Single gene initiates evolution of epithelial architecture and function

Epithelial monolayers are a hallmark of the architecture of metazoan tissues: they provide stability, serve as barriers, and fold into organs. Epithelial cells vary in shape, ranging from flat and spread out to tall and slim. Dynamic epithelial shape changes have been explored in the context of tissue folding, where local cytoskeletal modulations cause epithelial bending and folding. Comparatively little is known about how entire tissues are transformed from a short to tall architecture. Here we show that shape regulation in epithelia can be governed by the activity of a single gene. We use a comparative approach in distantly related flies to experimentally decode the developmental program that directs the formation of columnar epithelia in the blastoderm and thus determines the physiological features of the resulting epithelium. We uncover an evolutionary novel, membrane-associated protein that emerged in flies and triggered a new development program, the cuboidal-to-columnar transformation of epithelial tissues. slow-as-molasses (slam) encodes a Dia/F-actin regulator that exploits an intrinsic morphological plasticity of cells to transform tissues. Our findings demonstrate that a single, newly emerged factor that amplifies its activity in epithelia provides the basis for adaptation and initiates the evolution of novel developmental programs.