Limb type-specific regulation of bric a brac contributes to morphological diversity.
The insect antenna and leg are considered homologous structures, likely to have arisen via duplication and divergence from an ancestral limb. Consistent with this, the antenna and leg are derived from primordia with similar developmental potentials. Nonetheless, the adult structures differ in both form and function. In Drosophila, one conspicuous morphological difference is that the antenna has fewer distal segments than the leg. We propose that this is due in part to the variations in the regulation of bric a brac. bric a brac is required for joint formation, and loss of bric a brac function leads to fusion of distal antennal and leg segments, resulting in fewer total segments. Here, we address how bric a brac is regulated to generate the mature expression patterns of two concentric rings in the antenna versus four concentric rings in the leg. We find that bric a brac expression is activated early throughout most of the Distal-less domain in both antenna and leg and subsequently is restricted to the distal portion and into rings. Although bric a brac expression in the antenna and in all four tarsal rings of the leg requires Distal-less, only the proximal three tarsal rings are Spineless-dependent. Thus bric a brac is regulated differentially even within a single appendage type. The restriction of bric a brac expression to the distal portion of the Distal-less domain is a consequence of negative regulation by distinct sets of genes in different limb types. In the leg, the proximal boundary of bric a brac is established by the medial-patterning gene dachshund, but dachshund alone is insufficient to repress bric a brac, and the expression of the two genes overlaps. In the antenna, the proximal boundary of bric a brac is established by an antenna-specifying gene, homothorax, in conjunction with dachshund and spalt, and there is much less overlap between the bric a brac and the dachshund domains. Thus tissue-specific expression of other patterning genes that differentially repress bric a brac accounts for antenna-leg differences in bric a brac pattern. We propose that the limb type-specific variations in expression of bric a brac repressors contribute to morphological variations by controlling distal limb segment number.
Chu
Jessie
J
Department of Anatomy, University of Wisconsin, Madison, WI 53706, USA.
Dong
P D Si
PD
Panganiban
Grace
G
D000818:Animals; D019521:Body Patterning; D004268:DNA-Binding Proteins / Q000235:genetics*; D004330:Drosophila / Q000254:growth & development*; D029721:Drosophila Proteins; D005121:Extremities / Q000254:growth & development*; D018507:Gene Expression Regulation, Developmental; D009024:Morphogenesis; D014018:Tissue Distribution; D014157:Transcription Factors / Q000235:genetics*; D014921:Wings, Animal / Q000254:growth & development
C093752:Bric-a-brac protein 1, Drosophila; D004268:DNA-Binding Proteins; D029721:Drosophila Proteins; D014157:Transcription Factors