Gene expression in spider appendages reveals reversal of exd/hth spatial specificity, altered leg gap gene dynamics, and suggests divergent distal morphogen signaling

Abstract

Leg development in Drosophila has been studied in much detail. However, Drosophila limbs form in the larva as imaginal discs and not during embryogenesis as in most other arthropods. Here, we analyze appendage genes in the spider Cupiennius salei and the beetle Tribolium castaneum. Differences in decapentaplegic (dpp) expression suggest a different mode of distal morphogen signaling suitable for the specific geometry of growing limb buds. Also, expression of the proximal genes homothorax (hth) and extradenticle (exd) is significantly altered: in the spider, exd is restricted to the proximal leg and hth expression extends distally, while in insects, exd is expressed in the entire leg and hth is restricted to proximal parts. This reversal of spatial specificity demonstrates an evolutionary shift, which is nevertheless compatible with a conserved role of this gene pair as instructor of proximal fate. Different expression dynamics of dachshund and Distal-less point to modifications in the regulation of the leg gap gene system. We comment on the significance of this finding for attempts to homologize leg segments in different arthropod classes. Comparison of the expression profiles of H15 and optomotor-blind to the Drosophila patterns suggests modifications also in the dorsal-ventral patterning system of the legs. Together, our results suggest alterations in many components of the leg developmental system, namely proximal-distal and dorsal-ventral patterning, and leg segmentation. Thus, the leg developmental system exhibits a propensity to evolutionary change, which probably forms the basis for the impressive diversity of arthropod leg morphologies.

Differential recruitment of limb patterning genes during development and diversification of beetle horns

“…S1 and S2). Tchth is predicted to encode a 456-aa polypeptide with 2 highly conserved domains, an N-terminal MEIS domain (HM), and a homeodomain (HD) located near the C terminus (34). We observed 99% amino acid and 79% nucleotide identity with Tribolium hth over the 354 bp Ob region (consisting of the nearly complete MEIS domain).…”

Proximodistal identity during vertebrate limb regeneration is regulated by Meis homeodomain proteins

“…Mouse Meis proteins and their Drosophila ortholog Hth are translated and imported into the nucleus constitutively, whereas mouse Pbx1 and its Drosophila ortholog Exd require Meis/Hth expression to be imported into the nucleus and become functional (Abu-Shaar et al, 1999;Berthelsen et al, 1999;Capdevila et al, 1999;Mercader et al, 1999;Rieckhof et al, 1997). Data from Xenopus, zebrafish and spiders provide examples of the opposite situation; Pbx/Exd proteins are expressed constitutively in the nucleus whereas Meis/Hth proteins remain in the cytoplasm by default, and become nuclear only after co-expression with Pbx/Exd (Maeda et al, 2002;Prpic et al, 2003;Vlachakis et al, 2001). These observations suggest that the mechanisms for the regulation of Meis and Pbx activity have remained labile during evolution.…”

Mesodermal Wnt signaling organizes the neural plate via Meis3

“…In Drosophila, the wingless (Wg/Wnt) protein activates expression of the sole Meis protein homolog, the homothorax (hth) gene, which is required for wing hinge development (Casares and Mann, 2000). In both beetles and spiders, hth expression seems to be regulated by Wg during appendage development (Prpic et al, 2003). Thus, in diverged invertebrate systems, Wnt signaling controls Meis/hth family gene expression.…”