Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae

English version

Autoři: Jordan J. Tyrrell ^aff001; Jackson T. Wilbourne ^aff001; Alisa A. Omelchenko ^aff001; Jin Yoon ^aff001; Lina Ni ^aff001
Působiště autorů: School of Neuroscience, Virginia Tech, Blacksburg, Virginia, United States of America ^aff001
Vyšlo v časopise: Ionotropic Receptor-dependent cool cells control the transition of temperature preference in Drosophila larvae. PLoS Genet 17(4): e1009499. doi:10.1371/journal.pgen.1009499
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009499

Souhrn

Temperature sensation guides animals to avoid temperature extremes and to seek their optimal temperatures. The larval stage of Drosophila development has a dramatic effect on temperature preference. While early-stage Drosophila larvae pursue a warm temperature, late-stage larvae seek a significantly lower temperature. Previous studies suggest that this transition depends on multiple rhodopsins at the late larval stage. Here, we show that early-stage larvae, in which dorsal organ cool cells (DOCCs) are functionally blocked, exhibit similar cool preference to that of wild type late-stage larvae. The molecular thermoreceptors in DOCCs are formed by three members of the Ionotropic Receptor (IR) family, IR21a, IR93a, and IR25a. Early-stage larvae of each Ir mutant pursue a cool temperature, similar to that of wild type late-stage larvae. At the late larval stage, DOCCs express decreased IR proteins and exhibit reduced cool responses. Importantly, late-stage larvae that overexpress IR21a, IR93a, and IR25a in DOCCs exhibit similar warm preference to that of wild type early-stage larvae. These data suggest that IR21a, IR93a, and IR25a in DOCCs navigate early-stage larvae to avoid cool temperatures and the reduction of these IR proteins in DOCCs results in animals remaining in cool regions during the late larval stage. Together with previous studies, we conclude that multiple temperature-sensing systems are regulated for the transition of temperature preference in fruit fly larvae.

Klíčová slova:

Behavior – Body temperature – Drosophila melanogaster – Larvae – Neuronal dendrites – Neurons – Sensory perception – Temperature gradients

Zdroje

1. Garrity PA, Goodman MB, Samuel AD, Sengupta P. Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. Genes & development. 2010;24(21):2365–82.

2. Brown AW. Factors in the attractiveness of bodies for mosquitoes. Nature. 1951;167(4240):202. doi: 10.1038/167202a0 14806426

3. Howlett FM. The Influence of Temperature upon the Biting of Mosquitoes. Parasitology. 1910;3(4):479–84.

4. Corfas RA, Vosshall LB. The cation channel TRPA1 tunes mosquito thermotaxis to host temperatures. eLife. 2015;4:e11750. doi: 10.7554/eLife.11750 26670734

5. Benelli G, Mehlhorn H. Declining malaria, rising of dengue and Zika virus: insights for mosquito vector control. Parasitology research. 2016;115(5):1747–54. doi: 10.1007/s00436-016-4971-z 26932263

6. Greppi C, Budelli G, Garrity PA. Some like it hot, but not too hot. eLife. 2015;4.

7. Greppi C, Laursen WJ, Budelli G, Chang EC, Daniels AM, van Giesen L, et al. Mosquito heat seeking is driven by an ancestral cooling receptor. Science (New York, NY). 2020;367(6478):681–4. doi: 10.1126/science.aay9847 32029627

8. Luo L, Gershow M, Rosenzweig M, Kang K, Fang-Yen C, Garrity PA, et al. Navigational decision making in Drosophila thermotaxis. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010;30(12):4261–72. doi: 10.1523/JNEUROSCI.4090-09.2010 20335462

9. Sokabe T, Chen HC, Luo J, Montell C. A Switch in Thermal Preference in Drosophila Larvae Depends on Multiple Rhodopsins. Cell reports. 2016;17(2):336–44. doi: 10.1016/j.celrep.2016.09.028 27705783

10. Barbagallo B, Garrity PA. Temperature sensation in Drosophila. Current opinion in neurobiology. 2015;34:8–13. doi: 10.1016/j.conb.2015.01.002 25616212

11. Li K, Gong Z. Feeling Hot and Cold: Thermal Sensation in Drosophila. Neuroscience bulletin. 2017;33(3):317–22. doi: 10.1007/s12264-016-0087-9 27995563

12. Liu L, Yermolaieva O, Johnson WA, Abboud FM, Welsh MJ. Identification and function of thermosensory neurons in Drosophila larvae. Nature neuroscience. 2003;6(3):267–73. doi: 10.1038/nn1009 12563263

13. Klein M, Afonso B, Vonner AJ, Hernandez-Nunez L, Berck M, Tabone CJ, et al. Sensory determinants of behavioral dynamics in Drosophila thermotaxis. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(2):E220–9. doi: 10.1073/pnas.1416212112 25550513

14. Turner HN, Armengol K, Patel AA, Himmel NJ, Sullivan L, Iyer SC, et al. The TRP Channels Pkd2, NompC, and Trpm Act in Cold-Sensing Neurons to Mediate Unique Aversive Behaviors to Noxious Cold in Drosophila. Current biology: CB. 2016;26(23):3116–28. doi: 10.1016/j.cub.2016.09.038 27818173

15. Kwon Y, Shen WL, Shim HS, Montell C. Fine thermotactic discrimination between the optimal and slightly cooler temperatures via a TRPV channel in chordotonal neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010;30(31):10465–71.

16. Rosenzweig M, Kang K, Garrity PA. Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(38):14668–73. doi: 10.1073/pnas.0805041105 18787131

17. Ni L, Klein M, Svec KV, Budelli G, Chang EC, Ferrer AJ, et al. The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila. eLife. 2016;5. doi: 10.7554/eLife.13254 27126188

18. Knecht ZA, Silbering AF, Ni L, Klein M, Budelli G, Bell R, et al. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. eLife. 2016;5. doi: 10.7554/eLife.17879 27656904

19. Budelli G, Ni L, Berciu C, van Giesen L, Knecht ZA, Chang EC, et al. Ionotropic Receptors Specify the Morphogenesis of Phasic Sensors Controlling Rapid Thermal Preference in Drosophila. Neuron. 2019. doi: 10.1016/j.neuron.2018.12.022 30654923

20. Gallio M, Ofstad TA, Macpherson LJ, Wang JW, Zuker CS. The coding of temperature in the Drosophila brain. Cell. 2011;144(4):614–24. doi: 10.1016/j.cell.2011.01.028 21335241

21. Sweeney ST, Broadie K, Keane J, Niemann H, O’Kane CJ. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron. 1995;14(2):341–51. doi: 10.1016/0896-6273(95)90290-2 7857643

22. Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, et al. Independent optical excitation of distinct neural populations. Nat Methods. 2014;11(3):338–46. doi: 10.1038/nmeth.2836 24509633

23. Clark DA, Kohler D, Mathis A, Slankster E, Kafle S, Odell SR, et al. Tracking Drosophila Larval Behavior in Response to Optogenetic Stimulation of Olfactory Neurons. Journal of visualized experiments: JoVE. 2018(133). doi: 10.3791/57353 29630041

24. Hernandez-Nunez L, Belina J, Klein M, Si G, Claus L, Carlson JR, et al. Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics. eLife. 2015;4. doi: 10.7554/eLife.06225 25942453

25. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature. 2013;499(7458):295–300. doi: 10.1038/nature12354 23868258

26. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell. 2009;136(1):149–62. doi: 10.1016/j.cell.2008.12.001 19135896

27. Abuin L, Bargeton B, Ulbrich MH, Isacoff EY, Kellenberger S, Benton R. Functional architecture of olfactory ionotropic glutamate receptors. Neuron. 2011;69(1):44–60. doi: 10.1016/j.neuron.2010.11.042 21220098

28. Li Q, DeBeaubien NA, Sokabe T, Montell C. Temperature and Sweet Taste Integration in Drosophila. Current biology: CB. 2020;30(11):2051–67.e5.

29. Liu J, Sokabe T, Montell C. A Temperature Gradient Assay to Determine Thermal Preferences of Drosophila Larvae. Journal of visualized experiments: JoVE. 2018(136). doi: 10.3791/57963 29985331

30. Abuin L, Prieto-Godino LL, Pan H, Gutierrez C, Huang L, Jin R, et al. In vivo assembly and trafficking of olfactory Ionotropic Receptors. BMC biology. 2019;17(1):34. doi: 10.1186/s12915-019-0651-7 30995910

31. Rytz R, Croset V, Benton R. Ionotropic receptors (IRs): chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect biochemistry and molecular biology. 2013;43(9):888–97. doi: 10.1016/j.ibmb.2013.02.007 23459169

32. Pfeiffer BD, Truman JW, Rubin GM. Using translational enhancers to increase transgene expression in Drosophila. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(17):6626–31. doi: 10.1073/pnas.1204520109 22493255

33. Chen C, Buhl E, Xu M, Croset V, Rees JS, Lilley KS, et al. Drosophila Ionotropic Receptor 25a mediates circadian clock resetting by temperature. Nature. 2015;527(7579):516–20. doi: 10.1038/nature16148 26580016

34. Sanchez-Alcaniz JA, Silbering AF, Croset V, Zappia G, Sivasubramaniam AK, Abuin L, et al. An expression atlas of variant ionotropic glutamate receptors identifies a molecular basis of carbonation sensing. Nature communications. 2018;9(1):4252. doi: 10.1038/s41467-018-06453-1 30315166

35. Kwon Y, Shim HS, Wang X, Montell C. Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nature neuroscience. 2008;11(8):871–3. doi: 10.1038/nn.2170 18660806

36. Brooks DS, Vishal K, Kawakami J, Bouyain S, Geisbrecht ER. Optimization of wrMTrck to monitor Drosophila larval locomotor activity. Journal of insect physiology. 2016;93–94:11–7. doi: 10.1016/j.jinsphys.2016.07.007 27430166

37. Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, Jenkins AM, et al. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature. 2011;481(7379):76–80. doi: 10.1038/nature10715 22139422

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