Eya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis

Cooperative morphogenesis of cell lineages underlies the development of functional units and organs. To study mechanisms driving the coordination of lineages, we investigated soma-germline interactions during oogenesis. From invertebrates to vertebrates, oocytes develop as part of a germline cyst that consists of the oocyte itself and so-called nurse cells, which feed the oocyte and are eventually removed. The enveloping somatic cells specialize to facilitate either oocyte maturation or nurse cell removal, which makes it essential to establish the right match between germline and somatic cells. We uncover that the transcriptional regulator Eya, expressed in the somatic lineage, controls bilateral cell-cell affinity between germline and somatic cells in Drosophila oogenesis. Employing functional studies and mathematical modelling, we show that differential affinity and the resulting forces drive somatic cell redistribution over the germline surface and control oocyte growth to match oocyte and nurse cells with their respective somatic cells. Thus, our data demonstrate that differential affinity between cell lineages is sufficient to drive the complex assembly of inter-lineage functional units and underlies tissue self-organization during Drosophila oogenesis.