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Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages

Nature Neuroscience volume 10, pages 153–160 (2007)Cite this article

Abstract

An essential feature of the organization and function of the vertebrate and insect olfactory systems is the generation of a variety of olfactory receptor neurons (ORNs) that have different specificities in regard to both odorant receptor expression and axonal targeting. Yet the underlying mechanisms that generate this neuronal diversity remain elusive. Here we demonstrate that the Notch signal is involved in the diversification of ORNs in Drosophila melanogaster. A systematic clonal analysis showed that a cluster of ORNs housed in each sensillum were differentiated into two classes, depending on the level of Notch activity in their sibling precursors. Notably, ORNs of different classes segregated their axonal projections into distinct domains in the antennal lobes. In addition, both the odorant receptor expression and the axonal targeting of ORNs were specified according to their Notch-mediated identities. Thus, Notch signaling contributes to the diversification of ORNs, thereby regulating multiple developmental events that establish the olfactory map in Drosophila.

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Figure 1: Reciprocal phenotypes of axonal projections in mam and nb clones.
Figure 2: Combinatorial axonal projections from the Notch-ON– and Notch-OFF–class ORNs.
Figure 3: List of glomeruli receiving axonal projections from Notch-ON– and Notch-OFF–class ORNs.
Figure 4: Clustered distributions of the Notch-ON and Notch-OFF glomeruli.
Figure 5: Notch-mediated cell differentiation in the olfactory sensory lineage.
Figure 6: Notch signaling controls the selection of odorant receptor type and target glomerulus.

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Acknowledgements

We thank E. Buchner, A. Hofbauer, H. Bellen, F. Matsuzaki, Y. Hiromi and Y.-N. Jan for antibodies and L. Luo, L. Vosshall, K. Matsuno, the Bloomington stock center and the Drosophila Genetic Resource Center, Kyoto Institute of Technology, for fly stocks. We are grateful to K. Ito for the use of his laboratory's facility and also to all members of the Hama laboratory and Center for Developmental Biology for helpful discussion. This work was partly supported by a grant-in-aid for Scientific Research on Priority Areas, Advanced Brain Science Project, from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Authors and Affiliations

  1. Laboratory for Neural Network Development, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-minami, Chuo, Kobe, 650-0047, Hyogo, Japan

    Keita Endo, Tomoko Aoki, Yuka Yoda & Chihiro Hama

  2. Institute of Molecular and Cellular Biosciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, 113-0032, Tokyo, Japan

    Keita Endo

  3. Institute for Bioinformatics Research and Development, Japan Science and Technology Agency, 5-3, Yonbancho, Chiyoda-ku, 102-8666, Tokyo, Japan

    Keita Endo

  4. Hokkaido University of Education, Iwamizawa Campus, Iwamizawa, 068-8642, Hokkaido, Japan

    Ken-ichi Kimura

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Contributions

K.E. designed and performed most of the experiments in this study. T.A. and Y.Y. assisted in the experiments. K.-i.K. identified a fly line AM29, which drives reporter gene expression in ORNs projecting to two glomeruli. K.E. and C.H. contributed to the writing of this paper.

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Correspondence to Chihiro Hama.

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Endo, K., Aoki, T., Yoda, Y. et al. Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat Neurosci 10, 153–160 (2007). https://doi.org/10.1038/nn1832

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