Diversity and dynamics of chorion patterning across Drosophila species. Matthew G. Niepielko, Robert A. Marmion, Kenneth Kim, David Luor, Chelsea E. Ray, Nir Yakoby. Center for Computational and Integrative Biology, Rutgers University, Camden, NJ.
Drosophila oogenesis is an established model system for studying patterning dynamics and morphogenesis of epithelial cells. During oogenesis, a mono layer of follicle cells overlying the developing oocyte is guided by multiple cell signaling pathways to fold into the 3D Drosophila eggshell. Eggshell morphologies are highly diverse among Drosophila species, and we hypothesized that changes in gene patterning should reflect this diversity. Here, we focus on one of the major family of genes that pattern the Drosophila eggshell, the chorion proteins. Using in situ hybridization, we screened for the patterns of all nine chorion protein genes in three species (D. melanogaster, D. nebulosa, and D. willistoni). We found that most genes are expressed dynamically during mid and late stages of oogenesis. Applying an annotation matrix code to fully capture the complexity of all gene patterns, we compared the annotation matrices among species. Pattern annotations were sufficient to cluster the species according to their phylogenetic associations. Employing genetic manipulations and drugs, we analyzed the fundamental components of the patterns. Strikingly, these results were correlated with the clustering domains. Specifically, each component of the pattern is regulated jointly or independently by two major signaling pathways; the bone morphogenetic protein (BMP) and the epidermal growth factor receptor (EGFR). Our results provide strong evidence that complex gene patterns are combinatorially assembled from simple patterns.