Academic journal article Genetics

Regulation of Odor Receptor Genes in Trichoid Sensilla of the Drosophila Antenna

Academic journal article Genetics

Regulation of Odor Receptor Genes in Trichoid Sensilla of the Drosophila Antenna

Article excerpt

ABSTRACT

This study concerns the problem of odor receptor gene choice in the fruit fly Drosophila melanogaster. From a family of 60 Odor receptor genes, only one or a small number are selected for expression by each olfactory receptor neuron. Little is known about how an olfactory receptor neuron selects a receptor, or how the nucleotide sequences flanking a receptor gene dictate its expression in a particular neuron. Previous investigation has primarily concerned the maxillary palp, the simpler of the fly's two olfactory organs. Here we focus on genes encoding four antennal receptors that respond to fly odors in an in vivo expression system. To investigate the logic of odor receptor expression, we carry out a genetic analysis of their upstream regulatory sequences. Deletion analysis reveals that relatively short regulatory regions are sufficient to confer expression in the appropriate neurons, with limited if any misexpression. We find evidence for both positive and negative regulation. Multiple repressive functions restrict expression to the antenna, to a region of the antenna, and to neurons. Through deletion and base substitution mutagenesis we identify GCAATTA elements and find evidence that they act in both positive and negative regulation.

OLFACTORY systems of insects and vertebrates contain many odor receptors and many olfactory receptor neurons (ORNs), yet each ORN expresses only one or a small number of receptors (Mombaerts 2004; Fuss and Ray 2009). A critical problem in this system is the mechanism of receptor gene choice. What factors conspire to express one particular receptor in a particular ORN? Conversely, what factors prevent all the other receptors from being expressed in that ORN? This problem is especially challenging because in many organisms, including Drosophila, the expression of individual receptors is subject to a spatial constraint: each receptor is expressed only in a subset of ORNs that lie in a particular subdomain of the olfactory field.

The olfactory system of the fruit fly contains two organs, the third segment of the antenna, referred to henceforth for simplicity as ''the antenna,'' and the maxillary palp (Figure 1A). Each organ is covered with sensilla, 400 in the case of the antenna, and 60 in the maxillary palp (Shanbhag et al. 2001). Each sensillumis innervated by up to four ORNs. There are three major morphological types of antennal sensilla: trichoid, basiconic, and coeloconic sensilla. Trichoid sensilla are distributed predominantly in the distolateral region (Figure 1, B and C), basiconic sensilla are most highly concentrated in the proximomedial region of the antenna, and coeloconic sensilla are spread broadly on the antennal surface as well as in a sensory pit known as the sacculus. All of the olfactory sensilla on the maxillary palp are of the basiconic type.

Trichoid sensilla, examined in this study, have been implicated in the response to fly odors (Clyne et al. 1997; Ejima et al. 2007; Kurtovic et al. 2007; van der Goes van Naters and Carlson 2007; Datta et al. 2008), whereas ORNs of basiconic sensilla respond strongly to fruit odors (de Bruyne et al. 2001; Hallem et al. 2004; Hallem and Carlson 2006). Trichoid sensilla fall into four subtypes, designated at1, at2, at3, and at4 (Shanbhag et al. 1999; Couto et al. 2005; Fishilevich and Vosshall 2005). The at1 sensilla are most highly concentrated in the proximomedial portion of the trichoid zone, while the at4 sensilla are more densely distributed in the distolateral portion. Each at1 sensillum is innervated by a single ORN; an at2 sensillum contains two ORNs; and at3 and at4 sensilla each contain three ORNs. Among the 60 Or (Odor receptor) genes of Drosophila melanogaster (Clyne et al. 1999b; Gao and Chess 1999; Vosshall et al. 1999), 12 map to individual ORNs in trichoid sensilla (Couto et al. 2005; Fishilevich and Vosshall 2005). Of these 12, 4 were found to respond to fly odors in an in vivo expression system, the ''empty neuron'' system(Dobritsa et al. …

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