Elements controlling follicular expression of the s36 chorion gene during Drosophila oogenesis.

Abstract

An 84-bp proximal regulatory region (PRR) of the DrosophUa melanogaster s36 chorion gene is sufficient for directing proper temporal and spatial expression of a reporter gene in three domains of the follicle: anterior, posterior, and main body. Here we show that the fidelity of PRR-directed s36 expression is dependent on the proper dorsal-ventral differentiation of the foilicular epithelium, which requires the Drosophila epidermal growth factor receptor homolog. Transgenic analysis of site-directed mutants of the PRR suggests that s36 expression is regulated by the concerted action of multiple positive activators. Several cis-acting transcriptional elements have been identified: some appear to function in a quantitative manner, while others either are essential or appear to regulate expression in particular spatial domains. The approximate locations of these regulatory elements have been defined; some map within sequences that are strongly conserved in widely divergent dipteran species. In fact, the PRR analog of the medfly Ceratitis capitata Ccs36 gene directs expression in a manner similar to the D. melanogaster s36 PRR. We propose a model for transcriptional regulation of s36 based on the prechoriogenic polarization of the follicular epithelium that surrounds the developing egg chamber.Spatially restricted gene expression is an important feature of development in higher eukaryotes. The expression patterns of genes in the developing Drosophila embryo have been studied extensively (reviewed in references 1, 12, and 45); less well understood is spatial control during postembryonic development. A useful system for studying later developmental gene expression are the Drosophila chorion (eggshell) genes, which are regulated in distinct temporal and spatial patterns, exclusively in the somatic follicular epithelium that surrounds each developing oocyte (for reviews, see references 13 and 27).Several mutations that cause aberrant chorion formation also lead to incorrect pattern formation in the embryo [e.g., fs(1)K10, (51-53), dicephalic (7,20), and torpedo and gurken (36)]. Many of these chorion mutations are germ line dependent, suggesting that the pattern of chorion gene expression may depend on signals from the oocyte to the somatic follicular epithelium, where the chorion genes are actually expressed (4, 28, 36). Conversely, some somatic mutations affect both chorion and embryo (36), suggesting that regional specialization of the follicular epithelium may influence patterning in the oocyte and thus in the developing embryo. Therefore, elucidation of chorion gene regulatory mechanisms could contribute to our understanding of both embryonic and postembryonic developmental patterning.During the 5 to 6 h between stages 10b and 14 of late oogenesis (14) developing oocyte (21,22,29,50). The temporal and spatial regulation of chorion genes is reflected in morphological specializations of the eggshell along the anterior-posterior and dorsal-ventral axes (21,22) and has been documented by molecular studies at both the pr...

Ras signaling modulates activity of the ecdysone receptor EcR during cell migration in the drosophila ovary

“…Surprisingly, while Slbo2.6GAL4 UAS-EcR-DN does repress effectively Cp15 expression in the main body FC, it does not repress Cp15 expression in the centripetal FC where Slbo2.6 expression is high (with similar results for Cp16,18,19,36,and 38). The tissue-specific requirement for EcR regulation of Cp gene expression is consistent with previous work showing that Cp gene expression in the FC relies on composite tissue-specific promoter elements (Tolias et al, 1993). Amplification of the chorion protein genes is controlled by origin recognition complexes (ORCs), which act through conserved cis-acting amplification control elements (ACE elements, reviewed in Claycomb and Orr-Weaver, 2005).…”

bullwinkleandsharkregulate dorsal-appendage morphogenesis inDrosophilaoogenesis

“…Although our methods may miss subtle defects in main-body chorion, shark may play a DA-cell-specific role in the production/formation of chorion. Although regulatory sequences and a putative binding protein drive specific spatial expression of chorion-reporter constructs (Tolias and Kafatos, 1990;Tolias et al, 1993), no reported mutants disrupt DA-specific chorion expression.…”

Vitellogenesis and Post-Vitellogenic Maturation of the Insect Ovarian Follicle

“…Short (less than 100-400 bp) segments of 5 0 -flanking DNA are sufficient to confer correct tissue-specific expression and precise temporal regulation of the transgenes Romano et al, 1988). Cis-acting regulatory elements, identified by mutational analysis, include an essential positive element, characterized by the sequence TCACGT that is conserved in all the chorion gene promoters, negative and positive elements that confer temporal (early or late) specificity, and elements defining spatially restricted expression (review: Orr-Weaver, 1991;Tolias et al, 1993;Mariani et al, 1996). In the latter case, the elements delineate expression in specific subregions of the epithelial surface, notably at the anterior and posterior poles and at the dorsal-anterior surface, where the dorsal appendages are formed (Parks and Spradling, 1987;Tolias and Kafatos, 1990).…”