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First published online August 21, 2009
doi: 10.1242/10.1242/dev.038034

Development 136, 3153-3160 (2009)
Published by The Company of Biologists 2009
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Evolving enhancer-promoter interactions within the tinman complex of the flour beetle, Tribolium castaneum

Jessica Doran Cande, Vivek S. Chopra and Michael Levine*

Department of Molecular and Cell Biology, Division of Genetics, Genomics and Development, Center for Integrative Genomics, University of California at Berkeley, Berkeley, CA 94720, USA.

* Author for correspondence (mlevine{at}berkeley.edu)

Accepted 22 July 2009

Modifications of cis-regulatory DNAs, particularly enhancers, underlie changes in gene expression during animal evolution. Here, we present evidence for a distinct mechanism of regulatory evolution, whereby a novel pattern of gene expression arises from altered gene targeting of a conserved enhancer. The tinman gene complex (Tin-C) controls the patterning of dorsal mesodermal tissues, including the dorsal vessel or heart in Drosophila. Despite broad conservation of Tin-C gene expression patterns in the flour beetle (Tribolium castaneum), the honeybee (Apis mellifera) and the fruit fly (Drosophila melanogaster), the expression of a key pericardial determinant, ladybird, is absent from the dorsal mesoderm of Tribolium embryos. Evidence is presented that this loss in expression is replaced by expression of C15, the neighboring gene in the complex. This switch in expression from ladybird to C15 appears to arise from an inversion within the tinman complex, which redirects a conserved ladybird 3' enhancer to regulate C15. In Drosophila, this enhancer fails to activate C15 expression owing to the activity of an insulator at the intervening ladybird early promoter. By contrast, a chromosomal inversion allows the cardiac enhancer to bypass the ladybird insulator in Tribolium. Given the high frequency of genome rearrangements in insects, it is possible that such enhancer switching might be widely used in the diversification of the arthropods.

Key words: Evolution, Heart, Cis-regulation


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Development 2009 136: e1802. [Full Text]  





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