Year: 2013
Type: dissertation
Abstract: Evolutionarily conserved signaling pathways mediate cell-cell communications during development. While the extracellular signal is precisely regulated to achieve dynamic morphogenetic events at the species level, it must be also flexible to generate the diversified morphologies through evolution. However, little is known about the mechanisms behind the precision and flexibility. The insect wing vein pattern can provide an excellent model to address this fundamental question, since species-specific wing vein patterns have been diversified through evolution. In this thesis, I study how evolutionarily conserved bone morphogenetic protein (BMP)-type ligand specifies diversified insect wing vein patterns using Dipteran Drosophila melanogaster and Hymenopteran sawfly Athalia rosae as models. In Drosophila, BMP-type ligand Decapentaplegic (Dpp) is expressed in the longitudinal veins (LVs) to maintain LVs and induce crossveins (CVs) fates during pupal stages. However, the distribution of Dpp remained largely unknown. Using GFP-tagged Dpp, I demonstrated that Dpp is directionally transported from LVs into the posterior crossvein (PCV) region by two extracellular BMP-binding proteins, Short gastrulation (Sog) and Crossveinless (Cv). In contrast, most of Dpp did not diffuse from LVs by Type I BMP receptor and a positive feedback mechanism. Thus the active transport and retention mechanisms allow diffusible Dpp to draw the complex wing vein patterns in Drosophila. To investigate how BMP signal instructs wing vein morphogenesis that involves apposition and cell shape changes between two wing epithelial layers, I then focused on the function of RhoGAP Crossveinless-C (Cv-C) during the PCV morphogenesis. I found that cv-c mediates PCV morphogenesis downstream of BMP signal by inactivating various Rho-type small GTPases. Interestingly, I found that cv-c is also required for Dpp transport, while Sog/Cv mediated BMP signal is guided at the ectopic wing veins caused by loss of Rho-type small GTPases. These observations identified a feed-forward mechanism coupling Dpp transport and PCV morphogenesis. To address how BMP signal specifies diversified insect wing vein patterns, I then introduced sawfly as a new model. I found that dpp is ubiquitously expressed but BMP signal reflects distinct fore- and hindwing vein patterns in sawfly. To address if Dpp transport mechanism is involved in wing vein formation, Cv/Tsg was identified from sawfly. Loss of dpp or cv/tsg by RNAi affected BMP signal and all of wing venations. These observations suggest that ubiquitously expressed Dpp is redistributed to specify distinct fore- and hindwing vein patterns in sawfly. Taken together, I found that the extracellular distribution of Dpp/BMP is tightly regulated and coordinated to achieve precise patterning and morphogenesis of the insect wing veins. Furthermore, this study raises an interesting possibility that changes in the directionality of Dpp/BMP diffusion may underlie distinct insect wing vein patterns.
Source: Työväentutkimus Vuosikirja
Author: Shinya Matsuda
Language: English
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: green
Funder: Helsingin Yliopisto
OpenAlex ID: W628044542