Same Switches Program Taste and Smell in Fruit Flies

Findings help explain how complex nervous systems arise from few genes.

A new study sheds light on how fruit flies get their keen sense of smell.

Duke University biologist Pelin Volkan and colleagues have identified a set of genetic control switches that interact early in a fly’s development to generate dozens of types of olfactory neurons, specialized nerve cells for smell.

The same gene network also plays a role in programming the fly neurons responsible for taste, the researchers report in the journal PLOS Genetics.

The findings do more than merely explain how a household pest distinguishes rotting vegetables from ripening fruit, the authors say. The research could be a key to understanding how the nervous systems of other animals — including humans, whose brains have billions of neurons — produce such a dazzling array of cell types from a modest number of genes.

Fruit flies rely on their keen sense of smell to tell the difference between good food and bad, safety and danger, potential mates and those off-limits. The tiny insects perceive this wide range of chemical cues through a diverse set of olfactory sensory neurons along their antennae. More than 2000 such neurons are organized into 50 types, each of which transmits information to a specific region of the fly’s poppy seed-sized brain.

“Each neuron type detects a very specific range of odors,” Volkan said. Certain odors from fermenting fruit, for example, activate one class of neurons, and carbon dioxide activates another.

Volkan is interested in how the many types of smell neurons come to be as a fruit fly develops from egg to an adult.

Smell neurons begin as identical precursor cells, immature cells that have not yet “decided” which type of nerve cell they will become. All precursor cells have the same DNA, and how they produce one neuron type versus another was unknown.

One way to get many types of cells or proteins from the same genetic starting material is by mixing and matching different parts of one gene to produce multiple gene readouts, a phenomenon known as alternative splicing. The team’s results point to another strategy, however: using the same genes in different combinations, or “combinatorial coding.”

By tweaking different fly genes and counting how many neuron types were produced as the flies matured, the team identified a network of five genes that work together like coordinated control switches to guide the precursor cells’ transformation to mature neurons. The genes regulate each other’s activity, interacting in unique combinations to set each precursor cell on a distinct path by turning on different olfactory receptors in each cell.

Image shows concentric rings in a fruit fly larva’s antenna.

The researchers found that manipulating the network had similar effects in the legs, which flies use not only to walk but also to taste. “The same basic toolkit gives rise to diverse types of neurons in completely different tissues,” said Volkan, who is also a member of the Duke Institute for Brain Sciences.

Several of the network genes Volkan and her team identified have counterparts in humans and other vertebrates, which suggests the same basic mechanism could be at work in building the nervous system in other animals too.

ABOUT THIS NEUROSCIENCE RESEARCH

Authors include Qingyun Li, Scott Barish, Sumie Okuwa and Abigail Maciejewski of Duke, Alicia Brandt and Corbin Jones of University of North Carolina-Chapel Hill and Dominik Reinhold of Clark University.

Funding: This research was supported by the National Science Foundation (1457690).

Source: Robin Ann Smith – Duke University
Image Source: The image is credited to Tristan Qingyun Li, Duke University.
Original Research: Full open access research for “A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity” by Qingyun Li, Scott Barish, Sumie Okuwa, Abigail Maciejewski, Alicia T. Brandt, Dominik Reinhold, Corbin D. Jones, and Pelin Cayirlioglu Volkan in PLOS Genetics. Published online January 14 2016 doi:10.1371/journal.pgen.1005780


Abstract

A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity

Sensory neuron diversity is required for organisms to decipher complex environmental cues. In Drosophila, the olfactory environment is detected by 50 different olfactory receptor neuron (ORN) classes that are clustered in combinations within distinct sensilla subtypes. Each sensilla subtype houses stereotypically clustered 1–4 ORN identities that arise through asymmetric divisions from a single multipotent sensory organ precursor (SOP). How each class of SOPs acquires a unique differentiation potential that accounts for ORN diversity is unknown. Previously, we reported a critical component of SOP diversification program, Rotund (Rn), increases ORN diversity by generating novel developmental trajectories from existing precursors within each independent sensilla type lineages. Here, we show that Rn, along with BarH1/H2 (Bar), Bric-à-brac (Bab), Apterous (Ap) and Dachshund (Dac), constitutes a transcription factor (TF) network that patterns the developing olfactory tissue. This network was previously shown to pattern the segmentation of the leg, which suggests that this network is functionally conserved. In antennal imaginal discs, precursors with diverse ORN differentiation potentials are selected from concentric rings defined by unique combinations of these TFs along the proximodistal axis of the developing antennal disc. The combinatorial code that demarcates each precursor field is set up by cross-regulatory interactions among different factors within the network. Modifications of this network lead to predictable changes in the diversity of sensilla subtypes and ORN pools. In light of our data, we propose a molecular map that defines each unique SOP fate. Our results highlight the importance of the early prepatterning gene regulatory network as a modulator of SOP and terminally differentiated ORN diversity. Finally, our model illustrates how conserved developmental strategies are used to generate neuronal diversity.

“A Functionally Conserved Gene Regulatory Network Module Governing Olfactory Neuron Diversity” by Qingyun Li, Scott Barish, Sumie Okuwa, Abigail Maciejewski, Alicia T. Brandt, Dominik Reinhold, Corbin D. Jones, and Pelin Cayirlioglu Volkan in PLOS Genetics. Published online January 14 2016 doi:10.1371/journal.pgen.1005780

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