Evolution of extracellular Dpp modulators in insects: The roles of tolloid and twisted-gastrulation in dorsoventral patterning of the Tribolium embryo.
The formation of the BMP gradient which patterns the DV axis in flies and vertebrates requires several extracellular modulators like the inhibitory protein Sog/Chordin, the metalloprotease Tolloid (Tld), which cleaves Sog/Chordin, and the CR domain protein Twisted gastrulation (Tsg). While flies and vertebrates have only one sog/chordin gene they possess several paralogues of tld and tsg. A simpler and probably ancestral situation is observed in the short-germ beetle Tribolium castaneum (Tc), which possesses only one tld and one tsg gene. Here we show that in T. castaneum tld is required for early BMP signalling except in the head region and Tc-tld function is, as expected, dependent on Tc-sog. In contrast, Tc-tsg is required for all aspects of early BMP signalling and acts in a Tc-sog-independent manner. For comparison with Drosophila melanogaster we constructed fly embryos lacking all early Tsg activity (tsg;;srw double mutants) and show that they still establish a BMP signalling gradient. Thus, our results suggest that the role of Tsg proteins for BMP gradient formation has changed during insect evolution.
Institute of Developmental Biology, University of Cologne, Cologne, Gyrhofstrasse 17, D-50931, Germany.
Rodrigo
R
Nunes da Fonseca
Maurijn
M
van der Zee
Siegfried
S
Roth
D000818:Animals; D019521:Body Patterning / Q000235:genetics; D019485:Bone Morphogenetic Proteins / Q000235:genetics / Q000378:metabolism; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000196:embryology / Q000235:genetics; D004625:Embryo, Nonmammalian / Q000196:embryology / Q000378:metabolism; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D019476:Insect Proteins / Q000145:classification / Q000235:genetics* / Q000378:metabolism; D007313:Insecta / Q000145:classification / Q000196:embryology / Q000235:genetics*; D010802:Phylogeny; D034622:RNA Interference; D055394:Tolloid-Like Metalloproteinases / Q000235:genetics / Q000378:metabolism; D014231:Tribolium / Q000196:embryology / Q000235:genetics
D019485:Bone Morphogenetic Proteins; D029721:Drosophila Proteins; D019476:Insect Proteins; C090223:TSG protein, Drosophila; C064196:dpp protein, Drosophila; D055394:Tolloid-Like Metalloproteinases