Correlated evolution of the cis‐acting regulatory elements and developmental expression of the Drosophila Gld gene in seven species from the subgroup melanogaster

Abstract

The tissue-specific expression patterns of glucose dehydrogenase (GLD) exhibit a high degree of interspecific variation in the adult reproductive tract among the species in the genus Drosophila. We chose to focus on the evolution of GLD expression and the evolution of the Gld promoter in seven closely related species in the melanogaster subgroup as a means of elucidating the relationship of changes in cis-acting regulatory elements in the Gld promoter region with changes in tissue-specific expression. Although little variation in tissue-specific patterns of GLD was found in nonreproductive tissues during development, a surprisingly high level of variation was observed in the expression of GLD in both developing and mature reproductive organs. In some cases this variation is correlated with changes in sequence elements in the Gld promoter which were previously shown to direct tissue-specific expression in the reproductive tract. In particular D. teissieri adult males do not express GLD in their ejaculatory ducts, atypical of the melanogaster subgroup species. The Gld promoter region of D. teissieri specifically lacks all three of the TTAGA regulatory elements present in D. melanogaster. The TTAGA elements were previously shown to direct reporter gene expression to the ejaculatory duct. Together these data suggest the absence or presence of the TTAGA elements may be responsible for variation in the absence or presence of GLD in the ejaculatory duct among species.

Evolution of cis-regulatory sequence and function in Diptera

“…Changes in enhancer sequence are a common cause of cis-regulatory divergence (eg Fang and Brennan (1992), Ross et al (1994), Wittkopp et al (2002). Enhancer sequences specify when, where, and how much mRNA will be transcribed from the associated coding sequence.…”

“…Cisregulatory changes are also responsible for differences in the expression of the glucose dehydrogenase (gld) gene among flies (Schiff et al, 1992). The presence and absence of a five base pair sequence (TTAGA) in the gld enhancer correlates with the expression of Gld protein in the ejaculatory duct among Drosophila species (Ross et al, 1994), implying that enhancer functions may be modified by only a few changes in cis-regulatory sequence. Enhancers controlling lineage-specific patterns of gene expression can also evolve from existing cis-regulatory elements, taking advantage of transcription factor binding sites already present.…”

Perspective: Evolutionary Developmental Biology and the Problem of Variation

“…Most evidence for cis-regulatory evolution is inferred from qualitatively changed spatial patterns of expression (e.g., Dickinson 1980b;Dickinson et al 1984;Cavener 1992;Schiff et al 1992;Kelsh et al 1994;Panganiban et al 1994;Ross et al 1994;Warren et al 1994;Akam 1995;Averof and Akam 1995;Carroll 1995;Averof et al 1996;Averof and Patel 1997;Grenier et al 1997;Lowe and Wray 1997;Rogers et al 1997;Abzhanov and Kaufman 1999). Several studies have provided experimental evidence supporting cisregulatory evolution (Dickinson and Carson 1979;Dickinson 1980a;Rabinow and Dickinson 1981;Fischer and Maniatis 1986;Brennan et al 1988;Schiff et al 1992;Stam and Laurie 1996;Powell 1997, pp.…”

“…But additional studies by Cavener and coworkers indicate that correlations between the presence or absence of functional enhancer elements and particular expression patterns must be interpreted with caution. Ross et al (1994) searched for correlations between patterns of Gld expression and sequence changes in the enhancer region of Gld among species of the melanogaster subgroup. One promising result was that only D. teissieri lacks expression in the ejaculatory ducts and this species lacks all three TTAGA regulatory elements found within the D. melanogaster enhancer that had previously been shown to be capable of driving expression in the ejaculatory ducts (Quine et al 1993).…”

Evolution of functionally conserved enhancers can be accelerated in large populations: a population–genetic model

“…An examination of the sequence and expression patterns of the D. pseudoobscura esterase-5B and D. melanogaster esterase 6 genes (Tamarina et al 1997) concluded that the conservation of expression patterns need not be accompanied by preservation of the corresponding cis-regulatory elements. Studies of Drosophila glucose dehydrogenase (Gld ) expression in the melanogaster subgroup (Ross et al 1994) have demonstrated that one species, D. teissieri, lacks three elements in its enhancer region that are necessary for expression in the ejaculatory ducts of D. melanogaster, and also lacks Gld expression in this domain. Surprisingly, D. erecta and D. yakuba also lack these elements, but they retain the expression patterns observed in the non-teissieri species (Stern 2000), suggesting the presence of as yet undiscovered compensatory mechanisms.…”