Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade

Regulation of olfactory-based sex behaviors in the silkworm by genes in the sex-determination cascade
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性别决定级联中基因对蚕基于嗅觉的性别行为的调节

DOI:
10.1371/journal.pgen.1008622
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发表时间:
2020
期刊:
影响因子:
4.5
通讯作者:
Yongping Huang
Yongping Huang
中科院分区:
生物学2区
文献类型:
--
作者:
Jun Xu;Wei Liu;Dehong Yang;Shuqing Chen;Kai Chen;Zulian Liu;Xu Yang;Jing Meng;Guanheng Zhu;Shuanglin Dong;Yong Zhang;Shuai Zhan;Guirong Wang;Yongping Huang

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昆虫的求偶和交配依赖于嗅觉、视觉和触觉信号的整合。与其他昆虫相比,家蚕(家蚕)的性行为相对简单,因为它不会飞。通过使用CRISPR/Cas和电生理技术,我们发现雄性蚕蛾的求爱和交配行为是通过性别决定级联中属于两条保守途径的基因突变来调节的。Bmdsx基因表达的缺失,通过减少BmOR1基因产物的表达,显著降低了主要信息素成分蚕蛹kol的外周感知,从而完全阻断了成年雄性的求偶行为。有趣的是,我们发现交配行为是由另一个性别分化基因Bmfru独立调节的。失去Bmfru完全阻碍了交配,但雄性表现出正常的求爱行为。由于BmOR3表达下调,缺乏Bmfru表达显著降低了对次要信息素成分bombykal的感知;此外,功能分析表明BmOR3产物的缺失在雄性交配行为的终止中起着关键作用。我们的研究结果表明,Bmdsx和Bmfru是调节以嗅觉为基础的性行为的两条主要途径的基础。昆虫的基本性行为——求偶和交配,是嗅觉、视觉、触觉和其他复杂先天行为成功整合的结果。在广泛应用的昆虫模型——黑腹果蝇(Drosophila melanogaster)中,性别决定级联基因无果和双性参与了求爱和交配行为的调节;然而,这些性别分化基因在鳞翅目昆虫性行为调控中的作用尚不清楚。本研究将遗传学和电生理学相结合,对鳞翅目模式昆虫家蚕的性行为调控途径进行了研究。我们的研究结果支持家蚕中存在两种遗传途径,分别是Bmdsx-BmOR1-bombykol和Bmfru-BmOR3-bombykal,它们控制着由嗅觉调节的雄性性行为的不同方面。本文首次全面报道了性别分化基因在蚕蛾雄性性行为中的作用。
Insect courtship and mating depend on integration of olfactory, visual, and tactile cues. Compared to other insects, Bombyx mori, the domesticated silkworm, has relatively simple sexual behaviors as it cannot fly. Here by using CRISPR/Cas and electrophysiological techniques we found that courtship and mating behaviors are regulated in male silk moths by mutating genes in the sex determination cascade belonging to two conserved pathways. Loss of Bmdsx gene expression significantly reduced the peripheral perception of the major pheromone component bombykol by reducing expression of the product of the BmOR1 gene which completely blocked courtship in adult males. Interestingly, we found that mating behavior was regulated independently by another sexual differentiation gene, Bmfru. Loss of Bmfru completely blocked mating, but males displayed normal courtship behavior. Lack of Bmfru expression significantly reduced the perception of the minor pheromone component bombykal due to the down regulation of BmOR3 expression; further, functional analysis revealed that loss of the product of BmOR3 played a key role in terminating male mating behavior. Our results suggest that Bmdsx and Bmfru are at the base of the two primary pathways that regulate olfactory-based sexual behavior. Author Summary The fundamental insect sexual behaviors, courtship and mating, result from successful integration of olfactory, vision, tactile and other complex innate behaviors. In the widely used insect model, Drosophila melanogaster, the sex determination cascade genes fruitless and doublesex are involved in the regulation of courtship and mating behaviors; however, little is known about the function of these sexual differentiation genes in regulating sex behaviors of Lepidoptera. Here we combine genetics and electrophysiology to investigate regulation pathway of sexual behaviors in the model lepidopteran insect, the domesticated silk moth, Bombyx mori. Our results support the presence of two genetic pathways in B. mori, named Bmdsx-BmOR1-bombykol and Bmfru-BmOR3-bombykal, which control distinct aspects of male sexual behavior that are modulated by olfaction. This is the first comprehensive report about the role of sex differentiation genes in the male sexual behavior in the silk moth.