Molecules and Cells

  • 제44권12호
  • /
  • Pages.900-910
  • /
  • 2021
  • /
  • 1016-8478(pISSN)
  • /
  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
권호 표지
DOI QR코드

DOI QR Code

Mechanisms of Carboxylic Acid Attraction in Drosophila melanogaster

  • Shrestha, Bhanu (Department of Bio and Fermentation Convergence Technology, Kookmin University) ;
  • Lee, Youngseok (Department of Bio and Fermentation Convergence Technology, Kookmin University)
  • 투고 : 2021.08.02
  • 심사 : 2021.10.15
  • 발행 : 2021.12.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Sour is one of the fundamental taste modalities that enable taste perception in animals. Chemoreceptors embedded in taste organs are pivotal to discriminate between different chemicals to ensure survival. Animals generally prefer slightly acidic food and avoid highly acidic alternatives. We recently proposed that all acids are aversive at high concentrations, a response that is mediated by low pH as well as specific anions in Drosophila melanogaster. Particularly, some carboxylic acids such as glycolic acid, citric acid, and lactic acid are highly attractive to Drosophila compared with acetic acid. The present study determined that attractive carboxylic acids were mediated by broadly expressed Ir25a and Ir76b, as demonstrated by a candidate mutant library screen. The mutant deficits were completely recovered via wild-type cDNA expression in sweet-sensing gustatory receptor neurons. Furthermore, sweet gustatory receptors such as Gr5a, Gr61a, and Gr64a-f modulate attractive responses. These genetic defects were confirmed using binary food choice assays as well as electrophysiology in the labellum. Taken together, our findings demonstrate that at least two different kinds of receptors are required to discriminate attractive carboxylic acids from other acids.

키워드

과제정보

This work was supported by grants to Y.L. from the Basic Science Research Program of the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2021R1A2C1007628) and the Korea Environmental Industry and Technology Institute (KEITI) grant funded by the Ministry of Environment of Korea. B.S. was supported by the Global Scholarship Program for Foreign Graduate Students at Kookmin University in Korea. We would like to thank S. Dhakal for the help of tip recordings.

참고문헌

  1. Abuin, L., Bargeton, B., Ulbrich, M.H., Isacoff, E.Y., Kellenberger, S., and Benton, R. (2011). Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69, 44-60. https://doi.org/10.1016/j.neuron.2010.11.042
  2. Al-Anzi, B., Tracey, W.D., Jr., and Benzer, S. (2006). Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr. Biol. 16, 1034-1040. https://doi.org/10.1016/j.cub.2006.04.002
  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. https://doi.org/10.1016/j.cell.2008.12.001
  4. Cameron, P., Hiroi, M., Ngai, J., and Scott, K. (2010). The molecular basis for water taste in Drosophila. Nature 465, 91-95. https://doi.org/10.1038/nature09011
  5. Chen, Y. and Amrein, H. (2017). Ionotropic receptors mediate Drosophila oviposition preference through sour gustatory receptor neurons. Curr. Biol. 27, 2741-2750.e4. https://doi.org/10.1016/j.cub.2017.08.003
  6. Chen, Y.C.D. and Dahanukar, A. (2020). Recent advances in the genetic basis of taste detection in Drosophila. Cell. Mol. Life Sci. 77, 1087-1101. https://doi.org/10.1007/s00018-019-03320-0
  7. Dahanukar, A., Foster, K., van der Goes van Naters, W.M., and Carlson, J.R. (2001). A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat. Neurosci. 4, 1182-1186. https://doi.org/10.1038/nn765
  8. 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. https://doi.org/10.1016/j.neuron.2007.10.024
  9. Dethier, V.G. (1976). The Hungry Fly: A Physiological Study of the Behavior Associated with Feeding (Cambridge: Harvard University Press).
  10. Devineni, A.V., Sun, B., Zhukovskaya, A., and Axel, R. (2019). Acetic acid activates distinct taste pathways in Drosophila to elicit opposing, state-dependent feeding responses. Elife 8, e47677. https://doi.org/10.7554/elife.47677
  11. Dunipace, L., Meister, S., McNealy, C., and Amrein, H. (2001). Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 11, 822-835. https://doi.org/10.1016/S0960-9822(01)00258-5
  12. Falk, R., Bleiser-Avivi, N., and Atidia, J. (1976). Labellar taste organs of Drosophila melanogaster. J. Morphol. 150, 327-341. https://doi.org/10.1002/jmor.1051500206
  13. Fujishiro, N., Kijima, H., and Morita, H. (1984). Impulse frequency and action potential amplitude in labellar chemosensory neurones of Drosophila melanogaster. J. Insect Physiol. 30, 317-325. https://doi.org/10.1016/0022-1910(84)90133-1
  14. Ganguly, A., Chandel, A., Turner, H., Wang, S., Liman, E.R., and Montell, C. (2021). Requirement for an Otopetrin-Like protein for acid taste in Drosophila. BioRxiv, https://doi.org/10.1101/2021.06.18.449071
  15. Ganguly, A., Pang, L., Duong, V.K., Lee, A., Schoniger, H., Varady, E., and Dahanukar, A. (2017). A molecular and cellular context-dependent role for Ir76b in detection of amino acid taste. Cell Rep. 18, 737-750. https://doi.org/10.1016/j.celrep.2016.12.071
  16. Hiroi, M., Marion-Poll, F., and Tanimura, T. (2002). Differentiated response to sugars among labellar chemosensilla in Drosophila. Zoolog. Sci. 19, 1009-1018. https://doi.org/10.2108/zsj.19.1009
  17. Hiroi, M., Meunier, N., Marion-Poll, F., and Tanimura, T. (2004). Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333-342. https://doi.org/10.1002/neu.20063
  18. Jiao, Y., Moon, S.J., and Montell, C. (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. https://doi.org/10.1073/pnas.0702421104
  19. Jiao, Y., Moon, S.J., Wang, X., Ren, Q., and Montell, C. (2008). Gr64f is required in combination with other gustatory receptors for sugar detection in Drosophila. Curr. Biol. 18, 1797-1801. https://doi.org/10.1016/j.cub.2008.10.009
  20. Kim, H., Kim, H., Kwon, J.Y., Seo, J.T., Shin, D.M., and Moon, S.J. (2018). Drosophila Gr64e mediates fatty acid sensing via the phospholipase C pathway. PLoS Genet. 14, e1007229. https://doi.org/10.1371/journal.pgen.1007229
  21. Kim, S.H., Lee, Y., Akitake, B., Woodward, O.M., Guggino, W.B., and Montell, C. (2010). Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc. Natl. Acad. Sci. U. S. A. 107, 8440-8445. https://doi.org/10.1073/pnas.1001425107
  22. Lee, M.J., Sung, H.Y., Jo, H., Kim, H.W., Choi, M.S., Kwon, J.Y., and Kang, K. (2017). Ionotropic receptor 76b is required for gustatory aversion to excessive Na+ in Drosophila. Mol. Cells 40, 787-795. https://doi.org/10.14348/MOLCELLS.2017.0160
  23. Lee, Y., Kim, S.H., and Montell, C. (2010). Avoiding DEET through insect gustatory receptors. Neuron 67, 555-561. https://doi.org/10.1016/j.neuron.2010.07.006
  24. Lee, Y., Moon, S.J., and Montell, C. (2009). Multiple gustatory receptors required for the caffeine response in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 106, 4495-4500. https://doi.org/10.1073/pnas.0811744106
  25. Lee, Y., Poudel, S., Kim, Y., Thakur, D., and Montell, C. (2018). Calcium taste avoidance in Drosophila. Neuron 97, 67-74.e4. https://doi.org/10.1016/j.neuron.2017.11.038
  26. Marella, S., Fischler, W., Kong, P., Asgarian, S., Rueckert, E., and Scott, K. (2006). Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285-295. https://doi.org/10.1016/j.neuron.2005.11.037
  27. Meunier, N., Marion-Poll, F., Rospars, J.P., and Tanimura, T. (2003). Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139-152. https://doi.org/10.1002/neu.10235
  28. Mi, T., Mack, J.O., Lee, C.M., and Zhang, Y.V. (2021). Molecular and cellular basis of acid taste sensation in Drosophila. Nat. Commun. 12, 3730. https://doi.org/10.1038/s41467-021-23490-5
  29. Miyamoto, T. and Amrein, H. (2014). Diverse roles for the Drosophila fructose sensor Gr43a. Fly (Austin) 8, 19-25. https://doi.org/10.4161/fly.27241
  30. Miyamoto, T., Chen, Y., Slone, J., and Amrein, H. (2013). Identification of a Drosophila glucose receptor using Ca2+ imaging of single chemosensory neurons. PLoS One 8, e56304. https://doi.org/10.1371/journal.pone.0056304
  31. Miyamoto, T., Slone, J., Song, X., and Amrein, H. (2012). A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 151, 1113-1125. https://doi.org/10.1016/j.cell.2012.10.024
  32. Moon, S.J., Kottgen, M., Jiao, Y., Xu, H., and Montell, C. (2006). A taste receptor required for the caffeine response in vivo. Curr. Biol. 16, 1812-1817. https://doi.org/10.1016/j.cub.2006.07.024
  33. Nayak, S.V. and Singh, R.N. (1983). Sensilla on the tarsal segments and mouthparts of adult Drosophila melanogaster Meigen (Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol. 12, 273-291. https://doi.org/10.1016/0020-7322(83)90023-5
  34. Paradis, S., Sweeney, S.T., and Davis, G.W. (2001). Homeostatic control of presynaptic release is triggered by postsynaptic membrane depolarization. Neuron 30, 737-749. https://doi.org/10.1016/S0896-6273(01)00326-9
  35. Prieto-Godino, L.L., Rytz, R., Bargeton, B., Abuin, L., Arguello, J.R., Dal Peraro, M., and Benton, R. (2016). Olfactory receptor pseudo-pseudogenes. Nature 539, 93-97. https://doi.org/10.1038/nature19824
  36. Prieto-Godino, L.L., Rytz, R., Cruchet, S., Bargeton, B., Abuin, L., Silbering, A.F., Ruta, V., Dal Peraro, M., and Benton, R. (2017). Evolution of acid-sensing olfactory circuits in drosophilids. Neuron 93, 661-676.e6. https://doi.org/10.1016/j.neuron.2016.12.024
  37. Puri, S. and Lee, Y. (2021). Salt sensation and regulation. Metabolites 11, 175. https://doi.org/10.3390/metabo11030175
  38. Rimal, S. and Lee, Y. (2018). The multidimensional ionotropic receptors of Drosophila melanogaster. Insect Mol. Biol. 27, 1-7. https://doi.org/10.1111/imb.12347
  39. Rimal, S., Sang, J., Poudel, S., Thakur, D., Montell, C., and Lee, Y. (2019). Mechanism of acetic acid gustatory repulsion in Drosophila. Cell Rep. 26, 1432-1442.e4. https://doi.org/10.1016/j.celrep.2019.01.042
  40. Robertson, H.M., Warr, C.G., and Carlson, J.R. (2003). Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 100(Suppl 2), 14537-14542. https://doi.org/10.1073/pnas.2335847100
  41. Roper, S.D. and Chaudhari, N. (2017). Taste buds: cells, signals and synapses. Nat. Rev. Neurosci. 18, 485-497. https://doi.org/10.1038/nrn.2017.68
  42. Sanchez-Alcaniz, J.A., Silbering, A.F., Croset, V., Zappia, G., Sivasubramaniam, A.K., Abuin, L., Sahai, S.Y., Munch, D., Steck, K., Auer, T.O., et al. (2018). An expression atlas of variant ionotropic glutamate receptors identifies a molecular basis of carbonation sensing. Nat. Commun. 9, 4252. https://doi.org/10.1038/s41467-018-06453-1
  43. Shanbhag, S., Park, S.K., Pikielny, C., and Steinbrecht, R.A. (2001). Gustatory organs of Drosophila melanogaster: fine structure and expression of the putative odorant-binding protein PBPRP2. Cell Tissue Res. 304, 423-437. https://doi.org/10.1007/s004410100388
  44. Shrestha, B. and Lee, Y. (2021). Mechanisms of DEET gustation in Drosophila. Insect Biochem. Mol. Biol. 131, 103550. https://doi.org/10.1016/j.ibmb.2021.103550
  45. Silbering, A.F., Rytz, R., Grosjean, Y., Abuin, L., Ramdya, P., Jefferis, G.S., and Benton, R. (2011). Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J. Neurosci. 31, 13357-13375. https://doi.org/10.1523/JNEUROSCI.2360-11.2011
  46. Stanley, M., Ghosh, B., Weiss, Z.F., Christiaanse, J., and Gordon, M.D. (2021). Mechanisms of lactic acid gustatory attraction in Drosophila. BioRxiv, https://doi.org/10.1101/2021.01.22.427705
  47. Thorne, N., Chromey, C., Bray, S., and Amrein, H. (2004). Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079. https://doi.org/10.1016/j.cub.2004.05.019
  48. Tu, Y.H., Cooper, A.J., Teng, B., Chang, R.B., Artiga, D.J., Turner, H.N., Mulhall, E.M., Ye, W., Smith, A.D., and Liman, E.R. (2018). An evolutionarily conserved gene family encodes proton-selective ion channels. Science 359, 1047-1050. https://doi.org/10.1126/science.aao3264
  49. Weiss, L.A., Dahanukar, A., Kwon, J.Y., Banerjee, D., and Carlson, J.R. (2011). The molecular and cellular basis of bitter taste in Drosophila. Neuron 69, 258-272. https://doi.org/10.1016/j.neuron.2011.01.001
  50. Wieczorek, H. and Wolff, G. (1989). The labellar sugar receptor of Drosophila. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 164, 825-834. https://doi.org/10.1007/BF00616754
  51. Wisotsky, Z., Medina, A., Freeman, E., and Dahanukar, A. (2011). Evolutionary differences in food preference rely on Gr64e, a receptor for glycerol. Nat. Neurosci. 14, 1534-1541. https://doi.org/10.1038/nn.2944
  52. Zhang, Y.V., Ni, J., and Montell, C. (2013). The molecular basis for attractive salt-taste coding in Drosophila. Science 340, 1334-1338. https://doi.org/10.1126/science.1234133
  53. Zhao, G.Q., Zhang, Y., Hoon, M.A., Chandrashekar, J., Erlenbach, I., Ryba, N.J., and Zuker, C.S. (2003). The receptors for mammalian sweet and umami taste. Cell 115, 255-266. https://doi.org/10.1016/S0092-8674(03)00844-4