title: BMP signaling dynamics in the follicle cells of multiple Drosophila species.
abstract: The dorsal anterior region of the follicle cells (FCs) in the developing Drosophila egg gives rise to the respiratory eggshell appendages. These tubular structures display a wide range of qualitative and quantitative variations across Drosophila species, providing a remarkable example of a rapidly evolving morphology. In D. melanogaster, the bone morphogenetic protein (BMP) signaling pathway is an important regulator of FCs patterning and dorsal appendages morphology. To explore the mechanisms underlying the diversification of eggshell patterning, we analyzed BMP signaling in the FCs of 16 Drosophila species that span 45 million years of evolution. We found that the spatial patterns of BMP signaling in the FCs are dynamic and exhibit a range of interspecies' variations. In most of the species examined, the dynamics of BMP signaling correlate with the expression of the type I BMP receptor thickveins (tkv). This correlation suggests that interspecies' variations of tkv expression are responsible for the diversification of BMP signaling during oogenesis. This model was supported by genetic manipulations of tkv expression in the FCs of D. melanogaster that successfully recapitulated the signaling diversities found in the other species. Our results suggest that regulation of receptor expression mediates spatial diversification of BMP signaling in Drosophila oogenesis, and they provide insight into a mechanism underlying the evolution of eggshell patterning.
authors.affiliation: Biology Department and Center for Computational and Integrative Biology, Science Building, 315 Penn Street, Rutgers, The State University of New Jersey, Camden, NJ 08102, USA.
authors.forename: Matthew G
authors.initials: MG
authors.lastname: Niepielko
authors.forename: Yainna
authors.initials: Y
authors.lastname: Hernáiz-Hernández
authors.forename: Nir
authors.initials: N
authors.lastname: Yakoby
mesh_terms: D000818:Animals; D019485:Bone Morphogenetic Proteins / Q000235:genetics* / Q000378:metabolism; D004330:Drosophila / Q000145:classification / Q000196:embryology / Q000235:genetics*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000166:cytology / Q000235:genetics / Q000648:ultrastructure; D005260:Female; D018507:Gene Expression Regulation, Developmental; D017403:In Situ Hybridization; D008855:Microscopy, Electron, Scanning; D009866:Oogenesis / Q000235:genetics; D006080:Ovarian Follicle / Q000166:cytology / Q000378:metabolism* / Q000648:ultrastructure; D010802:Phylogeny; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D011956:Receptors, Cell Surface / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction; D013045:Species Specificity; D016212:Transforming Growth Factor beta / Q000235:genetics / Q000378:metabolism
chemical_list: D019485:Bone Morphogenetic Proteins; D029721:Drosophila Proteins; D011956:Receptors, Cell Surface; D016212:Transforming Growth Factor beta; C089440:gbb protein, Drosophila; C090169:tkv protein, Drosophila; D017346:Protein Serine-Threonine Kinases