited by Gilbert LI, Iatrou K, Gill SS. Oxford: Elsevier; 2005:243-285. vol. 3
- [3]Spindler KD, Honl C, Tremmel C, Braun S, Ruff H, Spindler-Barth M: Ecdysteroid hormone action. Cell Mol Life Sci 2009, 66(24):3837-3850.
- [4]Bonneton F, Zelus D, Iwema T, Robinson-Rechavi M, Laudet V: Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between ECR and USP-RXR. Mol Biol Evol 2003, 20(4):541-553.
- [5]Bonneton F, Brunet FG, Kathirithamby J, Laudet V: The rapid divergence of the ecdysone receptor is a synapomorphy for Mecopterida that clarifies the Strepsiptera problem. Insect Mol Biol 2006, 15(3):351-362.
- [6]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.
- [7]Iwema T, Billas IM, Beck Y, Bonneton F, Nierengarten H, Chaumot A, Richards G, Laudet V, Moras D: Structural and functional characterization of a novel type of ligand-independent RXR-USP receptor. EMBO J 2007, 26(16):3770-3782.
- [8]Iwema T, Chaumot A, Studer RA, Robinson-Rechavi M, Billas IML, Moras D, Laudet V, Bonneton F: Structural and Evolutionary Innovation of the Heterodimerization Interface between USP and the Ecdysone Receptor ECR in Insects. Mol Biol Evol 2009, 26(4):753-768.
- [9]Philippe H, Casane D, Gribaldo S, Lopez P, Meunier J: Heterotachy and functional shift in protein evolution. IUBMB Life 2003, 55(4–5):257-265.
- [10]Anisimova M, Liberles DA: The quest for natural selection in the age of comparative genomics. Heredity 2007, 99(6):567-579.
- [11]Hughes AL: Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity 2007, 99(4):364-373.
- [12]Studer RA, Robinson-Rechavi M: Evidence for an episodic model of protein sequence evolution. Biochem Soc Trans 2009, 37(Pt 4):783-786.
- [13]Studer RA, Penel S, Duret L, Robinson-Rechavi M: Pervasive positive selection on duplicated and nonduplicated vertebrate protein coding genes. Genome Res 2008, 18(9):1393-1402.
- [14]Baer CF, Miyamoto MM, Denver DR: Mutation rate variation in multicellular eukaryotes: causes and consequences. Nat Rev Genet 2007, 8(8):619-631.
- [15]Galtier N, Duret L: Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Trends Genet 2007, 23(6):273-277.
- [16]Tamura K, Subramanian S, Kumar S: Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 2004, 21(1):36-44.
- [17]Angelini DR, Jockusch EL: Relationships among pest flour beetles of the genus Tribolium (Tenebrionidae) inferred from multiple molecular markers. Mol Phylogenet Evol 2008, 46(1):127-141.
- [18]Grandcolas P, D’haese C: The phylogeny of cockroach families: is the current molecular hypothesis robust? Cladistics-the Int J Willi Hennig Soc 2001, 17(1):48-55.
- [19]Mukha D, Wiegmann BM, Schal C: Evolution and phylogenetic information content of the ribosomal DNA repeat unit in the Blattodea (Insecta). Insect Biochem Mol Biol 2002, 32(9):951-960.
- [20]Gaunt MW, Miles MA: An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 2002, 19(5):748-761.
- [21]Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997, 13(5):555-556.
- [22]Yang Z, Bielawski JP: Statistical methods for detecting molecular adaptation. Trends Ecol Evol 2000, 15(12):496-503.
- [23]Zhang J, Hu X, Lazar MA: A novel role for helix 12 of retinoid X receptor in regulating repression. Mol Cell Biol 1999, 19(9):6448-6457.
- [24]Marimuthu A, Feng W, Tagami T, Nguyen H, Jameson JL, Fletterick RJ, Baxter JD, West BL: TR surfaces and conformations required to bind nuclear receptor corepressor. Mol Endocrinol 2002, 16(2):271-286.
- [25]Billas IML, Moulinier L, Rochel N, Moras D: Crystal structure of the ligand-binding domain of the ultraspiracle protein USP, the ortholog of retinoid X receptors in insects. J Biol Chem 2001, 276(10):7465-7474.
- [26]Clayton GM, Peak-Chew SY, Evans RM, Schwabe JW: The structure of the ultraspiracle ligand-binding domain reveals a nuclear receptor locked in an inactive conformation. Proc Natl Acad Sci U S A 2001, 98(4):1549-1554.
- [27]Hu X, Cherbas L, Cherbas P: Transcription activation by the ecdysone receptor (EcR/USP): identification of activation functions. Mol Endocrinol 2003, 17(4):716-731.
- [28]Carmichael JA, Lawrence MC, Graham LD, Pilling PA, Epa VC, Noyce L, Lovrecz G, Winkler DA, Pawlak-Skrzecz A, Eaton RE, et al.: The X-ray structure of a hemipteran ecdysone receptor ligand-binding domain - Comparison with a Lepidopteran ecdysone receptor ligand-binding domain and implications for insecticide design. J Biol Chem 2005, 280(23):22258-22269.
- [29]Billas IM, Iwema T, Garnier JM, Mitschler A, Rochel N, Moras D: Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Nature 2003, 426(6962):91-96.
- [30]Zhang J, Nielsen R, Yang Z: Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 2005, 22(12):2472-2479.
- [31]Kostka D, Hubisz MJ, Siepel A, Pollard KS: The role of GC-biased gene conversion in shaping the fastest evolving regions of the human genome. Mol Biol Evol 2012, 29(3):1047-1057.
- [32]Clare EL, Kerr KC, von Konigslow TE, Wilson JJ, Hebert PD: Diagnosing mitochondrial DNA diversity: applications of a sentinel gene approach. J Mol Evol 2008, 66(4):362-367.
- [33]Krasowski MD, Yasuda K, Hagey LR, Schuetz EG: Evolutionary selection across the nuclear hormone receptor superfamily with a focus on the NR1I subfamily (vitamin D, pregnane X, and constitutive androstane receptors). Nucl Recept 2005, 3:2. BioMed Central Full Text
- [34]Philip S, Castro LF, da Fonseca RR, Reis-Henriques MA, Vasconcelos V, Santos MM, Antunes A: Adaptive evolution of the Retinoid X receptor in vertebrates. Genomics 2012, 99:81-89.
- [35]Zhang Z, Burch PE, Cooney AJ, Lanz RB, Pereira FA, Wu J, Gibbs RA, Weinstock G, Wheeler DA: Genomic analysis of the nuclear receptor family: new insights into structure, regulation, and evolution from the rat genome. Genome Res 2004, 14(4):580-590.
- [36]Pal C, Papp B, Lercher MJ: An integrated view of protein evolution. Nat Rev Genet 2006, 7(5):337-348.
- [37]Perissi V, Rosenfeld MG: Controlling nuclear receptors: the circular logic of cofactor cycles. Nat Rev Mol Cell Biol 2005, 6(7):542-554.
- [38]Raviscioni M, He Q, Salicru EM, Smith CL, Lichtarge O: Evolutionary identification of a subtype specific functional site in the ligand binding domain of steroid receptors. Proteins 2006, 64(4):1046-1057.
- [39]Nowickyj SM, Chithalen JV, Cameron D, Tyshenko MG, Petkovich M, Wyatt GR, Jones G, Walker VK: Locust retinoid X receptors: 9-Cis-retinoic acid in embryos from a primitive insect. Proc Natl Acad Sci U S A 2008, 105(28):9540-9545.
- [40]Arakawa T, Ejima D, Kita Y, Tsumoto K: Small molecule pharmacological chaperones: From thermodynamic stabilization to pharmaceutical drugs. Biochim Biophys Acta 2006, 1764(11):1677-1687.
- [41]Nagl SB, Freeman J, Smith TF: Evolutionary constraint networks in ligand-binding domains: an information-theoretic approach. Pac Symp Biocomput 1999, 4:90-101.
- [42]Minakuchi C, Ogura T, Miyagawa H, Nakagawa Y: Effects of the structures of ecdysone receptor (EcR) and ultraspiracle (USP) on the ligand-binding activity of the EcR/USP heterodimer. J Pestic Sci 2007, 32(4):379-384.
- [43]Nakagawa Y, Sakai A, Magata F, Ogura T, Miyashita M, Miyagawa H: Molecular cloning of the ecdysone receptor and the retinoid X receptor from the scorpion Liocheles australasiae. Febs J 2007, 274(23):6191-6203.
- [44]Ogura T, Minakuchi C, Nakagawa Y, Smagghe G, Miyagawa H: Molecular cloning, expression analysis and functional confirmation of ecdysone receptor and ultraspiracle from the Colorado potato beetle Leptinotarsa decemlineata. Febs Journal 2005, 272(16):4114-4128.
- [45]Henrich VC: The ecdysteroid receptor. In Insect endocrinology. Edited by Gilbert LI. Amsterdam, Boston: Academic Press, Elsevier; 2012:177-218.
- [46]Li C, Schwabe JWR, Banayo E, Evans RM: Coexpression of nuclear receptor partners increases their solubility and biological activities. Proc Natl Acad Sci U S A 1997, 94(6):2278-2283.
- [47]Graham LD, Pilling PA, Eaton RE, Gorman JJ, Braybrook C, Hannan GN, Pawlak-Skrzecz A, Noyce L, Lovrecz GO, Lu L, et al.: Purification and characterization of recombinant ligand-binding domains from the ecdysone receptors of four pest insects. Protein Expr Purif 2007, 53(2):309-324.
- [48]Lezzi M, Bergman T, Henrich VC, Vogtli M, Fromel C, Grebe M, Przibilla S, Spindler-Barth M: Ligand-induced heterodimerization between the ligand binding domains of the Drosophila ecdysteroid receptor and ultraspiracle. Eur J Biochem 2002, 269(13):3237-3245.
- [49]Vivat-Hannah V, Bourguet W, Gottardis M, Gronemeyer H: Separation of retinoid X receptor homo- and heterodimerization functions. Mol Cell Biol 2003, 23(21):7678-7688.
- [50]Hult EF, Tobe SS, Chang BS: Molecular evolution of ultraspiracle protein (USP/RXR) in insects. PLoS One 2011, 6(8):e23416.
- [51]Dover GA, Strachan T, Coen ES, Brown SD: Molecular drive. Science 1982, 218(4577):1069.
- [52]Dover GA: Evolution of genetic redundancy for advanced players. Curr Opin Genet Dev 1993, 3(6):902-910.
- [53]Krasowski MD, Yasuda K, Hagey LR, Schuetz EG: Evolution of the pregnane x receptor: adaptation to cross-species differences in biliary bile salts. Mol Endocrinol 2005, 19(7):1720-1739.
- [54]Shyu C, Brown CJ, Ytreberg FM: Computational study of evolutionary selection pressure on rainbow trout estrogen receptors. PLoS One 2010, 5(3):e9392.
- [55]Krasowski MD, Ni A, Hagey LR, Ekins S: Evolution of promiscuous nuclear hormone receptors: LXR, FXR, VDR, PXR, and CAR. Mol Cell Endocrinol 2011, 334(1–2):39-48.
- [56]Domazet-Loso T, Tautz D: An evolutionary analysis of orphan genes in Drosophila. Genome Res 2003, 13(10):2213-2219.
- [57]Savard J, Tautz D, Lercher MJ: Genome-wide acceleration of protein evolution in flies (Diptera). BMC Evol Biol 2006, 6:7. BioMed Central Full Text
- [58]Bonneton F, Laudet V: Evolution of nuclear receptors in insects. In Insect endocrinology. Edited by Gilbert LI. Amsterdam, Boston: Academic Press; Elsevier; 2012:219.
- [59]Kondrashov AS, Sunyaev S, Kondrashov FA: Dobzhansky-Muller incompatibilities in protein evolution. Proc Natl Acad Sci U S A 2002, 99(23):14878-14883.
- [60]Gloor G, Engels W: Single fly DNA preps for PCR. Drosophila Information Service 1992, 71:148-149.
- [61]Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN, et al.: Evolution of genes and genomes on the Drosophila phylogeny. Nature 2007, 450(7167):203-218.
- [62]Cruz J, Martin D, Pascual N, Maestro JL, Piulachs MD, Belles X: Quantity does matter. Juvenile hormone and the onset of vitellogenesis in the German cockroach. Insect Biochem Mol Biol 2003, 33(12):1219-1225.
- [63]Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591.
- [64]Galtier N, Gouy M, Gautier C: SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 1996, 12(6):543-548.
- [65]Yeates DK, Wiegmann BM: Congruence and controversy: toward a higher-level phylogeny of Diptera. Annu Rev Entomol 1999, 44:397-428.
- [66]Remsen J, O’Grady P: Phylogeny of Drosophilinae (Diptera: Drosophilidae), with comments on combined analysis and character support. Mol Phylogenet Evol 2002, 24(2):249-264.
- [67]Weller SJ, Friedlander TP, Martin JA, Pashley DP: Phylogenetic studies of ribosomal RNA variation in higher moths and butterflies (Lepidoptera: Ditrysia). Mol Phylogenet Evol 1992, 1(4):312-337.
- [68]Regier JC, Mitter C, Friedlander TP, Peigler RS: Re: Phylogenetic relationships in Sphingidae (Insecta: Lepidoptera): initial evidence from two nuclear genes. Mol Phylogenet Evol 2001, 20(2):311-316.
- [69]Lo N, Bandi C, Watanabe H, Nalepa C, Beninati T: Evidence for cocladogenesis between diverse dictyopteran lineages and their intracellular endosymbionts. Mol Biol Evol 2003, 20(6):907-913.
- [70]Kristensen NP: Phylogeny of insect orders. Annu Rev Entomol 1981, 26:135-157.
- [71]Whiting MF, Carpenter JC, Wheeler QD, Wheeler WC: The streptisera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst Biol 1997, 46:1-68.
- [72]Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA, Winterton SL, Yeates DK: Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol 2009, 7:34. BioMed Central Full Text
- [73]R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2009.
- [74]Yang Z, Wong WS, Nielsen R: Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005, 22(4):1107-1118.