Zasp52 strengthens whole embryo tissue integrity through supracellular actomyosin networks

Abstract

During morphogenesis, large scale changes of tissue primordia occur that are all coordinated across an embryo. In Drosophila, several tissue primordia and embryonic regions are bordered or encircled by supracellular actomyosin cables, junctional actomyosin enrichments networked between many neighbouring cells. We show that the single Drosophila Alp/Enigma family protein Zasp52, which is most prominently found in Z-discs of muscles, is a component of many supracellular actomyosin structures during embryogenesis, including the ventral midline and the boundary of the salivary gland placode. Zasp52, we uncover, contains within its central coiled-coil region a type of actin-binding motif usually found in CapZbeta proteins, and this domain displays actin binding activity. Using endogenously-tagged lines we identify that Zasp52 interacts with a subset of junctional components, including APC2, Polychaetoid/ZO-1, and Sidekick, as well as actomyosin regulators. Analysis of zasp52 mutant embryos revealed that the severity of the embryonic defects observed scales inversely with the amount of functional protein left. Large tissue deformations occur at sites where actomyosin cables are found during embryogenesis, suggesting a model whereby supracellular cables containing Zasp52 aid to insulate morphogenetic changes from one another. This is further supported by the analysis of in vivo processes as well as by an in silico vertex model of morphogenetic domains separated by a stiffness boundary.