Co-expression of six tightly clustered odorant receptor genes in the antenna of the malaria mosquito Anopheles gambiae

Frontiers in Ecology and Evolution

Volumn 3, Issue MAR, 2015, Pages

  Karner, Tim ^a   Kellner, Isabelle ^a   Schultze, Anna ^a   Breer, Heinz ^a   Krieger, Jürgen ^a,b  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Antenna; Expression; Insect olfaction; Odorant receptor; Polycistronic mRNA

Indexed keywords

EID: 84989935376     PISSN: None     EISSN: 2296701X     Source Type: Journal    
DOI: 10.3389/fevo.2015.00026     Document Type: Article

References (45)

1. Adler, E., Hoon, M. A., Mueller, K. L., Chandrashekar, J., Ryba, N. J., and Zuker, C. S. (2000). A novel family of mammalian taste receptors. Cell 100, 693-702. doi: 10.1016/S0092-8674(00)80705-9
2. Angerer, L. M., and Angerer, R. C. (1992). "In situ hybridization to cellular RNA with radiolabelled RNA probes". in In Situ Hybridization, ed D. G. Wilkinson (Oxford: IRL Press), 15-32
3. Benton, R., Vannice, K. S., Gomez-Diaz, C., and Vosshall, L. B. (2009). Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149-162. doi: 10.1016/j.cell.2008.12.001
4. Blumenthal, T. (2004). Operons in eukaryotes. Brief. Funct. Genomic. Proteomic. 3, 199-211. doi: 10.1093/bfgp/3.3.199
5. Bohbot, J., Pitts, R. J., Kwon, H. W., Rutzler, M., Robertson, H. M., and Zwiebel, L. J. (2007). Molecular characterization of the Aedes aegypti odorant receptor gene family. Insect. Mol. Biol. 16, 525-537. doi: 10.1111/j.1365-2583.2007.00748.x
6. Carey, A. F., Wang, G., Su, C. Y., Zwiebel, L. J., and Carlson, J. R. (2010). Odorant reception in the malaria mosquito Anopheles gambiae. Nature 464, 66-71. doi: 10.1038/nature08834
7. Chandrashekar, J., Mueller, K. L., Hoon, M. A., Adler, E., Feng, L., Guo, W., et al. (2000). T2Rs function as bitter taste receptors. Cell 100, 703-711. doi: 10.1016/S0092-8674(00)80706-0
8. Couto, A., Alenius, M., and Dickson, B. J. (2005). Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535-1547. doi: 10.1016/j.cub.2005.07.034
9. Dahanukar, A., Lei, Y. T., Kwon, J. Y., and Carlson, J. R. (2007). Two Gr genes underlie sugar reception in Drosophila. Neuron 56, 503-516. doi: 10.1016/j.neuron.2007.10.024
10. Dobritsa, A. A., van der Goes van Naters, W., Warr, C. G., Steinbrecht, R. A., and Carlson, J. R. (2003). Integrating the molecular and cellular basis of odor coding in the Drosophila antenna. Neuron 37, 827-841. doi: 10.1016/S0896-6273(03)00094-1
11. Dormont, L., Bessiere, J. M., and Cohuet, A. (2013). Human skin volatiles: a review. J. Chem. Ecol. 39, 569-578. doi: 10.1007/s10886-013-0286-z
12. Dreos, R., Ambrosini, G., Cavin, P. R., and Bucher, P. (2013). EPD and EPDnew, high-quality promoter resources in the next-generation sequencing era. Nucleic Acids Res. 41, D157-D164. doi: 10.1093/nar/gks1233
13. Engsontia, P., Sanderson, A. P., Cobb, M., Walden, K. K., Robertson, H. M., and Brown, S. (2008). The red flour beetle's large nose: an expanded odorant receptor gene family in Tribolium castaneum. Insect Biochem. Mol. Biol. 38, 387-397. doi: 10.1016/j.ibmb.2007.10.005
14. Fishilevich, E., and Vosshall, L. B. (2005). Genetic and functional subdivision of the Drosophila antennal lobe. Curr. Biol. 15, 1548-1553. doi: 10.1016/j.cub.2005.07.066
15. Fox, A. N., Pitts, R. J., and Zwiebel, L. J. (2002). A cluster of candidate odorant receptors from the malaria vector mosquito, Anopheles gambiae. Chem. Senses 27, 453-459. doi: 10.1093/chemse/27.5.453
16. Galindo, M. I., Pueyo, J. I., Fouix, S., Bishop, S. A., and Couso, J. P. (2007). Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol. 5:e106. doi: 10.1371/journal.pbio.0050106
17. Guidobaldi, F., May-Concha, I. J., and Guerenstein, P. G. (2014). Morphology and physiology of the olfactory system of blood-feeding insects. J. Physiol. Paris 108, 96-111. doi: 10.1016/j.jphysparis.2014.04.006
18. Hallem, E. A., Ho, M. G., and Carlson, J. R. (2004). The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965-979. doi: 10.1016/j.cell.2004.05.012
19. Hansson, B. S., and Stensmyr, M. C. (2011). Evolution of insect olfaction. Neuron 72, 698-711. doi: 10.1016/j.neuron.2011.11.003
20. Hill, C. A., Fox, A. N., Pitts, R. J., Kent, L. B., Tan, P. L., Chrystal, M. A., et al. (2002). G protein-coupled receptors in Anopheles gambiae. Science 298, 176-178. doi: 10.1126/science.1076196
21. Himeidan, Y. E., Temu, E. A., El Rayah, E. A., Munga, S., and Kweka, E. J. (2013). Chemical cues for malaria vectors oviposition site selection: challenges and opportunities. J. Insects 2013:685182. doi: 10.1155/2013/685182
22. Iatrou, K., and Biessmann, H. (2008). Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae. Insect Biochem. Mol. Biol. 38, 268-274. doi: 10.1016/j.ibmb.2007.11.008
23. Jacquin-Joly, E., and Merlin, C. (2004). Insect olfactory receptors: contributions of molecular biology to chemical ecology. J. Chem. Ecol. 30, 2359-2397. doi: 10.1007/s10886-004-7941-3
24. Kwon, H. W., Lu, T., Rutzler, M., and Zwiebel, L. J. (2006). Olfactory responses in a gustatory organ of the malaria vector mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 103, 13526-13531. doi: 10.1073/pnas.0601107103
25. Kwon, J. Y., Dahanukar, A., Weiss, L. A., and Carlson, J. R. (2007). The molecular basis of CO2 reception in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 104, 3574-3578. doi: 10.1073/pnas.0700079104
26. Lin, M. F., Carlson, J. W., Crosby, M. A., Matthews, B. B., Yu, C., Park, S., et al. (2007). Revisiting the protein-coding gene catalog of Drosophila melanogaster using 12 fly genomes. Genome Res. 17, 1823-1836. doi: 10.1101/gr.6679507
27. Lu, T., Qiu, Y. T., Wang, G., Kwon, J. Y., Rutzler, M., Kwon, H. W., et al. (2007). Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr. Biol. 17, 1533-1544. doi: 10.1016/j.cub.2007.07.062
28. McIver, S. B. (1982). Sensilla of mosquitoes (Diptera: Culicidae). J. Med. Entomol. 19, 489-535
29. Pi, H., Lee, L. W., and Lo, S. J. (2009). New insights into polycistronic transcripts in eukaryotes. Chang Gung. Med. J. 32, 494-498
30. Pitts, R. J., Rinker, D. C., Jones, P. L., Rokas, A., and Zwiebel, L. J. (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. doi: 10.1186/1471-2164-12-271
31. Pitts, R. J., and Zwiebel, L. J. (2006). Antennal sensilla of two female anopheline sibling species with differing host ranges. Malaria J. 5:26. doi: 10.1186/1475-2875-5-26
32. Qiu, Y. T., van Loon, J. J., Takken, W., Meijerink, J., and Smid, H. M. (2006). Olfactory coding in antennal neurons of the malaria mosquito, Anopheles gambiae. Chem. Senses 31, 845-863. doi: 10.1093/chemse/bjl027
33. Ray, A., van Naters, W. G., Shiraiwa, T., and Carlson, J. R. (2007). Mechanisms of odor receptor gene choice in Drosophila. Neuron 53, 353-369. doi: 10.1016/j.neuron.2006.12.010
34. Rinker, D. C., Pitts, R. J., Zhou, X., Suh, E., Rokas, A., and Zwiebel, L. J. (2013). Blood meal-induced changes to antennal transcriptome profiles reveal shifts in odor sensitivities in Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 110, 8260-8265. doi: 10.1073/pnas.1302562110
35. Robertson, H. M., and Wanner, K. W. (2006). The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res. 16, 1395-1403. doi: 10.1101/gr.5057506
36. Rytz, R., Croset, V., and Benton, R. (2013). Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem. Mol. Biol. 43, 888-897. doi: 10.1016/j.ibmb.2013.02.007
37. Schultze, A., Breer, H., and Krieger, J. (2014). The blunt trichoid sensillum of female mosquitoes, Anopheles gambiae: odorant binding protein and receptor types. Int. J. Biol. Sci. 10, 426-437. doi: 10.7150/ijbs.8754
38. Schultze, A., Pregitzer, P., Walter, M. F., Woods, D. F., Marinotti, O., Breer, H., et al. (2013). The co-expression pattern of odorant binding proteins and olfactory receptors identify distinct trichoid sensilla on the antenna of the malaria mosquito Anopheles gambiae. PLoS ONE 8:e69412. doi: 10.1371/journal.pone.0069412
39. Slone, J., Daniels, J., and Amrein, H. (2007). Sugar receptors in Drosophila. Curr. Biol. 17, 1809-1816. doi: 10.1016/j.cub.2007.09.027
40. Takken, W., and Knols, B. G. (1999). Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 44, 131-157. doi: 10.1146/annurev.ento.44.1.131
41. Tauxe, G. M., MacWilliam, D., Boyle, S. M., Guda, T., and Ray, A. (2013). Targeting a dual detector of skin and CO2 to modify mosquito host seeking. Cell 155, 1365-1379. doi: 10.1016/j.cell.2013.11.013
42. Touhara, K., and Vosshall, L. B. (2009). Sensing odorants and pheromones with chemosensory receptors. Annu. Rev. Physiol. 71, 307-332. doi: 10.1146/annurev.physiol.010908.163209
43. Wang, G., Carey, A. F., Carlson, J. R., and Zwiebel, L. J. (2010). Molecular basis of odor coding in the malaria vector mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 107, 4418-4423. doi: 10.1073/pnas.0913392107
44. WHO (2013). World Malaria Report. Geneva: WHO Press
45. Zwiebel, L. J., and Takken, W. (2004). Olfactory regulation of mosquito-host interactions. Insect Biochem. Mol. Biol. 34, 645-652. doi: 10.1016/j.ibmb.2004.03.017