Complex cis‐acting regulatory genes demonstrated in Drosophila hybrids

Abstract

Drosophila heteroneura and D differens are closely related, interfertile species of the Hawaiian picture-winged group. They display marked qualitative and quantitative differences in the pattern of expression of alcohol dehydrogenase (ADH) and an aldehyde oxidase (AO-1). These presumptive regulatory differences are revealed by comparisons of the relative levels of these enzymes in various tissues in larvae and adults. In hybrids produced between parents carrying different electrophoretic alleles at the structural loci for these two enzymes, each allele is expressed according to the developmental program characteristic of the parent from which it was derived. This result indicates control of the differences in pattern of expression by one or more cis-acting sites associated with each structural locus. The distribution of activity among the three forms of these dimeric enzymes produced in hybrids indicates that the pattern differences reflect differential accumulation of enzyme molecules, not altered catalytic properties. As expected, the regulatory differences segregate with the electrophoretic markers in backcrosses.Key words: aldehyde oxidase, alcohol dehydrogenase, Hawaiian Drosophila, interspecific hybridiza. tion, regulatory genes I N T RODUCT IONThe appearance of specific gene products in characteristic tissue and stage-specific patterns is a central feature of animal development. The nature and mode of operation of the information that controls such developmental programs remain largely unknown and their elucidation is the goal of much current research. There is limited but significant direct evidence for the location of information concerned with the pattern of expression of specific structural genes in linked, cis-acting sites [ 1-63 . Somewhat indirect arguments based on patterns of molecular organization of eukaryotic genomes and the apparent large excess of DNA over that required to encode structural information have led to similar suggestions [7-91.

Regulatory gene evolution: Adaptive differences in expression of alcohol dehydrogenase in Drosophila melanogaster and Drosophila simulans

“…Differences in cis-acting regulators are revealed as temporal or spatial variation in the ratio of the two products (Dickinson, 1980b(Dickinson, , 1983). An analysis of ADH in tissues of D. melanogaster x D. simulans hybrids is displayed in fig.…”

“…In those cases, cis-acting factors alone were sufficient to account for major regulatory differences (Dickinson and Carson, 1979;Dickinson, 1980b) and differences in enzyme activity were reflected at the RNA level (Rabinow and Dickinson, 1981 and unpublished). In the present case, the cis-acting component accounts for only about half of the difference seen between species.…”

“…For example, we have used interspecific Drosophila hybrids to demonstrate complex, cis-acting genetic elements that control the tissue and stage specific expression of linked structural genes. (Dickinson and Carson, 1979;Dickinson, 1980bDickinson, , 1983. Molecular comparisons of the parental species can provide evidence concerning the level at which these elements operate (Rabinow and Dickinson, 1981) and may lead to identification of relevant DNA sequences.…”

“…Thus, it appears that expression in these two stages can evolve more or less independently. We previously have reported a number of similar examples that indicate that various aspects of the developmental program of a specific gene can change independently, all under cis-acting control (Dickinson, 1980b(Dickinson, , 1983. We have suggested that these results imply some sort of complexity in the regulatory region of such genes and have published a speculative model involving multiple promoters (Dickinson, 1983).…”

Regulatory differences in developmental expression of alcohol dehydrogenase are related to interspecies differences in ethanol tolerance of Drosophila

“…As the allozymes coded by D. vi ri/is and D. novamexicana differ in electrophoretic mobility patterns a strategy designed by Dickinson (1980) was used to compare the relative expression of the alleles in interspecific hybrids. From the results shown in Fig.…”