The bone morphogenetic protein (BMP) signaling network, comprising evolutionary conserved BMP2/4/Decapentaplegic (Dpp) and Chordin/Short gastrulation (Sog), is widely utilized for dorsal-ventral (DV) patterning during animal development. A similar network is required for posterior crossvein (PCV) formation in the Drosophila pupal wing. Although both transcriptional and post-transcriptional regulation of co-factors in the network gives rise to tissue-specific and species-specific properties, their mechanisms are incompletely understood. In Drosophila, BMP5/6/7/8-type ligands, Screw (Scw) and Glass bottom boat (Gbb), form heterodimers with Dpp for DV patterning and PCV development, respectively. Sequence analysis indicates that the Scw ligand contains two N-glycosylation motifs: one being highly conserved between BMP2/4- and BMP5/6/7/8-type ligands, and the other being Scw ligand specific. Our data reveal that N-glycosylation of the Scw ligand boosts BMP signaling both in cell culture and in the embryo. In contrast, N-glycosylation modifications of Gbb or Scw ligands reduce the consistency of PCV development. These results suggest that tolerance for structural changes of BMP5/6/7/8-type ligands is dependent on developmental constraints. Furthermore, gain and loss of N-glycosylation motifs in conserved signaling molecules under evolutionary constraints appear to constitute flexible modules to adapt to developmental processes.
The authors declare no competing or financial interests.
P.M.T. performed most of the experiments and all data analysis. J.G. performed wing experiments. P.M.T. and O.S. designed the experiments and wrote the paper.
This work was supported by the Academy of Finland (Suomen Akatemia) [265648 to O.S. and Center of Excellence in Experimental and Computational Developmental Biology]; the Sigrid Juselius Foundation (O.S.); and the Integrative Life Science Doctoral Program of the University of Helsinki (J.G.).
Supplementary information available online at http://dev.biologists.org/lookup/doi/10.1242/dev.130427.supplemental
- Received September 2, 2015.
- Accepted August 17, 2016.