Leg development in flies versus grasshoppers: differences in dpp expression do not lead to differences in the expression of downstream components of the leg patterning pathway

• Published in: Development (Cambridge) Vol. 127; no. 8; pp. 1617 - 1626
• Main Authors: Jockusch, E L, Nulsen, C, Newfeld, S J, Nagy, L M
• Format: Journal Article
• Language: English
• Published: England The Company of Biologists Limited 01.04.2000
• Subjects: Animals; decapentaplegic (dpp) gene; distalless (dll) gene; Drosophila; Drosophila melanogaster - genetics; Drosophila melanogaster - growth & development; Drosophila Proteins; Extradenticle protein; Gene Expression Regulation, Developmental; Grasshoppers - genetics; Grasshoppers - growth & development; Homeodomain Proteins - genetics; Insect Proteins - genetics; Proto-Oncogene Proteins - genetics; Pupa; RNA, Messenger; Schistocerca; Transcription Factors - genetics; wingless (wg) gene; Wnt1 Protein
• ISSN: 0950-1991; 1477-9129
• DOI: 10.1242/dev.127.8.1617

All insect legs are structurally similar, characterized by five primary segments. However, this final form is achieved in different ways. Primitively, the legs developed as direct outgrowths of the body wall, a condition retained in most insect species. In some groups, including the lineage containing the genus Drosophila, legs develop indirectly from imaginal discs. Our understanding of the molecular mechanisms regulating leg development is based largely on analysis of this derived mode of leg development in the species D. melanogaster. The current model for Drosophila leg development is divided into two phases, embryonic allocation and imaginal disc patterning, which are distinguished by interactions among the genes wingless (wg), decapentaplegic (dpp) and distalless (dll). In the allocation phase, dll is activated by wg but repressed by dpp. During imaginal disc patterning, dpp and wg cooperatively activate dll and also indirectly inhibit the nuclear localization of Extradenticle (Exd), which divide the leg into distal and proximal domains. In the grasshopper Schistocerca americana, the early expression pattern of dpp differs radically from the Drosophila pattern, suggesting that the genetic interactions that allocate the leg differ between the two species. Despite early differences in dpp expression, wg, Dll and Exd are expressed in similar patterns throughout the development of grasshopper and fly legs, suggesting that some aspects of proximodistal (P/D) patterning are evolutionarily conserved. We also detect differences in later dpp expression, which suggests that dpp likely plays a role in limb segmentation in Schistocerca, but not in Drosophila. The divergence in dpp expression is surprising given that all other comparative data on gene expression during insect leg development indicate that the molecular pathways regulating this process are conserved. However, it is consistent with the early divergence in developmental mode between fly and grasshopper limbs.