Development, Vol 127, Issue 8 1617-1626, Copyright © 2000 by Company of Biologists

JOURNAL ARTICLES

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

EL Jockusch, C Nulsen, SJ Newfeld and LM Nagy
Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ 85721, USA.

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.

This article has been cited by other articles:

				D. F. Erezyilmaz Imperfect eggs and oviform nymphs: a history of ideas about the origins of insect metamorphosis Integr. Comp. Biol., December 1, 2006; 46(6): 795 - 807. [Abstract] [Full Text] [PDF]

				E. L. Jockusch and K. A. Ober Hypothesis Testing in Evolutionary Developmental Biology: A Case Study from Insect Wings J. Hered., September 1, 2004; 95(5): 382 - 396. [Abstract] [Full Text] [PDF]

				A. Beermann, M. Aranda, and R. Schroder The Sp8 zinc-finger transcription factor is involved in allometric growth of the limbs in the beetle Tribolium castaneum Development, February 15, 2004; 131(4): 733 - 742. [Abstract] [Full Text] [PDF]

				D. J. Emlen and C. E. Allen Genotype to Phenotype: Physiological Control of Trait Size and Scaling in Insects Integr. Comp. Biol., November 1, 2003; 43(5): 617 - 634. [Abstract] [Full Text] [PDF]

				M. I. Galindo, S. A. Bishop, S. Greig, and J. P. Couso Leg Patterning Driven by Proximal-Distal Interactions and EGFR Signaling Science, July 12, 2002; 297(5579): 256 - 259. [Abstract] [Full Text] [PDF]

				C. Rauskolb The establishment of segmentation in the Drosophila leg Development, November 15, 2001; 128(22): 4511 - 4521. [Abstract] [Full Text] [PDF]

				A Beermann, D. Jay, R. Beeman, M Hulskamp, D Tautz, and G Jurgens The Short antennae gene of Tribolium is required for limb development and encodes the orthologue of the Drosophila Distal-less protein Development, January 1, 2001; 128(2): 287 - 297. [Abstract] [PDF]

				N Niwa, Y Inoue, A Nozawa, M Saito, Y Misumi, H Ohuchi, H Yoshioka, and S Noji Correlation of diversity of leg morphology in Gryllus bimaculatus (cricket) with divergence in dpp expression pattern during leg development Development, January 10, 2000; 127(20): 4373 - 4381. [Abstract] [PDF]