A tandem duplication in Drosophila melanogaster shows enhanced expression beyond the gene copy number

Abstract

Abstract Tandem duplicated genes are common features of genomes, but the phenotypic consequences of their origins are not well understood. It is not known whether a simple doubling of gene expression should be expected, or else some other expression outcome. This study describes an experimental framework using engineered deletions to assess any contribution of locally acting cis- and globally acting trans-regulatory factors to expression interactions of particular tandem duplicated genes. Acsx1L (CG6300) and Acsx1R (CG11659) are tandem duplicates of a putative acyl-CoA synthetase gene found in Drosophila melanogaster. Experimental deletions of the duplicated segments were used to investigate whether the presence of 1 tandem duplicated block influences the expression of its neighbor. Acsx1L, the gene in the left block, shows much higher expression than either its duplicate Acsx1R or the single Acsx1 in Drosophila simulans. Acsx1L expression decreases drastically upon deleting the right-hand duplicated block. Crosses among wildtype and deletion strains show that high tandem expression is primarily due to cis-acting interactions between the duplicated blocks. No effect of these genes on cuticular hydrocarbons was detected. Sequence and phylogenetic analysis suggest that the duplication rose to fixation in D. melanogaster and has been subject to extensive gene conversion. Some strains actually carry 3 tandem copies, yet strains with 3 Acsx1s do not have higher expression levels than strains with 2. Surveys of tandem duplicate expression have typically not found the expected 2-fold increase in expression. This study suggests that cis-regulatory interactions between duplicated blocks could be responsible for this trend.