The Glucose dehydrogenase (Gld) gene is highly expressed in the mature Drosophila reproductive tract. Unlike several other Drosophila genes which function in reproductive physiological processes, Gld is also expressed extensively in the developing reproductive tract during metamorphosis. Proximal promoter elements drive Gld expression in a variety of tissues throughout development, but not in the reproductive tract. Herein, we have identified a somatic reproductive organ enhancer complex (SREC) containing multiple redundant enhancer modules in Gld intron I (+639 to +3906 nt). The SREC, in combination with the Gld promoter, activates beta galactosidase reporter gene expression in both the developing and the mature reproductive tract. The SREC activates a heterologous hsp70 promoter in the ejaculatory duct, but not in other reproductive tract tissues, suggesting that the SREC acts synergistically with Gld promoter proximal elements. Through deletion analysis we have delimited a 361-nt region of the SREC that is involved in ejaculatory duct/oviduct-specific expression. The ejaculatory duct/oviduct enhancer retains the ability to activate expression in both the developing and the mature reproductive tract, suggesting that the same basic enhancer elements activate Gld expression during metamorphosis and in adults. A model of the evolution of Gld expression in the ejaculatory duct and oviduct is presented.
The Drosophila melanogaster Gld gene has multiple and diverse developmental and physiological functions. We report herein that interactions among proximal promoter elements and a cluster of intronically located enhancers and silencers specify the complex regulation of Gld that underlies its diverse functions. Gld expression in nonreproductive tissues is largely determined by proximal promoter elements with the exception of the embryonic labium where Gld is activated by an enhancer within the first intron. A nuclear protein, GPAL, has been identified that binds the Gpal elements in the proximal promoter region. Regulation of Gld in the reproductive organs is particularly complex, involving interactions among the Gpal proximal promoter elements, a unique TATA box, three distinct enhancer types, and one or more silencer elements. The three somatic reproductive organ enhancers each activate expression in male and female pairs of reproductive organs. One of these pairs, the male ejaculatory duct and female oviduct, are known to be developmentally homologous. We report evidence that the other two pairs of organs are developmentally homologous as well. A comprehensive model to explain the full developmental regulation of Gld and its evolution is presented.
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