Chemosensory sensilla of the Drosophila wing express a candidate ionotropic pheromone receptor

Chemosensory sensilla of the Drosophila wing express a candidate ionotropic pheromone receptor
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DOI:
10.1371/journal.pbio.2006619
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发表时间:
2019-05-01
期刊:
影响因子:
9.8
通讯作者:
Carlson, John R.
Carlson, John R.
中科院分区:
生物学1区
文献类型:
--
作者:
He, Zhe;Luo, Yichen;Carlson, John R.

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果蝇的翅膀在35年前就被认为是一种味觉器官,但关于它在化学感受中的作用的研究非常少。我们对前翅缘的一排感器进行了差异RNA测序分析,发现了许多与信息素和化学感知相关的基因的表达。要问这些感受器是否可能接受信息素输入,我们设计了一个染料转移范例,发现大的,疏水分子相当于信息素可以从一个苍蝇转移到另一个翅膀边缘。一个基因,离子型受体(IR)52 a,在这些感器的神经元中与性回路的标志物fruitless共表达; IR 52 a也在腿中表达。IR 52 a的突变和IR 52 a(+)神经元的光遗传学沉默降低了男性性行为的水平。IR 52 a(+)神经元的光遗传激活诱导雄性向其他雄性求爱,特别是向另一个物种的雌性求爱。令人惊讶的是,IR 52 a也是女性正常性行为所必需的。在交配的雌性中,IR 52 a(+)神经元的光遗传激活诱导交配,这通常发生在非常低的水平。与其他在雄性中起作用以抑制雄性-雄性相互作用和促进雄性-雌性相互作用的化学感受器不同,IR 52 a在雄性和雌性中都起作用,并且可以促进雄性-雄性以及雄性-雌性相互作用。此外,IR 52 a(+)神经元可以覆盖通常抑制对非生产性目标的性行为的电路。使用trans-Tango系统的电路映射和Ca 2+成像揭示了食管下区(SEZ)中IR 52 a(+)神经元的二级投射,其中一些是性二型的。翅膀中IR 52 a(+)神经元的光遗传激活激活了SEZ中的二级投射。两者合计,这项研究提供了一个分子描述的化学感受器的一个大大不足的味觉器官,并定义了一个基因,调节性电路的苍蝇。
The Drosophila wing was proposed to be a taste organ more than 35 years ago, but there has been remarkably little study of its role in chemoreception. We carry out a differential RNA-seq analysis of a row of sensilla on the anterior wing margin and find expression of many genes associated with pheromone and chemical perception. To ask whether these sensilla might receive pheromonal input, we devised a dye-transfer paradigm and found that large, hydrophobic molecules comparable to pheromones can be transferred from one fly to the wing margin of another. One gene, Ionotropic receptor (IR)52a, is coexpressed in neurons of these sensilla with fruitless, a marker of sexual circuitry; IR52a is also expressed in legs. Mutation of IR52a and optogenetic silencing of IR52a(+) neurons decrease levels of male sexual behavior. Optogenetic activation of IR52a(+) neurons induces males to show courtship toward other males and, remarkably, toward females of another species. Surprisingly, IR52a is also required in females for normal sexual behavior. Optogenetic activation of IR52a(+) neurons in mated females induces copulation, which normally occurs at very low levels. Unlike other chemoreceptors that act in males to inhibit male-male interactions and promote male-female interactions, IR52a acts in both males and females, and can promote male-male as well as male-female interactions. Moreover, IR52a(+) neurons can override the circuitry that normally suppresses sexual behavior toward unproductive targets. Circuit mapping and Ca2+ imaging using the trans-Tango system reveals second-order projections of IR52a(+) neurons in the subesophageal zone (SEZ), some of which are sexually dimorphic. Optogenetic activation of IR52a(+) neurons in the wing activates second-order projections in the SEZ. Taken together, this study provides a molecular description of the chemosensory sensilla of a greatly understudied taste organ and defines a gene that regulates the sexual circuitry of the fly.