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Transforming the architecture of compound eyes

Nature volume 443, pages 696–699 (2006)Cite this article

Abstract

Eyes differ markedly in the animal kingdom, and are an extreme example of the evolution of multiple anatomical solutions to light detection and image formation. A salient feature of all photoreceptor cells is the presence of a specialized compartment (disc outer segments in vertebrates, and microvillar rhabdomeres in insects), whose primary role is to accommodate the millions of light receptor molecules required for efficient photon collection. In insects, compound eyes can have very different inner architectures1,2,3. Fruitflies and houseflies have an open rhabdom system, in which the seven rhabdomeres of each ommatidium are separated from each other and function as independent light guides. In contrast, bees and various mosquitoes and beetle species have a closed system, in which rhabdomeres within each ommatidium are fused to each other, thus sharing the same visual axis. To understand the transition between open and closed rhabdom systems, we isolated and characterized the role of Drosophila genes involved in rhabdomere assembly. Here we show that Spacemaker, a secreted protein expressed only in the eyes of insects with open rhabdom systems, acts together with Prominin and the cell adhesion molecule Chaoptin to choreograph the partitioning of rhabdomeres into an open system. Furthermore, the complete loss of spacemaker (spam) converts an open rhabdom system to a closed one, whereas its targeted expression to photoreceptors of a closed system markedly reorganizes the architecture of the compound eyes to resemble an open system. Our results provide a molecular atlas for the construction of microvillar assemblies and illustrate the critical effect of differences in a single structural protein in morphogenesis.

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Figure 1: spam and prom mutants have severe defects in IRS formation.
Figure 2: Prom and Spam cooperate to antagonize the adhesive force of Chaoptin.
Figure 3: spam is expressed only in insect eyes with an open rhabdomere system.
Figure 4: Expression of Spam induces the formation of an IRS.

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Acknowledgements

We thank T. Meerloo for help with cryosections; D. Cowan for help with P-element injections; Glenn Apiaries, L. McCuiston, R. Denell, S. Brown, T. Shippy, M. Lorenzen, P. Atkinson and A. James for providing various insect species; and W. McGinnis, N. Ryba, S. L. Zipursky, K. Kirschfeld and members of the Zuker laboratory for comments. This work was supported in part by a grant from the National Eye Institute. C.S.Z. is an investigator of the Howard Hughes Medical Institute.

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  1. Howard Hughes Medical Institute and Departments of Neurobiology and Neurosciences, University of California at San Diego, La Jolla, California, 92093-0649, USA

    Andrew C. Zelhof, Robert W. Hardy, Ann Becker & Charles S. Zuker

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  1. Andrew C. Zelhof
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  2. Robert W. Hardy
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Correspondence to Andrew C. Zelhof or Charles S. Zuker.

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Competing interests

The cDNA sequences for spacemaker and prominin are deposited in GenBank under accession numbers DQ780942 and DQ780943, respectively. Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

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Zelhof, A., Hardy, R., Becker, A. et al. Transforming the architecture of compound eyes. Nature 443, 696–699 (2006). https://doi.org/10.1038/nature05128

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