#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Transposable Element Insertion Confers Xenobiotic Resistance in Drosophila


Given the predictions of future environmental fluctuations, it is crucial to understand how organisms adapt to changing environments. The fruit fly Drosophila melanogaster is an ideal model organism to study environmental adaptation because of our deep understanding of developmental, physiological, and metabolic networks, as well as the ease of experimental manipulation. In this study, we showed that a previously identified putatively adaptive mutation, the insertion of the transposable element FBti0019627, mediates resistance to both natural and synthetic xenobiotics in Drosophila melanogaster. By combining experimental and computational approaches, we further elucidated the molecular and the biochemical mechanisms underlying this natural adaptive mutation. Our results should be relevant for other organisms as well since there are many similarities between species in the way cells respond to stress.


Vyšlo v časopise: A Transposable Element Insertion Confers Xenobiotic Resistance in Drosophila. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004560
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004560

Souhrn

Given the predictions of future environmental fluctuations, it is crucial to understand how organisms adapt to changing environments. The fruit fly Drosophila melanogaster is an ideal model organism to study environmental adaptation because of our deep understanding of developmental, physiological, and metabolic networks, as well as the ease of experimental manipulation. In this study, we showed that a previously identified putatively adaptive mutation, the insertion of the transposable element FBti0019627, mediates resistance to both natural and synthetic xenobiotics in Drosophila melanogaster. By combining experimental and computational approaches, we further elucidated the molecular and the biochemical mechanisms underlying this natural adaptive mutation. Our results should be relevant for other organisms as well since there are many similarities between species in the way cells respond to stress.


Zdroje

1. StapleyJ, RegerJ, FeulnerPGD, SmadjaC, GalindoJ, et al. (2010) Adaptation genomics: the next generation. Trends Ecol Evol 25: 705–712 doi:10.1016/j.tree.2010.09.002

2. KorvesTM, SchmidKJ, CaicedoAL, MaysC, StinchcombeJR, et al. (2007) Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. Am Nat 169: E141–57 doi:10.1086/513111

3. TishkoffSA, ReedFA, RanciaroA, VoightBF, BabbittCC, et al. (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39: 31–40 doi:10.1038/ng1946

4. SchluterD, MarchinkoKB, BarrettRDH, RogersSM (2010) Natural selection and the genetics of adaptation in threespine stickleback. Philos Trans R Soc Lond B Biol Sci 365: 2479–2486 doi:10.1098/rstb.2010.0036

5. LinnenCR, PohY-P, PetersonBK, BarrettRDH, LarsonJG, et al. (2013) Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339: 1312–1316 doi:10.1126/science.1233213

6. WuR (2012) Predicting the Genotype-Phenotype Map of Complex Traits. J Biom Biostat 03: 3–5 doi:10.4172/2155-6180.1000e109

7. LehnerB (2013) Genotype to phenotype: lessons from model organisms for human genetics. Nat Rev Genet 14: 168–178 doi:10.1038/nrg3404

8. HouleD, GovindarajuDR, OmholtS (2010) Phenomics: the next challenge. Nat Rev Genet 11: 855–866 doi:10.1038/nrg2897

9. SwarupS, HuangW, MackayTFC, AnholtRRH (2013) Analysis of natural variation reveals neurogenetic networks for Drosophila olfactory behavior. Proc Natl Acad Sci U S A 110: 1017–1022 doi:10.1073/pnas.1220168110

10. AyrolesJF, CarboneMA, StoneEA, JordanKW, LymanRF, et al. (2009) Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41: 299–307 doi:10.1038/ng.332

11. MackayTFC, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173–178 doi:10.1038/nature10811

12. HuangW, RichardsS, CarboneMA, ZhuD, AnholtRRH, et al. (2012) Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc Natl Acad Sci U S A 109: 15553–15559 doi:10.1073/pnas.1213423109

13. BiémontC, VieiraC (2006) Junk DNA as an evolutionary force. Nature 443: 521–524 doi:10.1038/443521a

14. ChénaisB, CarusoA, HiardS, CasseN (2012) The impact of transposable elements on eukaryotic genomes: from genome size increase to genetic adaptation to stressful environments. Gene 509: 7–15 doi: 10.1016/j.gene.2012.07.042

15. CasacubertaE, GonzálezJ (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22: 1503–1517 doi:10.1111/mec.12170

16. GonzálezJ, LenkovK, LipatovM, MacphersonJM, PetrovDA (2008) High rate of recent transposable element-induced adaptation in Drosophila melanogaster. PLoS Biol 6: e251 doi:10.1371/journal.pbio.0060251

17. GonzálezJ, KarasovTL, MesserPW, PetrovDA (2010) Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLoS Genet 6: e1000905 doi:10.1371/journal.pgen.1000905

18. GonzálezJ, MacphersonJM, MesserPW, PetrovDA (2009) Inferring the strength of selection in Drosophila under complex demographic models. Mol Biol Evol 26: 513–526 doi:10.1093/molbev/msn270

19. GonzálezJ, MacphersonJM, PetrovDA (2009) A recent adaptive transposable element insertion near highly conserved developmental loci in Drosophila melanogaster. Mol Biol Evol 26: 1949–1961 doi:10.1093/molbev/msp107

20. AminetzachYT, MacphersonJM, PetrovDA (2005) Pesticide resistance via transposition-mediated adaptive gene truncation in Drosophila. Science 309: 764–767 doi:10.1126/science.1112699

21. MagwireMM, BayerF, WebsterCL, CaoC, JigginsFM (2011) Successive increases in the resistance of Drosophila to viral infection through a transposon insertion followed by a Duplication. PLoS Genet 7: e1002337 doi: 10.1371/journal.pgen.1002337

22. GuioL, BarrónMG, GonzálezJ (2014) The transposable element Bari-Jheh mediates oxidative stress response in Drosophila. Mol Ecol 23: 2020–2030 doi: 10.1111/mec.12711

23. MarygoldSJ, LeylandPC, SealRL, GoodmanJL, ThurmondJ, et al. (2013) FlyBase: improvements to the bibliography. Nucleic Acids Res 41: D751–7 doi:10.1093/nar/gks1024

24. OkamuraK, BallaS, MartinR, LiuN, LaiEC (2008) Two distinct mechanisms generate endogenous siRNAs from bidirectional transcription in Drosophila melanogaster. Nat Struct Mol Biol 15: 581–590 doi:10.1038/nsmb.1438

25. RetelskaD, IseliC, BucherP, JongeneelCV, NaefF (2006) Similarities and differences of polyadenylation signals in human and fly. BMC Genomics 7: 176 doi:10.1186/1471-2164-7-176

26. SandbergR, NeilsonJR, SarmaA, SharpPA, BurgeCB (2008) Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites. Science 320: 1643–1647 doi:10.1126/science.1155390

27. Di GiammartinoDC, NishidaK, ManleyJL (2011) Mechanisms and consequences of alternative polyadenylation. Mol Cell 43: 853–866 doi:10.1016/j.molcel.2011.08.017

28. GiotL, BaderJS, BrouwerC, ChaudhuriA, KuangB, et al. (2003) A protein interaction map of Drosophila melanogaster. Science 302: 1727–1736 doi:10.1126/science.1090289

29. ArthaudL, BenRokia-Mille S, RaadH, DombrovskyA, PrevostN, et al. (2011) Trade-off between toxicity and signal detection orchestrated by frequency- and density-dependent genes. PLoS One 6: e19805 doi:10.1371/journal.pone.0019805

30. MarchittiSA, BrockerC, OrlickyDJ, VasiliouV (2010) Molecular characterization, expression analysis, and role of ALDH3B1 in the cellular protection against oxidative stress. Free Radic Biol Med 49: 1432–1443 doi:10.1016/j.freeradbiomed.2010.08.004

31. SinghAK, PandeyOP, SenguptaSK (2013) Synthesis, spectral and antimicrobial activity of Zn(II) complexes with Schiff bases derived from 2-hydrazino-5-[substituted phenyl]-1,3,4-thiadiazole and benzaldehyde/2-hydroxyacetophenone/indoline-2,3-dione. Spectrochim Acta A Mol Biomol Spectrosc 113: 393–399 doi: 10.1016/j.saa.2013.04.045

32. MattiaCJ, AdamsJD, BondySC (1993) Free radical induction in the brain and liver by products of toluene catabolism. Biochem Pharmacol 46: 103–110.

33. LindahlR, PetersenDR (1991) Lipid aldehyde oxidation as a physiological role for class 3 aldehyde dehydrogenases. Biochem Pharmacol 41: 1583–1587.

34. R'KhaS, CapyP, DavidJR (1991) Host-plant specialization in the Drosophila melanogaster species complex: a physiological, behavioral, and genetical analysis. Proc Natl Acad Sci U S A 88: 1835–1839.

35. MattheisJP, BuchananDA, FellmanJK (1992) Volatile compounds emitted by sweet cherries (Prunus avium Cv. Bing) during fruit development and ripening. J Agric Food Chem 40: 471–474.

36. AllenEMG, AndersonDGR, FlorangVR, KhannaM, HurleyDT, et al. (2011) Relative inhibitory potency of molinate and metabolites with aldehyde dehydrogenase2: implications for the mechanism of enzyme inhibition. 23: 1843–1850 doi:10.1021/tx100317q.Relative

37. KoppakaV, ThompsonDC, ChenY, EllermannM, NicolaouKC, et al. (2012) Aldehyde dehydrogenase inhibitors: a comprehensive review of the pharmacology, mechanism of action, substrate specificity, and clinical application. Pharmacol Rev 64: 520–539 doi:10.1124/pr.111.005538

38. LiuZJ, SunYJ, RoseJ, ChungYJ, HsiaoCD, et al. (1997) The first structure of an aldehyde dehydrogenase reveals novel interactions between NAD and the Rossmann fold. Nat Struct Biol 4: 317–326.

39. MilatovicD, GuptaRC, DekundyA, MontineTJ, DettbarnW-D (2005) Carbofuran-induced oxidative stress in slow and fast skeletal muscles: prevention by memantine and atropine. Toxicology 208: 13–24 doi:10.1016/j.tox.2004.11.004

40. KambojA, KiranR, SandhirR (2006) N-acetylcysteine ameliorates carbofuran-induced alterations in lipid composition and activity of membrane bound enzymes. Mol Cell Biochem 286: 107–114 doi:10.1007/s11010-005-9100-8

41. RaiDK, SharmaB (2007) Carbofuran-induced oxidative stress in mammalian brain. Mol Biotechnol 37: 66–71 doi:10.1007/s12033-007-0046-9

42. LaFaveMC, SekelskyJ (2011) Transcription initiation from within P elements generates hypomorphic mutations in Drosophila melanogaster. Genetics 188: 749–752 doi:10.1534/genetics.111.129825

43. GirardotF, MonnierV, TricoireH (2004) Genome wide analysis of common and specific stress responses in adult drosophila melanogaster. BMC Genomics 5: 74 doi:10.1186/1471-2164-5-74

44. StępniakJ, LewińskiA, Karbownik-LewińskaM (2013) Membrane lipids and nuclear DNA are differently susceptive to Fenton reaction substrates in porcine thyroid. Toxicol In Vitro 27: 71–78 doi:10.1016/j.tiv.2012.09.010

45. GahanLJ, GouldF, HeckelDG (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293: 857–860.

46. DabornPJ, YenJL, BogwitzMR, Le GoffG, FeilE, et al. (2002) A Single P450 Allele Associated with Insecticide Resistance in Drosophila. 297: 2253–2256.

47. SchlenkeTA, BegunDJ (2004) Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci U S A 101: 1626–1631.

48. Rostant WG, Wedell N, Hosken DJ (2012) Transposable elements and insecticide resistance. 1st ed. Elsevier Inc. doi:10.1016/B978-0-12-394394-1.00002-X.

49. LiX, SchulerMA, BerenbaumMR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52: 231–253 doi: 10.1146/annurev.ento.51.110104.151104

50. ChenS, LiX (2007) Transposable elements are enriched within or in close proximity to xenobiotic-metabolizing cytochrome P450 genes. BMC Evol Biol 7: 46 doi: 10.1186/1471-2148-7-46

51. MayrC, BartelDP (2009) Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673–684 doi:10.1016/j.cell.2009.06.016

52. BenfeyPN, Mitchell-OldsT (2008) From genotype to phenotype: systems biology meets natural variation. Science 320: 495–497 doi:10.1126/science.1153716

53. BarrettRDH, HoekstraHE (2011) Molecular spandrels: tests of adaptation at the genetic level. Nat Rev Genet 12: 767–780 doi:10.1038/nrg3015

54. Fiston-LavierA-S, CarriganM, PetrovDA, GonzálezJ (2011) T-lex: a program for fast and accurate assessment of transposable element presence using next-generation sequencing data. Nucleic Acids Res 39: e36 doi:10.1093/nar/gkq1291

55. KoflerR, BetancourtAJ, SchlöttererC (2012) Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet 8: e1002487 doi: 10.1371/journal.pgen.1002487

56. Fiston-LavierA-S, BarronMG, PetrovDA, GonzalezJ (2014) T-lex2: genotyping, frequency estimation and re-annotation of transposable elements using single or pooled next-generation sequencing data. Cold Spring Harbor Labs Journals doi: 10.1101/002964

57. KhannaMR, StanleyBA, ThomasGH (2010) Towards a membrane proteome in Drosophila: a method for the isolation of plasma membrane. BMC Genomics 11: 302 doi:10.1186/1471-2164-11-302

58. MontoothKL, SiebenthallKT, ClarkAG (2006) Membrane lipid physiology and toxin catabolism underlie ethanol and acetic acid tolerance in Drosophila melanogaster. J Exp Biol 209: 3837–3850 Available: http://www.ncbi.nlm.nih.gov/pubmed/16985200. Accessed 28 April 2014.

59. FryJD, SaweikisM (2006) Aldehyde dehydrogenase is essential for both adult and larval ethanol resistance in Drosophila melanogaster. Genet Res 87: 87–92.

60. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al.. (2007) Comparative protein structure modeling using MODELLER. doi:10.1002/0471140864.ps0209s50.

61. HumphreyW, DalkeA, SchultenK (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33–38.

62. PhillipsJC, BraunR, WangW, GumbartJ, TajkhorshidE, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781–1802 doi: 10.1002/jcc.20289

63. LaskowskiRA, MacArthurMW, MossDB, ThorntonJM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26: 283–291 doi:10.1107/S0021889892009944

64. WiedersteinM, SipplMJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35: W407–10 doi:10.1093/nar/gkm290

65. RussellRB, BartonGJ (1992) Multiple protein sequence alignment from tertiary structure comparison: assignment of global and residue confidence levels. Proteins 14: 309–323 doi:10.1002/prot.340140216

66. JonesDT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195–202.

67. KabschW, SanderC (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577–2637.

68. KhannaM, ChenC-H, Kimble-HillA, ParajuliB, Perez-MillerS, et al. (2011) Discovery of a novel class of covalent inhibitor for aldehyde dehydrogenases. J Biol Chem 286: 43486–43494 doi: 10.1074/jbc.M111.293597

69. SeeligerD, de GrootBL (2010) Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J Comput Aided Mol Des 24: 417–422 doi: 10.1007/s10822-010-9352-6

70. TrottO, OlsonA (2011) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading. 31: 455–461 doi:10.1002/jcc.21334

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 8
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#