Gene expression in spider appendages reveals reversal of exd/hth spatial specificity, altered leg gap gene dynamics, and suggests divergent distal morphogen signaling.
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.
Prpic
Nikola-Michael
NM
Institut für Genetik, Universität zu Köln, Weyertal 121, D-50931 Köln, Germany.
Janssen
Ralf
R
Wigand
Barbara
B
Klingler
Martin
M
Damen
Wim G M
WG
D000595:Amino Acid Sequence; D000818:Animals; D019521:Body Patterning; D029721:Drosophila Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000033:anatomy & histology / Q000196:embryology / Q000235:genetics / Q000378:metabolism; D005121:Extremities / Q000033:anatomy & histology / Q000254:growth & development; D018507:Gene Expression Regulation, Developmental; D018398:Homeodomain Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism; D017403:In Situ Hybridization; D008969:Molecular Sequence Data; D009024:Morphogenesis; D009687:Nuclear Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism; D010802:Phylogeny; D011518:Proto-Oncogene Proteins / Q000235:genetics / Q000378:metabolism; D016415:Sequence Alignment; D013112:Spiders / Q000033:anatomy & histology / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D020825:T-Box Domain Proteins / Q000145:classification / Q000235:genetics / Q000378:metabolism; D014231:Tribolium / Q000033:anatomy & histology / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism; D051155:Wnt1 Protein
D029721:Drosophila Proteins; D018398:Homeodomain Proteins; D009687:Nuclear Proteins; D011518:Proto-Oncogene Proteins; D020825:T-Box Domain Proteins; D051155:Wnt1 Protein; C103968:dac protein, Drosophila; C064196:dpp protein, Drosophila; C108704:hth protein, Drosophila; C074622:wg protein, Drosophila