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H2O2-Sensitive Isoforms of Drosophila melanogaster TRPA1 Act in Bitter-Sensing Gustatory Neurons to Promote Avoidance of UV During Egg-Laying.

Publication ,  Journal Article
Guntur, AR; Gou, B; Gu, P; He, R; Stern, U; Xiang, Y; Yang, C-H
Published in: Genetics
February 2017

The evolutionarily conserved TRPA1 channel can sense various stimuli including temperatures and chemical irritants. Recent results have suggested that specific isoforms of Drosophila TRPA1 (dTRPA1) are UV-sensitive and that their UV sensitivity is due to H2O2 sensitivity. However, whether such UV sensitivity served any physiological purposes in animal behavior was unclear. Here, we demonstrate that H2O2-sensitive dTRPA1 isoforms promote avoidance of UV when adult Drosophila females are selecting sites for egg-laying. First, we show that blind/visionless females are still capable of sensing and avoiding UV during egg-laying when intensity of UV is high yet within the range of natural sunlight. Second, we show that such vision-independent UV avoidance is mediated by a group of bitter-sensing neurons on the proboscis that express H2O2-sensitive dTRPA1 isoforms. We show that these bitter-sensing neurons exhibit dTRPA1-dependent UV sensitivity. Importantly, inhibiting activities of these bitter-sensing neurons, reducing their dTRPA1 expression, or reducing their H2O2-sensitivity all significantly reduced blind females' UV avoidance, whereas selectively restoring a H2O2-sensitive isoform of dTRPA1 in these neurons restored UV avoidance. Lastly, we show that specifically expressing the red-shifted channelrhodopsin CsChrimson in these bitter-sensing neurons promotes egg-laying avoidance of red light, an otherwise neutral cue for egg-laying females. Together, these results demonstrate a physiological role of the UV-sensitive dTRPA1 isoforms, reveal that adult Drosophila possess at least two sensory systems for detecting UV, and uncover an unexpected role of bitter-sensing taste neurons in UV sensing.

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Published In

Genetics

DOI

EISSN

1943-2631

Publication Date

February 2017

Volume

205

Issue

2

Start / End Page

749 / 759

Location

United States

Related Subject Headings

  • Ultraviolet Rays
  • Taste
  • TRPC Cation Channels
  • TRPA1 Cation Channel
  • Protein Isoforms
  • Oviposition
  • Locomotion
  • Ion Channels
  • Hydrogen Peroxide
  • Female
 

Citation

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Guntur, A. R., Gou, B., Gu, P., He, R., Stern, U., Xiang, Y., & Yang, C.-H. (2017). H2O2-Sensitive Isoforms of Drosophila melanogaster TRPA1 Act in Bitter-Sensing Gustatory Neurons to Promote Avoidance of UV During Egg-Laying. Genetics, 205(2), 749–759. https://doi.org/10.1534/genetics.116.195172
Guntur, Ananya R., Bin Gou, Pengyu Gu, Ruo He, Ulrich Stern, Yang Xiang, and Chung-Hui Yang. “H2O2-Sensitive Isoforms of Drosophila melanogaster TRPA1 Act in Bitter-Sensing Gustatory Neurons to Promote Avoidance of UV During Egg-Laying.Genetics 205, no. 2 (February 2017): 749–59. https://doi.org/10.1534/genetics.116.195172.
Guntur, Ananya R., et al. “H2O2-Sensitive Isoforms of Drosophila melanogaster TRPA1 Act in Bitter-Sensing Gustatory Neurons to Promote Avoidance of UV During Egg-Laying.Genetics, vol. 205, no. 2, Feb. 2017, pp. 749–59. Pubmed, doi:10.1534/genetics.116.195172.
Guntur AR, Gou B, Gu P, He R, Stern U, Xiang Y, Yang C-H. H2O2-Sensitive Isoforms of Drosophila melanogaster TRPA1 Act in Bitter-Sensing Gustatory Neurons to Promote Avoidance of UV During Egg-Laying. Genetics. 2017 Feb;205(2):749–759.

Published In

Genetics

DOI

EISSN

1943-2631

Publication Date

February 2017

Volume

205

Issue

2

Start / End Page

749 / 759

Location

United States

Related Subject Headings

  • Ultraviolet Rays
  • Taste
  • TRPC Cation Channels
  • TRPA1 Cation Channel
  • Protein Isoforms
  • Oviposition
  • Locomotion
  • Ion Channels
  • Hydrogen Peroxide
  • Female