Hybrid Neurons in a MicroRNA Mutant Are Putative Evolutionary Intermediates in Insect CO2 Sensory Systems
Pelin Cayirlioglu,1*
Ilona Grunwald Kadow,1*
Xiaoli Zhan,1
Katsutomo Okamura,2
Greg S. B. Suh,3
Dorian Gunning,1
Eric C. Lai,2
S. Lawrence Zipursky1
Carbon dioxide (CO2) elicits different olfactory behaviors across species. In Drosophila, neurons that detect CO2 are located in the antenna, form connections in a ventral glomerulus in the antennal lobe, and mediate avoidance. By contrast, in the mosquito these neurons are in the maxillary palps (MPs), connect to medial sites, and promote attraction. We found in Drosophila that loss of a microRNA, miR-279, leads to formation of CO2 neurons in the MPs. miR-279 acts through down-regulation of the transcription factor Nerfin-1. The ectopic neurons are hybrid cells. They express CO2 receptors and form connections characteristic of CO2 neurons, while exhibiting wiring and receptor characteristics of MP olfactory receptor neurons (ORNs). We propose that this hybrid ORN reveals a cellular intermediate in the evolution of species-specific behaviors elicited by CO2.
1 Department of Biological Chemistry, Howard Hughes Medical Institute, David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA.
2 Sloan-Kettering Institute, 521 Rockefeller Research Labs, 1275 York Avenue, Box 252, New York, NY 10021, USA.
3 Division of Biology 216-76, California Institute of Technology, Pasadena, CA 91125, USA.
* These authors contributed equally to this work.
Present address: Department of Molecular Neurobiology, Max Planck Institute of Neurobiology, Am Klopferspitz 18, 82152 Martinsried, Germany.
Present address: Molecular Neurobiology Program, Skirball Institute, Department of Cell Biology, New York University School of Medicine, New York, NY 10016, USA.
To whom correspondence should be addressed. E-mail: lzipursky{at}mednet.ucla.edu