Spatially localized rhomboid is required for establishment of the dorsal-ventral axis in Drosophila oogenesis

Abstract

The establishment of dorsal-ventral asymmetry of the Drosophila embryo requires a group of genes that act maternally. None of the previously identified dorsal-ventral axis genes are known to produce asymmetrically localized gene products during oogenesis. We show that rhomboid (rho), a novel member of this group, encodes a protein that is localized on the apical surface of the dorsal-anterior follicle cells surrounding the oocyte. Loss of rho function causes ventralization of the eggshell and the embryo, whereas ectopic expression leads to dorsalization of both structures. Thus, spatially restricted rho is necessary and sufficient for dorsal-ventral axis formation. We propose, based on these observations and double mutant experiments, that the spatially restricted rho protein leads to selective activation of the epidermal growth factor receptor in the dorsal follicle cells and subsequently the specification of the dorsal follicle cells.

orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis.

“…3). Similar eggshell defects have been described for grk, top/DER, cni, rho, and brn mutations, which block dorsal follicle cell fate determination and produce eggshells referred to as ventralized (Schiipbach 1987;Ashburner et al 1990;Goode et al 1992;Ruohola-Baker et al 1993). As shown in Table 2, 23% of the eggs produced by orh""^^Iorh""^^ females displayed fused dorsal appendages and 6% lacked both dorsal appendages.…”

“…Since this phenotype suggests that too many follicle cells receive a dorsalizing signal, these genes may act to restrict the expression of the signal temporally and/or spatially. The opposite phenotype is produced by gurken {grk), torpedo [top/DER], coinichon [cni], rhomboid (rho), and brainiac [brn] mutations, which cause cells that normally develop as dorsal to adopt a ventral fate on the eggshell (Schiipbach 1987;Ashbumer et al 1990;Goode et al 1992;Ruohola-Baker et al 1993). The embryos within grk, top/DER, cni, and rho eggs are ventralized as well.…”

“…The embryos within grk, top/DER, cni, and rho eggs are ventralized as well. top/DER and rho activities are required in the follicle cells during oogenesis for dorsal follicle cell determination (Schupbach 1987;Ruohola-Baker et al 1993), whereas grk, cni, and brn activities are required in the germ line for proper dorsal folhcle cell fate (Schupbach 1987;Goode et al 1992). top/DER is an oogenesis-specific allele of the Drosophila epidermal growth factor receptor (DER; Schejter and Shilo 1989;Price et al 1989) and is hypothesized to be a receptor for the dorsalizing signal (Schiipbach 1987;Price et al 1989).…”

windbeutel,a gene required for dorsoventral patterning inDrosophila,encodes a protein that has homologies to vertebrate proteins of the endoplasmic reticulum

“…The Grk-Egfr signaling process that is required for dorsoventral patterning, is believed to take place during stage 9, after the oocyte nucleus has moved to its dorsal-anterior position during stage 8 (Montell et al 1991). Early response genes in the follicle cells, such as kek-1 and rhomboid, begin to show a dorsoventral asymmetry in their expression pattern beginning at stage 9 of oogenesis (Ruohola-Baker et al 1993;Musacchio and Perrimon 1996). The gene nudel has also been shown to be expressed during stage 10 of oogenesis (Hong and Hashimoto 1995).…”

Regulation of Receptor Tyrosine Kinase Ligand Processing

“…2) (Freeman 2009). First identified in flies, genetic analysis showed that rhomboid-1 was involved in EGFR signaling but its precise role was obscure (Ruohola-Baker et al 1993;Sturtevant et al 1993;Freeman 1994). Genetic mosaic experiments indicated that it acted in the signal-emitting cell, rather than the EGFRexpressing cell, implying a role in signal generation (Wasserman et al 2000).…”