Extramacrochaetae functions in dorsal-ventral patterning ofDrosophilaimaginal discs

Abstract

One of the seminal events in the history of a tissue is the establishment of the anterior-posterior, dorsal-ventral (D/V) and proximal-distal axes. Axis formation is important for the regional specification of a tissue and allows cells along the different axes to obtain directional and positional information. Within the Drosophila retina, D/V axis formation is essential to ensure that each unit eye first adopts the proper chiral form and then rotates precisely 90°in the correct direction. These two steps are important because the photoreceptor array must be correctly aligned with the neurons of the optic lobe. Defects in chirality and/or ommatidial rotation will lead to disorganization of the photoreceptor array, misalignment of retinal and optic lobe neurons, and loss of visual acuity. Loss of the helixloop-helix protein Extramacrochaetae (Emc) leads to defects in both ommatidial chirality and rotation. Here, we describe a new role for emc in eye development in patterning the D/V axis. We show that the juxtaposition of dorsal and ventral fated tissue in the eye leads to an enrichment of emc expression at the D/V midline. emc expression at the midline can be eliminated when D/V patterning is disrupted and can be induced in situations in which ectopic boundaries are artificially generated. We also show that emc functions downstream of Notch signaling to maintain the expression of four-jointed along the midline.

Inhibition of Daughterless by Extramacrochaetae mediates Notch-induced cell proliferation

“…We have demonstrated here that Notch signaling can activate emc expression in proliferating cells ahead of the morphogenetic furrow ( Fig. 2A-C; Spratford and Kumar, 2015). These results are similar to those obtained by others in the wing and in developing photoreceptor neurons.…”

“…In several contexts, emc appears to function downstream of the Notch pathway (Baonza et al, 2000;Baonza and Freeman, 2001;Adam and Montell, 2004;Tapanes-Castillo and Baylies, 2004;Bhattacharya and Baker, 2009;Spratford and Kumar, 2015). Here, we show that the Notch pathway activates emc expression.…”

“…In this manuscript, we have attempted to bring several observations together and demonstrate that Emc mediates some of the Notchmediated growth in the developing eye by sequestering the type I bHLH protein Da. Several previous findings are crucial for this study: first, in several developmental contexts, emc appears to lie downstream of the Notch signaling pathway (de Celis et al, 1995;Baonza and García-Bellido, 1999;Baonza et al, 2000;Adam and Montell, 2004;Bhattacharya and Baker, 2009;Spratford and Kumar, 2015). This is an important observation as Notch signaling is a key promoter of growth in the eye (Cho and Choi, 1998;de Celis et al, 1998;Domínguez and de Celis, 1998;Go et al, 1998;Papayannopoulos et al, 1998;Kenyon et al, 2003;Chao et al, 2004;Dominguez et al, 2004;Baonza and Freeman, 2005;Firth and Baker, 2005;Reynolds-Kenneally and Mlodzik, 2005).…”

“…We focused on a potential connection between Notch signaling and Emc as several studies have demonstrated that Emc functions downstream of the Notch pathway in the wing and eye discs, embryonic mesodermal segments, and ovarian follicle cells (Baonza et al, 2000;Adam and Montell, 2004;Tapanes-Castillo and Baylies, 2004;Bhattacharya and Baker, 2009;Spratford and Kumar, 2015). In fact, emc expression appears to be dependent upon Notch pathway activity in several different contexts (Baonza et al, 2000;Baonza and Freeman, 2001;Bhattacharya and Baker, 2009;Spratford and Kumar, 2015).…”

“…In fact, emc expression appears to be dependent upon Notch pathway activity in several different contexts (Baonza et al, 2000;Baonza and Freeman, 2001;Bhattacharya and Baker, 2009;Spratford and Kumar, 2015). Activation of an emc transcriptional reporter (emc-lacZ) by overexpression of an activated Notch receptor (N ICD ) in the eye ( Fig.…”