Genetic characterization of the apterous Life Span Enhancer in Drosophila melanogaster

Abstract

The selector gene apterous (ap) of Drosophila melanogaster is best known for its prominent role in wing formation. apnull flies are viable but have no wings. However, apnull flies are associated with another phenotype whose analysis was largely neglected in the past 40 years: adults die precociously 2-3 days after eclosion. We have recently published a comprehensive analysis on the physiology of this striking phenotype. We showed that Ap protein is essential early in metamorphosis during hindgut remodeling where it is required for rectal papillae formation in the rectal ampulla. Wild-type flies have four rectal papillae that are involved in selective reabsorption of essential ions and metabolites from the primary urine produced by the Malpighian tubules. In apnull flies, rectal papillae formation is aborted prematurely. The corresponding papillar cells remain stuck in the rectal lumen. This leads to complete intestinal blockage and a cascade of pathologies resulting in premature death. In this study, we genetically identify and functionally dissect a novel tissue specific cis- regulatory element that directs Ap expression in the hindgut. This Life Span Enhancer (apLSE) maps to a [~]400 bp DNA fragment that is activated via only two small regulatory modules. Genetic analysis of apLSE alleles proves that they are essential for papilla formation and thus for adult survival. Our studies solve the 110-year-old enigma about the ap syndrome. They establish the apLSE as a key player linking hindgut morphogenesis and survival. We propose that several aspects of the ap syndrome are a consequence of drastic changes in endocrine homeostasis.