Coordinating Proliferation and Tissue Specification to Promote Regional Identity in the Drosophila Head

Abstract

The Decapentaplegic and Notch signaling pathways are thought to direct regional specification in the Drosophila eye-antennal epithelium by controlling the expression of selector genes for the eye (Eyeless/Pax6, Eyes absent) and/or antenna (Distal-less). Here, we investigate the function of these signaling pathways in this process. We find that organ primordia formation is indeed controlled at the level of Decapentaplegic expression but critical steps in regional specification occur earlier than previously proposed. Contrary to previous findings, Notch does not specify eye field identity by promoting Eyeless expression but it influences eye primordium formation through its control of proliferation. Our analysis of Notch function reveals an important connection between proliferation, field size, and regional specification. We propose that field size modulates the interaction between the Decapentaplegic and Wingless pathways, thereby linking proliferation and patterning in eye primordium development.

The Basic Helix-Loop-Helix Leucine Zipper Transcription Factor Mitf Is Conserved in Drosophila and Functions in Eye Development

“…Although the Drosophila mouse Mitf genes than between Dmel/Mitf and any of the three Tfe genes (arrows in Figure 1B thia roretzi is expressed in pigment lineage blastomeres, it does not appear to contain sequences that resemble The Drosophila Mitf protein is considerably larger than its vertebrate counterpart. In addition to the highly exon 1M (Yajima et al 2003). Interestingly, the ascidian Mitf gene is expressed maternally, like its Drosophila conserved bHLH-Zip domains, several other conserved regions were identified, suggesting that they represent counterpart.…”

“…The ey-Gal4 (Hazelet between fly and vertebrates. We discuss below the impliet al 1998; Kenyon et al 2003) driver expresses throughcations of this conservation at the molecular and develout the disc proper and peripodial cell layers until mid opmental levels. L2.…”

Wingless Signaling in Drosophila Eye Development

“…The two Pax6 homologues toy and ey act at the top of the cascade, with toy upstream of ey; both are necessary and sufficient for eye development but are also required for formation of the entire head, reflecting their early expression in the antennal disc (2,3,17,18). Subdivision of the disc into separate eye and antennal primordia is first apparent in the early second instar, when Eyes absent (Eya), a target of Ey, is specifically expressed at the posterior margin of the eye disc in response to signaling by the secreted molecules Hedgehog (Hh) and Decapentaplegic (Dpp) (5,18,19). Ey also activates the expression of Sine oculis (So), a homeodomain protein that interacts with Eya and acts in conjunction with it to promote eye specification (18,20,21).…”

“…Wg protein is present throughout the entire second instar eye disc, where it blocks the induction of Eya expression by Dpp until disc growth brings posterior cells out of the range of Wg diffusion (5,30,32). Consistent with this model, the lack of eye development in mutants for eyegone, a target of Notch signaling that is required for disc growth (33), can be rescued by inhibiting Wg signaling in posterior cells (34).…”

“…The disc invaginates from the embryonic ectoderm and grows by asynchronous cell divisions until the third larval instar (1,4). The columnar epithelium of the disc is partitioned into separate eye and antennal primordia in the second larval instar (5). The squamous peripodial epithelium gives rise to head structures and may also communicate with the columnar epithelium (6,7).…”