DoOR 2.0 - Comprehensive Mapping of Drosophila melanogaster Odorant Responses

Odors elicit complex patterns of activated olfactory sensory neurons. Knowing the complete olfactome, i.e. the responses in all sensory neurons for all relevant odorants, is desirable to understand olfactory coding. The DoOR project combines all available Drosophila odorant response data into a single consensus response matrix. Since its first release many studies were published: receptors were deorphanized and several response profiles were expanded. In this study, we add unpublished data to the odor-response profiles for four odorant receptors (Or10a, Or42b, Or47b, Or56a). We deorphanize Or69a, showing a broad response spectrum with the best ligands including 3-hydroxyhexanoate, alpha-terpineol, 3-octanol and linalool. We include all of these datasets into DoOR, provide a comprehensive update of both code and data, and new tools for data analyses and visualizations. The DoOR project has a web interface for quick queries (http://neuro.uni.kn/DoOR), and a downloadable, open source toolbox written in R, including all processed and original datasets. DoOR now gives reliable odorant-responses for nearly all Drosophila olfactory responding units, listing 693 odorants, for a total of 7381 data points.

[1]  C Giovanni Galizia,et al.  The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). , 2006, Journal of neurobiology.

[2]  John R. Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Larva , 2005, Neuron.

[3]  Daniela Pelz.  Functional characterization of Drosophila melanogaster Olfactory Receptor Neurons , 2005 .

[4]  John R. Carlson,et al.  The molecular basis of CO2 reception in Drosophila , 2007, Proceedings of the National Academy of Sciences.

[5]  Olfactory Proxy Detection of Dietary Antioxidants in Drosophila , 2015, Current Biology.

[6]  M. Nei,et al.  Extensive Gains and Losses of Olfactory Receptor Genes in Mammalian Evolution , 2007, PloS one.

[7]  Flavio Roces,et al.  The Antennal Lobes of Fungus-Growing Ants (Attini): Neuroanatomical Traits and Evolutionary Trends , 2009, Brain, Behavior and Evolution.

[8]  J. Carlson,et al.  Similar Odorants Elicit Different Behavioral and Physiological Responses, Some Supersustained , 2011, The Journal of Neuroscience.

[9]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[10]  Richard D. Newcomb,et al.  Insect olfaction and the evolution of receptor tuning , 2015, Front. Ecol. Evol..

[11]  John R Carlson,et al.  The Molecular Basis of Odor Coding in the Drosophila Antenna , 2004, Cell.

[12]  Markus Knaden,et al.  Pheromones mediating copulation and attraction in Drosophila , 2015, Proceedings of the National Academy of Sciences.

[13]  Markus Meister,et al.  Can Humans Really Discriminate 1 Trillion Odors? , 2014, 1411.0165.

[14]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[15]  John G Hildebrand,et al.  Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet , 2015, Proceedings of the National Academy of Sciences.

[16]  John R Carlson,et al.  Chemosensory Coding by Neurons in the Coeloconic Sensilla of the Drosophila Antenna , 2005, The Journal of Neuroscience.

[17]  Fredrik Schlyter,et al.  What reaches the antenna? How to calibrate odor flux and ligand-receptor affinities. , 2012, Chemical senses.

[18]  Stephen R. Heller,et al.  InChI - the worldwide chemical structure identifier standard , 2013, Journal of Cheminformatics.

[19]  G. Shepherd,et al.  Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. , 1997, Annual review of neuroscience.

[20]  C Giovanni Galizia,et al.  Olfactory coding in the insect brain: data and conjectures , 2014, The European journal of neuroscience.

[21]  John R. Carlson,et al.  Coexpression of Two Functional Odor Receptors in One Neuron , 2005, Neuron.

[22]  Anandasankar Ray,et al.  Modification of CO2 avoidance behaviour in Drosophila by inhibitory odorants , 2009, Nature.

[23]  B. Alman,et al.  Mutant IDH is sufficient to initiate enchondromatosis in mice , 2015, Proceedings of the National Academy of Sciences.

[24]  Silke Sachse,et al.  Physicochemical vs. Vibrational Descriptors for Prediction of Odor Receptor Responses , 2013, Molecular informatics.

[25]  Barry J. Dickson,et al.  Molecular, Anatomical, and Functional Organization of the Drosophila Olfactory System , 2005, Current Biology.

[26]  Elisabetta Chicca,et al.  Exploring olfactory sensory networks: Simulations and hardware emulation , 2010, 2010 Biomedical Circuits and Systems Conference (BioCAS).

[27]  L. Buck,et al.  Olfactory receptors are sensitive to molecular volume of odorants , 2015 .

[28]  Bill S Hansson,et al.  Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster , 2015, The Journal of comparative neurology.

[29]  S. Sachse,et al.  The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code , 1999, The European journal of neuroscience.

[30]  Pavan Ramdya,et al.  Complementary Function and Integrated Wiring of the Evolutionarily Distinct Drosophila Olfactory Subsystems , 2011, The Journal of Neuroscience.

[31]  D. Tolhurst,et al.  Characterizing the sparseness of neural codes , 2001, Network.

[32]  Thomas A Neubert,et al.  Ionotropic Glutamate Receptors IR64a and IR8a Form a Functional Odorant Receptor Complex In Vivo in Drosophila , 2013, The Journal of Neuroscience.

[33]  Richard C Gerkin,et al.  The number of olfactory stimuli that humans can discriminate is still unknown , 2015, eLife.

[34]  Markus Knaden,et al.  A Conserved Dedicated Olfactory Circuit for Detecting Harmful Microbes in Drosophila , 2012, Cell.

[35]  Gisbert Schneider,et al.  Predicting olfactory receptor neuron responses from odorant structure , 2007, Chemistry Central journal.

[36]  John R. Carlson,et al.  Coding of Odors by a Receptor Repertoire , 2006, Cell.

[37]  Pedro A. F. Galante,et al.  Identification of agonists for a group of human odorant receptors , 2015, Front. Pharmacol..

[38]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[39]  Peter J. Clyne,et al.  Odor Coding in a Model Olfactory Organ: TheDrosophila Maxillary Palp , 1999, The Journal of Neuroscience.

[40]  J. Hildebrand,et al.  Insect Olfaction , 1999, Springer Berlin Heidelberg.

[41]  C. Giovanni Galizia,et al.  Optical methods for analyzing odor-evoked activity in the insect brain , 2004 .

[42]  David J. Anderson,et al.  A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila , 2004, Nature.

[43]  John R. Carlson,et al.  Translation of Sensory Input into Behavioral Output via an Olfactory System , 2008, Neuron.

[44]  C. Giovanni Galizia,et al.  Olfactory Sensor Processing in Neural Networks: Lessons from Modeling the Fruit Fly Antennal Lobe , 2011, Front. Neuroeng..

[45]  Daniel Flanagan,et al.  An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae) , 1989 .

[46]  Richard Axel,et al.  Topographic organization of sensory projections to the olfactory bulb , 1994, Cell.

[47]  John R. Carlson,et al.  Odor Coding in the Drosophila Antenna , 2001, Neuron.

[48]  Silke Sachse,et al.  Olfactory Preference for Egg Laying on Citrus Substrates in Drosophila , 2013, Current Biology.

[49]  Leslie B. Vosshall,et al.  Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila , 2009, Cell.

[50]  R. Benton,et al.  Acid sensing by the Drosophila olfactory system , 2010, Nature.

[51]  Leslie B. Vosshall,et al.  Genetic and Functional Subdivision of the Drosophila Antennal Lobe , 2005, Current Biology.

[52]  John R. Carlson,et al.  Receptors and Neurons for Fly Odors in Drosophila , 2007, Current Biology.

[53]  Bill S Hansson,et al.  Novel natural ligands for Drosophila olfactory receptor neurones , 2003, Journal of Experimental Biology.

[54]  H. Eisthen.  Why Are Olfactory Systems of Different Animals So Similar? , 2002, Brain, Behavior and Evolution.

[55]  Linda B. Buck,et al.  Information coding in the olfactory system: Evidence for a stereotyped and highly organized epitope map in the olfactory bulb , 1994, Cell.

[56]  M. Knaden,et al.  Functional loss of yeast detectors parallels transition to herbivory (commentary) , 2015 .

[57]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[58]  Roberto Paolesse,et al.  More than apples and oranges - Detecting cancer with a fruit fly's antenna , 2014, Scientific Reports.

[59]  A. Keller,et al.  Humans Can Discriminate More than 1 Trillion Olfactory Stimuli , 2014, Science.

[60]  Martin Strauch,et al.  Integrating Heterogeneous Odor Response Data into a Common Response Model: A DoOR to the Complete Olfactome , 2010, Chemical senses.

[61]  Joel D Mainland,et al.  Human olfactory receptor responses to odorants , 2015, Scientific Data.

[62]  Coral G. Warr,et al.  Detection of Volatile Indicators of Illicit Substances by the Olfactory Receptors of Drosophila melanogaster , 2010, Chemical senses.

[63]  Valerio Mazzoni,et al.  Olfactory responses of Drosophila suzukii females to host plant volatiles , 2015 .

[64]  M. Ohkura,et al.  A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein , 2001, Nature Biotechnology.

[65]  Shawn R. Olsen,et al.  Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations , 2007, Nature Neuroscience.

[66]  C. Warr,et al.  Functional and molecular evolution of olfactory neurons and receptors for aliphatic esters across the Drosophila genus , 2010, Journal of Comparative Physiology A.

[67]  Christopher J. Potter,et al.  Farnesol-Detecting Olfactory Neurons in Drosophila , 2014, The Journal of Neuroscience.

[68]  John R. Carlson,et al.  Integrating the Molecular and Cellular Basis of Odor Coding in the Drosophila Antenna , 2003, Neuron.