Menuz Karen, Larter Nikki K, Park Joori, Carlson John R
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, United States of America.
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, United States of America; Interdepartmental Neuroscience Program, Yale University, New Haven, Connecticut, United States of America.
PLoS Genet. 2014 Nov 20;10(11):e1004810. doi: 10.1371/journal.pgen.1004810. eCollection 2014 Nov.
Many insect vectors of disease detect their hosts through olfactory cues, and thus it is of great interest to understand better how odors are encoded. However, little is known about the molecular underpinnings that support the unique function of coeloconic sensilla, an ancient and conserved class of sensilla that detect amines and acids, including components of human odor that are cues for many insect vectors. Here, we generate antennal transcriptome databases both for wild type Drosophila and for a mutant that lacks coeloconic sensilla. We use these resources to identify genes whose expression is highly enriched in coeloconic sensilla, including many genes not previously implicated in olfaction. Among them, we identify an ammonium transporter gene that is essential for ammonia responses in a class of coeloconic olfactory receptor neurons (ORNs), but is not required for responses to other odorants. Surprisingly, the transporter is not expressed in ORNs, but rather in neighboring auxiliary cells. Thus, our data reveal an unexpected non-cell autonomous role for a component that is essential to the olfactory response to ammonia. The defective response observed in a Drosophila mutant of this gene is rescued by its Anopheles ortholog, and orthologs are found in virtually all insect species examined, suggesting that its role is conserved. Taken together, our results provide a quantitative analysis of gene expression in the primary olfactory organ of Drosophila, identify molecular components of an ancient class of olfactory sensilla, and reveal that auxiliary cells, and not simply ORNs, play an essential role in the coding of an odor that is a critical host cue for many insect vectors of human disease.
许多疾病的昆虫传播媒介通过嗅觉线索来探测宿主，因此，更深入地了解气味是如何编码的就变得非常有趣。然而，对于支持腔锥感器独特功能的分子基础，我们却知之甚少。腔锥感器是一类古老且保守的感器，能够探测胺类和酸类物质，包括人类气味中的某些成分，而这些成分是许多昆虫传播媒介的线索。在这里，我们生成了野生型果蝇和缺乏腔锥感器的突变体的触角转录组数据库。我们利用这些资源来鉴定那些在腔锥感器中表达高度富集的基因，其中包括许多以前未涉及嗅觉的基因。在这些基因中，我们鉴定出一个铵转运蛋白基因，它对于一类腔锥嗅觉受体神经元（ORN）对氨的反应至关重要，但对其他气味剂的反应则不是必需的。令人惊讶的是，该转运蛋白并非在ORN中表达，而是在相邻的辅助细胞中表达。因此，我们的数据揭示了一个对氨嗅觉反应至关重要的成分具有意想不到的非细胞自主作用。该基因的果蝇突变体中观察到的缺陷反应可由其按蚊直系同源基因挽救，并且在几乎所有检测的昆虫物种中都发现了直系同源基因，这表明其作用是保守的。综上所述，我们的结果对果蝇主要嗅觉器官中的基因表达进行了定量分析，鉴定了一类古老嗅觉感器的分子成分，并揭示了辅助细胞而非仅仅ORN在编码一种对许多人类疾病昆虫传播媒介至关重要的宿主线索气味中发挥着重要作用。
