An RNA-Seq Screen of the Antenna Identifies a Transporter Necessary for Ammonia Detection

English version České info

Olfaction underlies the attraction of insect pests and vectors of disease to their plant and human hosts. In the genetic model insect Drosophila, the neuronal basis of odor coding has been extensively analyzed in the antenna, its major olfactory organ, but the molecular basis of odor coding has not. Additionally, there has been little analysis of any olfactory cells other than neurons. We have undertaken a comprehensive and quantitative analysis of gene expression in the Drosophila antenna. This analysis revealed a surprisingly broad dynamic range of odor receptor and odor binding protein expression, and unexpected expression of taste receptor genes. Further analysis identified 250 genes that are expressed at reduced levels in a mutant lacking an evolutionarily ancient class of sensilla, antennal hairs housing neurons that respond to human odors. One of these genes, a transporter, is expressed in non-neuronal cells but is essential to the response of a neuron to ammonia, a key cue for insect vectors of disease. A mutation in this transporter can be rescued by its mosquito homolog. While many studies of sensory coding consider the neural circuit in isolation, our analysis reveals an essential role for an auxiliary cell.

Vyšlo v časopise: An RNA-Seq Screen of the Antenna Identifies a Transporter Necessary for Ammonia Detection. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004810
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004810

Souhrn

Zdroje

1. CareyAF, CarlsonJR (2011) Insect olfaction from model systems to disease control. Proc Natl Acad Sci U S A 108: 12987–12995.

2. van der Goes van NatersW, CarlsonJR (2006) Insects as chemosensors of humans and crops. Nature 444: 302–307.

3. ShanbhagS, MullerB, SteinbrechtA (1999) Atlas of olfactory organs of Drosophila melanogaster. 1. Types, external organization, innervation and distribution of olfactory sensilla. Int J Insect Morphol Embryol 28: 377–397.

4. StockerRF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275: 3–26.

5. SilberingAF, RytzR, GrosjeanY, AbuinL, RamdyaP, et al. (2011) Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J Neurosci 31: 13357–13375.

6. YaoCA, IgnellR, CarlsonJR (2005) Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25: 8359–8367.

7. van der Goes van NatersW, CarlsonJR (2007) Receptors and neurons for fly odors in Drosophila. Curr Biol 17: 606–612.

8. de BruyneM, FosterK, CarlsonJR (2001) Odor coding in the Drosophila antenna. Neuron 30: 537–552.

9. HallemEA, HoMG, CarlsonJR (2004) The molecular basis of odor coding in the Drosophila antenna. Cell 117: 965–979.

10. FishilevichE, VosshallLB (2005) Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15: 1548–1553.

11. CoutoA, AleniusM, DicksonBJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15: 1535–1547.

12. LarssonMC, DomingosAI, JonesWD, ChiappeME, AmreinH, et al. (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43: 703–714.

13. AbuinL, BargetonB, UlbrichMH, IsacoffEY, KellenbergerS, et al. (2011) Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69: 44–60.

14. CrosetV, RytzR, CumminsSF, BuddA, BrawandD, et al. (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6: e1001064.

15. BentonR, VanniceKS, Gomez-DiazC, VosshallLB (2009) Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila. Cell 136: 149–162.

16. QiuYT, van LoonJJA, TakkenW, MeijerinkJ, SmidHM (2006) Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chemical Senses 31: 845–863.

17. MeijerinkJ, BraksMA, Van LoonJJ (2001) Olfactory receptors on the antennae of the malaria mosquito Anopheles gambiae are sensitive to ammonia and other sweat-borne components. J Insect Physiol 47: 455–464.

18. SyedZ, LealWS (2009) Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc Natl Acad Sci U S A 106: 18803–18808.

19. ShanbhagSR, MullerB, SteinbrechtRA (2000) Atlas of olfactory organs of Drosophila melanogaster 2. Internal organization and cellular architecture of olfactory sensilla. Arthropod Struct Dev 29: 211–229.

20. LealWS (2013) Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu Rev Entomol 58: 373–391.

21. Vogt RG (2003) Biochemical diversity of odor detection: OBPs, ODEs, and SNMPs. In: Blomquist GJ, Vogt RG, editors. Insect pheromone biochemistry and molecular biology: the biosynthesis and detection of pheromones and plant volatiles. Amsterdam: Elsevier. pp. 391-445.

22. RutzlerM, ZwiebelLJ (2005) Molecular biology of insect olfaction: recent progress and conceptual models. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191: 777–790.

23. GuptaBP, RodriguesV (1997) Atonal is a proneural gene for a subset of olfactory sense organs in Drosophila. Genes Cells 2: 225–233.

24. VosshallLB, WongAM, AxelR (2000) An olfactory sensory map in the fly brain. Cell 102: 147–159.

25. ClynePJ, WarrCG, FreemanMR, LessingD, KimJ, et al. (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22: 327–338.

26. GoldmanAL, Van der Goes van NatersW, LessingD, WarrCG, CarlsonJR (2005) Coexpression of two functional odor receptors in one neuron. Neuron 45: 661–666.

27. SenthilanPR, PiepenbrockD, OvezmyradovG, NadrowskiB, BechstedtS, et al. (2012) Drosophila auditory organ genes and genetic hearing defects. Cell 150: 1042–1054.

28. GaliziaCG, MunchD, StrauchM, NisslerA, MaS (2010) Integrating heterogeneous odor response data into a common response model: A DoOR to the complete olfactome. Chem Senses 35: 551–563.

29. MarshallB, WarrCG, de BruyneM (2010) Detection of volatile indicators of illicit substances by the olfactory receptors of Drosophila melanogaster. Chem Senses 35: 613–625.

30. RootCM, SemmelhackJL, WongAM, FloresJ, WangJW (2007) Propagation of olfactory information in Drosophila. Proc Natl Acad Sci U S A 104: 11826–11831.

31. MiyamotoT, SloneJ, SongX, AmreinH (2012) A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 151: 1113–1125.

32. FreemanEG, WisotskyZ, DahanukarA (2014) Detection of sweet tastants by a conserved group of insect gustatory receptors. Proc Natl Acad Sci U S A 111: 1598–1603.

33. SatoK, TanakaK, TouharaK (2011) Sugar-regulated cation channel formed by an insect gustatory receptor. Proc Natl Acad Sci U S A 108: 11680–11685.

34. DahanukarA, LeiYT, KwonJY, CarlsonJR (2007) Two Gr genes underlie sugar reception in Drosophila. Neuron 56: 503–516.

35. JiaoY, MoonSJ, MontellC (2007) A Drosophila gustatory receptor required for the responses to sucrose, glucose, and maltose identified by mRNA tagging. Proc Natl Acad Sci U S A 104: 14110–14115.

36. SloneJ, DanielsJ, AmreinH (2007) Sugar receptors in Drosophila. Curr Biol 17: 1809–1816.

37. JiaoY, MoonSJ, WangX, RenQ, MontellC (2008) Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr Biol 18: 1797–1801.

38. JonesWD, CayirliogluP, KadowIG, VosshallLB (2007) Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445: 86–90.

39. KwonJY, DahanukarA, WeissLA, CarlsonJR (2007) The molecular basis of CO2 reception in Drosophila. Proc Natl Acad Sci U S A 104: 3574–3578.

40. TauxeGM, MacWilliamD, BoyleSM, GudaT, RayA (2013) Targeting a dual detector of skin and CO2 to modify mosquito host seeking. Cell 155: 1365–1379.

41. NiL, BronkP, ChangEC, LowellAM, FlamJO, et al. (2013) A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila. Nature 500: 580–584.

42. LeeY, MoonSJ, MontellC (2009) Multiple gustatory receptors required for the caffeine response in Drosophila. Proc Natl Acad Sci U S A 106: 4495–4500.

43. MoonSJ, KottgenM, JiaoY, XuH, MontellC (2006) A taste receptor required for the caffeine response in vivo. Curr Biol 16: 1812–1817.

44. LeeY, KimSH, MontellC (2010) Avoiding DEET through insect gustatory receptors. Neuron 67: 555–561.

45. XuP, AtkinsonR, JonesDN, SmithDP (2005) Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron 45: 193–200.

46. Hekmat-ScafeDS, ScafeCR, McKinneyAJ, TanouyeMA (2002) Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12: 1357–1369.

47. GalindoK, SmithDP (2001) A large family of divergent Drosophila odorant-binding proteins expressed in gustatory and olfactory sensilla. Genetics 159: 1059–1072.

48. ZhouJJ, HuangW, ZhangGA, PickettJA, FieldLM (2004) "Plus-C" odorant-binding protein genes in two Drosophila species and the malaria mosquito Anopheles gambiae. Gene 327: 117–129.

49. CameronP, HiroiM, NgaiJ, ScottK (2010) The molecular basis for water taste in Drosophila. Nature 465: 91–95.

50. DamannN, VoetsT, NiliusB (2008) TRPs in our senses. Curr Biol 18: R880–889.

51. Al-AnziB, TraceyWDJr, BenzerS (2006) Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr Biol 16: 1034–1040.

52. KwonY, KimSH, RonderosDS, LeeY, AkitakeB, et al. (2010) Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr Biol 20: 1672–1678.

53. BadshaF, KainP, PrabhakarS, SundaramS, PadinjatR, et al. (2012) Mutants in Drosophila TRPC channels reduce olfactory sensitivity to carbon dioxide. PLoS One 7: e49848.

54. SunY, LiuL, Ben-ShaharY, JacobsJS, EberlDF, et al. (2009) TRPA channels distinguish gravity sensing from hearing in Johnston's organ. Proc Natl Acad Sci U S A 106: 13606–13611.

55. GallioM, OfstadTA, MacphersonLJ, WangJW, ZukerCS (2011) The coding of temperature in the Drosophila brain. Cell 144: 614–624.

56. LiuL, LiY, WangR, YinC, DongQ, et al. (2007) Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature 450: 294–298.

57. JhaveriD, SenA, RodriguesV (2000) Mechanisms underlying olfactory neuronal connectivity in Drosophila-the atonal lineage organizes the periphery while sensory neurons and glia pattern the olfactory lobe. Dev Biol 226: 73–87.

58. JarmanAP, GrellEH, AckermanL, JanLY, JanYN (1994) Atonal is the proneural gene for Drosophila photoreceptors. Nature 369: 398–400.

59. PikielnyCW, HasanG, RouyerF, RosbashM (1994) Members of a family of Drosophila putative odorant-binding proteins are expressed in different subsets of olfactory hairs. Neuron 12: 35–49.

60. StarostinaE, LiuT, VijayanV, ZhengZ, SiwickiKK, et al. (2012) A Drosophila DEG/ENaC subunit functions specifically in gustatory neurons required for male courtship behavior. J Neurosci 32: 4665–4674.

61. JarmanA, GrauY, JanL, JanY (1993) atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73: 1307–1321.

62. MariniAM, VissersS, UrrestarazuA, AndreB (1994) Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J 13: 3456–3463.

63. NinnemannO, JauniauxJC, FrommerWB (1994) Identification of a high affinity NH4+ transporter from plants. EMBO J 13: 3464–3471.

64. PengJ, HuangCH (2006) Rh proteins vs Amt proteins: an organismal and phylogenetic perspective on CO2 and NH3 gas channels. Transfus Clin Biol 13: 85–94.

65. TanejaJG (1997) P.M (1997) Ammonia attracts the haematophagous bug Triatoma infestans: behavioural and neurophysiological data on nymphs. J Comp Physiol A 181: 21–34.

66. GeierM, BoschOJ, BoeckhJ (1999) Ammonia as an attractive component of host odour for the yellow fever mosquito, Aedes aegypti. Chem Senses 24: 647–653.

67. BraksMAH, MeijerinkJ, TakkenW (2001) The response of the malaria mosquito, Anopheles gambiae, to two components of human sweat, ammonia and L-lactic acid, in an olfactometer. Physiol Entomol 26: 142–148.

68. HaggartDA, DavisEE (1980) Ammonia-sensitive neurones on the first tarsi of the tick, Rhipicephalus Sanguineus. J Insect Physiol 26: 517–523.

69. MinS, AiM, ShinSA, SuhGS (2013) Dedicated olfactory neurons mediating attraction behavior to ammonia and amines in Drosophila. Proc Natl Acad Sci U S A 110: E1321–1329.

70. AltnerH, SassH, AltnerI (1977) Relationship between structure and function of antennal chemo-, hygro-, and thermoreceptive sensilla in Periplaneta americana. Cell Tissue Res 176: 389–405.

71. HarracaV, IgnellR, LofstedtC, RyneC (2010) Characterization of the antennal olfactory system of the bed bug (Cimex lectularius). Chem Senses 35: 195–204.

72. BellenHJ, LevisRW, LiaoG, HeY, CarlsonJW, et al. (2004) The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167: 761–781.

73. CookRK, ChristensenSJ, DealJA, CoburnRA, DealME, et al. (2012) The generation of chromosomal deletions to provide extensive coverage and subdivision of the Drosophila melanogaster genome. Genome Biol 13: R21.

74. HingHK, BangaloreL, SunX, Artavanis-TsakonasS (1999) Mutations in the heatshock cognate 70 protein (hsc4) modulate Notch signaling. Eur J Cell Biol 78: 690–697.

75. KaisslingKE (1986) Chemo-electrical transduction in insect olfactory receptors. Ann Rev Neurosci 9: 121–145.

76. OlsenSR, BhandawatV, WilsonRI (2007) Excitatory interactions between olfactory processing channels in the Drosophila antennal lobe. Neuron 54: 89–103.

77. RayA, van NatersWG, ShiraiwaT, CarlsonJR (2007) Mechanisms of odor receptor gene choice in Drosophila. Neuron 53: 353–369.

78. ShiaoM-S, FanW-L, FangS, LuM-YJ, KondoR, et al. (2013) Transcriptional profiling of adult Drosophila antennae by high-throughput sequencing. Zoological Studies 52: 1–10.

79. SwarupS, WilliamsTI, AnholtRR (2011) Functional dissection of Odorant binding protein genes in Drosophila melanogaster. Genes Brain Behav 10: 648–657.

80. LiX, SchulerMA, BerenbaumMR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52: 231–253.

81. HeydelJM, CoelhoA, ThiebaudN, LegendreA, Le BonAM, et al. (2013) Odorant-binding proteins and xenobiotic metabolizing enzymes: implications in olfactory perireceptor events. Anat Rec (Hoboken) 296: 1333–1345.

82. LegeaiF, MalpelS, MontagneN, MonsempesC, CousseransF, et al. (2011) An Expressed Sequence Tag collection from the male antennae of the Noctuid moth Spodoptera littoralis: a resource for olfactory and pheromone detection research. BMC Genomics 12: 86.

83. PittsRJ, RinkerDC, JonesPL, RokasA, ZwiebelLJ (2011) Transcriptome profiling of chemosensory appendages in the malaria vector Anopheles gambiae reveals tissue- and sex-specific signatures of odor coding. BMC Genomics 12: 271.

84. HovemannBT, SehlmeyerF, MalzJ (1997) Drosophila melanogaster NADPH-cytochrome P450 oxidoreductase: pronounced expression in antennae may be related to odorant clearance. Gene 189: 213–219.

85. WangQ, HasanG, PikielnyCW (1999) Preferential expression of biotransformation enzymes in the olfactory organs of Drosophila melanogaster, the antennae. J Biol Chem 274: 10309–10315.

86. Maibeche-CoisneM, NikonovAA, IshidaY, Jacquin-JolyE, LealWS (2004) Pheromone anosmia in a scarab beetle induced by in vivo inhibition of a pheromone-degrading enzyme. Proc Natl Acad Sci U S A 101: 11459–11464.

87. von Wiren N, Merrick M (2004) Regulation and function of ammonium carriers in bacteria, fungi, and plants. In: Boles E, Kramer R, editors. Molecular Mechanisms Controlling Transmembrane Transport. Berlin: Springer. pp. 95-120.

88. TsayYF, HoCH, ChenHY, LinSH (2011) Integration of nitrogen and potassium signaling. Annu Rev Plant Biol 62: 207–226.

89. NakhoulNL, Lee HammL (2013) Characteristics of mammalian Rh glycoproteins (SLC42 transporters) and their role in acid-base transport. Mol Aspects Med 34: 629–637.

90. WeinerID, VerlanderJW (2014) Ammonia transport in the kidney by Rhesus glycoproteins. Am J Physiol Renal Physiol 306: F1107–F1120.

91. WeihrauchD, DoniniA, O'DonnellMJ (2012) Ammonia transport by terrestrial and aquatic insects. J Insect Physiol 58: 473–487.

92. WuY, ZhengX, ZhangM, HeA, LiZ, et al. (2010) Cloning and functional expression of Rh50-like glycoprotein, a putative ammonia channel, in Aedes albopictus mosquitoes. J Insect Physiol 56: 1599–1610.

93. WaterhouseRM, TegenfeldtF, LiJ, ZdobnovEM, KriventsevaEV (2013) OrthoDB: a hierarchical catalog of animal, fungal and bacterial orthologs. Nucleic Acids Res 41: D358–365.

94. LealWS, ChooYM, XuP, da SilvaCS, Ueira-VieiraC (2013) Differential expression of olfactory genes in the southern house mosquito and insights into unique odorant receptor gene isoforms. Proc Natl Acad Sci U S A 110: 18704–18709.

95. MamidalaP, WijeratneAJ, WijeratneS, PolandT, QaziSS, et al. (2013) Identification of odor-processing genes in the emerald ash borer, Agrilus planipennis. PLoS One 8: e56555.

96. LiuY, GuS, ZhangY, GuoY, WangG (2012) Candidate olfaction genes identified within the Helicoverpa armigera Antennal Transcriptome. PLoS One 7: e48260.

97. AiM, BlaisS, ParkJY, MinS, NeubertTA, et al. (2013) Ionotropic glutamate receptors IR64a and IR8a form a functional odorant receptor complex in vivo in Drosophila. J Neurosci 33: 10741–10749.

98. BrowneA, O'DonnellMJ (2013) Ammonium secretion by Malpighian tubules of Drosophila melanogaster: application of a novel ammonium-selective microelectrode. J Exp Biol 216: 3818–3827.

99. BorashDJ, GibbsAG, JoshiA, MuellerLD (1998) A genetic polymorphism maintained by natural selection in a temporally varying environment. Am Nat 151: 148–156.

100. TrussellLO, FischbachGD (1989) Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3: 209–218.

101. OverstreetLS, JonesMV, WestbrookGL (2000) Slow desensitization regulates the availability of synaptic GABA(A) receptors. J Neurosci 20: 7914–7921.

102. ChertempsT, FrancoisA, DurandN, RosellG, DekkerT, et al. (2012) A carboxylesterase, Esterase-6, modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila. BMC Biol 10: 56.

103. LeeT, LuoL (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451–461.

104. ThibaultST, SingerMA, MiyazakiWY, MilashB, DompeNA, et al. (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36: 283–287.

105. PfeifferBD, JenettA, HammondsAS, NgoTT, MisraS, et al. (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A 105: 9715–9720.

106. KohTW, HeZ, Gorur-ShandilyaS, MenuzK, LarterNK, et al. (2014) The Drosophila IR20a Clade of Ionotropic Receptors Are Candidate Taste and Pheromone Receptors. Neuron 83: 850–865.

107. WangJW, BeckES, McCabeBD (2012) A modular toolset for recombination transgenesis and neurogenetic analysis of Drosophila. PLoS One 7: e42102.

108. GrothAC, FishM, NusseR, CalosMP (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775–1782.

109. MarksteinM, PitsouliC, VillaltaC, CelnikerSE, PerrimonN (2008) Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes. Nat Genet 40: 476–483.

110. SmithCD, ShuS, MungallCJ, KarpenGH (2007) The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316: 1586–1591.

111. R Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

112. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.

113. CarbonS, IrelandA, MungallCJ, ShuS, MarshallB, et al. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25: 288–289.

114. DobritsaAA, van der Goes van NatersW, WarrCG, SteinbrechtRA, CarlsonJR (2003) Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37: 827–841.

115. Kaissling KE, Thorson J (1980) Insect olfactory sensilla: Structural, chemical and electrical aspects of the functional organization. In: Sattelle DB, Hall LM, Hildebrand JG, editors. Receptors for neurotransmitters, hormones, and pheromones in insects. Amsterdam: Elsevier/North-Holland pp. 261-282.

116. GuY, LucasP, RosparsJP (2009) Computational model of the insect pheromone transduction cascade. PLoS Comput Biol 5: e1000321.

117. DweckHK, EbrahimSA, KromannS, BownD, HillburY, et al. (2013) Olfactory preference for egg laying on citrus substrates in Drosophila. Curr Biol 23: 2472–2480.

118. RonderosDS, LinCC, PotterCJ, SmithDP (2014) Farnesol-detecting olfactory neurons in Drosophila. J Neurosci 34: 3959–3968.