The formation of epithelial lumina is a fundamental process in animal development. Each ommatidium of the Drosophila retina forms an epithelial lumen, the interrhabdomeral space, which has a critical function in vision as it optically isolates individual photoreceptor cells. Ommatidia containing an interrhabdomeral space have evolved from ancestral insect eyes that lack this lumen, as seen, for example, in bees. In a genetic screen, we identified eyes shut (eys) as a gene that is essential for the formation of matrix-filled interrhabdomeral space. Eys is closely related to the proteoglycans agrin and perlecan and secreted by photoreceptor cells into the interrhabdomeral space. The honeybee ortholog of eys is not expressed in photoreceptors, raising the possibility that recruitment of eys expression has made an important contribution to insect eye evolution. Our findings show that the secretion of a proteoglycan into the apical matrix is critical for the formation of epithelial lumina in the fly retina.
Bibliographical noteFunding Information:
We thank Seymour Benzer, Don Ready, Sabrina Kim, Gabrielle Boulianne, Horst Goelder, Ellen Larsen, the Developmental Studies Hybridoma Bank, the Bloomington Drosophila Stock Center, and the Drosophila Genomic Resource Center for fly stocks, bees, and reagents. We thank Dorothea Godt for discussion and critical comments on the manuscript and Andrew Zelhof for discussing data prior to publication. This work was supported by a predoctoral fellowship of the Vision Research Program, University of Toronto (N.H.), and grants from the National Institutes of Health, USA (R01, EY015231-01A1; T.R.C.) and the National Science and Engineering Research Council, Canada (U.T.).
All Science Journal Classification (ASJC) codes
- Molecular Biology
- Biochemistry, Genetics and Molecular Biology(all)
- Developmental Biology
- Cell Biology