Developmental variability of metallothionein Mtn gene expression in the species of the Drosophila melanogaster subgroup

Abstract

Developmental expression of the Drosophila melanogaster metallothionein Mtn gene has been analysed. Transcripts of this gene accumulate during the vitellogenic phase of oogenesis in a ring of follicular cells at the oocyte-nurse cell margin and in the follicular cells surrounding the oocyte. There is also strong expression of the Mtn gene during the second half of embryogenesis in hemocytes, the endoderm midgut, and Malpighian tubules. A banded expression pattern is observed transiently in the midgut at stage 13. The two Mtn alleles, Mtn and Mtn, show quantitative differences in their expression patterns. Copper intoxication of flies does not induce ectopic expression of the Mtn gene, but rather leads to over-expression of the gene in the structures where it is normally transcribed. Mtn transcription is not altered in homozygous mutants of four genes (lab, wg, dpp, bap) known to be involved in midgut morphogenesis. Expression of Mtn has been also studied in six other species of the melanogaster subgroup. This analysis demonstrates that regulation of Mtn gene transcription has changed during evolution of the Drosophila lineage. For example, Mtn is expressed specifically in the Malpighian tubules of D. melanogaster, while in D. mauritiana and D. sechellia the amnioserosa is a specific location of expression. Nonetheless, expression of Mtn in the midgut is common to the seven species, suggesting a basic role for the MTN protein during embryogenesis in this organ, possibly in the release of metallic ions from vitellogenins. In contrast, two genes also expressed in the embryonic midgut, lab and dFRA, display identical patterns in all species of the melanogaster subgroup. The diversity of Mtn patterns in closely related Drosophila species exemplifies the rapid evolution of a gene regulatory system.