A dorsal/ventral boundary established by Notch controls growth and polarity in the Drosophila eye

Abstract

In the Drosophila compound eye the dorsal and ventral fields of eye units (ommatidia) meet along the dorsoventral midline, forming a line of mirror image symmetry called the equator. The molecular mechanism establishing the equator is not fully understood, but it involves the transcription factors encoded by the Iroquois gene complex. The Iroquois genes are expressed in the dorsal half of the eye and here we show that they regulate the expression of the secreted molecule Fringe. A boundary between fringe-expressing and fringe-non-expressing cells is essential, from the time of the second larval instar, for eye growth and formation of the equator. Boundaries of fringe expression determine where the transmembrane receptor Notch is activated. We find that Notch is activated at the dorsoventral midline, where it is required to promote growth and set up the axis of mirror symmetry. As boundaries of fringe expression and Notch activation are also important during Drosophila wing formation and vertebrate somitogenesis, we suggest that these boundaries constitute a general mechanism that directs growth and patterning of large fields of cells.

Growth and specification of the eye are controlled independently by Eyegone and Eyeless in Drosophila melanogaster

“…Consistent with this model, several Notch target genes, including four jointed (ref. 25) and Enhancer of split-mβ (E(spl)-mβ) 24 , are expressed prominently on both sides of the dorsal-ventral boundary (see also Fig. 1c).…”

“…1b) 3,21,24 . The localized activation of Notch receptor on both sides of the compartment boundary is believed to establish the dorsal-ventral organizer that controls growth of the entire eye primordium [23][24][25] . Consistent with this model, several Notch target genes, including four jointed (ref.…”

“…First, the growth of the eye primordium (called the eye disc) depends on an evolutionarily conserved organizer (Fig. 1b) 3,[21][22][23][24][25] . Second, the D. melanogaster genome has both classes of Pax transcription factors, but unlike mammalian genomes, these proteins are encoded by separate genes, enabling us to inactivate or activate each class individually.…”

Wingless Signaling in Drosophila Eye Development

“…The Iro-C proteins repress the expression of fringe (fng), which encodes a glycosyltransferase that modulates the affinity of the Notch receptor for its ligands Delta (Dl) and Serrate (Ser) (46)(47)(48). The Fng expression border, in combination with the restriction of Ser to the ventral compartment and Dl to the dorsal compartment, results in activation of Notch precisely at the dorsal/ventral boundary of the disc, known as the equator (46)(47)(48) (Fig.…”

“…Final eye size must depend on the interplay between Wg and other growth regulators such as Dpp, Notch and its target Upd (6,(46)(47)(48)(54)(55)(56). Expression of Wg or activated Arm throughout the eye disc reduces eye size in addition to blocking differentiation (31,34,49), probably due to its effects on these other factors.…”