INTRODUCTION The pathway from a developmental decision to a morphological change in a cell or tissue can typically be divided into two sets of events. The first is a cascade of regulatory processes, such as cell-cell signals and changes in gene expression. Many of the molecules involved in these processes can be readily identified by molecular or genetic screens, because their expression patterns or mutant phenotypes are tissue-specific. However, these molecules have no direct impact on cell morphology. The second set of events includes activation of ‘effector’ molecules that actually drive cell shape changes. Effectors are often cell adhesion and cytoskeletal proteins that tend to be generally expressed and have multiple and/or redundant functions. These properties can make the genetic analysis of effectors rather difficult; as a result, effectors of many developmental processes remain unidentified or poorly characterized. Drosophila provides not one, but several outstanding model systems to study the regulation and mechanics of tissue mor- phogenesis. Adult eyes, wings, ovaries and testes can yield a wide range of mutant phenotypes because each of these organs is highly differentiated, but dispensable for viability of the fly. Many upstream regulators of morphogenesis have been char- acterized for these and other structures. The connection between these regulators and their effectors may be elucidated by a variety of methods including genetic interaction strategies and ‘reverse’ genetics (disrupting the function of proteins suspected to be important). We have performed a reverse genetic analysis of the actin- based motor protein nonmuscle myosin II. Numerous studies have shown that the actin cytoskeleton plays a major role in tissue morphogenesis and can produce specific forces within the cell in direct response to external signals (aspects of this are reviewed by von Kalm et al., 1995; Hall, 1994). Of all the actin modulating proteins that can influence cell shape, the myosins are uniquely suited to generate contractile forces by sliding actin filaments past each other or along the plasma membrane. However, the in vivo composition, organization and regulation of an actomyosin contractile system are well described only in the specialized case of muscle cells, where contraction is powered by sarcomeric myosin II (Harrington and Rodgers, 1984; Rayment et al., 1993). In nonmuscle cells, myosin II is ubiquitous and has been suspected to drive numerous motile events (Warrick and Spudich, 1987). However, all eucaryotes studied express multiple, distinct types of myosin, as well as numerous other motor proteins, complicating the assignment of 1499 Development 122, 1499-1511 (1996) Printed in Great Britain © The Company of Biologists Limited 1996 DEV6218 Morphogenesis is characterized by orchestrated changes in the shape and position of individual cells. Many of these movements are thought to be powered by motor proteins. However, in metazoans, it is often difficult to match specific motors with the movements they drive. The nonmuscle myosin II heavy chain (MHC) encoded by zipper is required for cell sheet movements in Drosophila embryos. To determine if myosin II is required for other processes, we examined the phenotypes of strong and weak larval lethal mutations in spaghetti squash (sqh), which encodes the nonmuscle myosin II regulatory light chain (RLC). sqh mutants can be rescued to adulthood by daily induction of a sqh cDNA transgene driven by the hsp70 promoter. By transiently ceasing induction of the cDNA, we depleted RLC at specific times during development. When RLC is transiently depleted in larvae, the resulting adult pheno- types demonstrate that RLC is required in a stage-specific fashion for proper development of eye and leg imaginal discs. When RLC is depleted in adult females, oogenesis is reversibly disrupted. Without RLC induction, developing egg chambers display a succession of phenotypes that demonstrate roles for myosin II in morphogenesis of the interfollicular stalks, three morphologically and mechanis- tically distinct types of follicle cell migration, and com- pletion of nurse cell cytoplasm transport (dumping). Finally, we show that in sqh mutant tissues, MHC is abnor- mally localized in punctate structures that do not contain appreciable amounts of filamentous actin or the myosin tail-binding protein p127. This suggests that sqh mutant phenotypes are chiefly caused by sequestration of myosin into inactive aggregates. These results show that myosin II is responsible for a surprisingly diverse array of cell shape changes throughout development. Key words: nonmuscle myosin, spaghetti squash, imaginal disc, oogenesis, cell migration, Drosophila, egg chamber SUMMARY Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis Kevin A. Edwards and Daniel P. Kiehart* Department of Cell Biology, Duke University Medical Center, Box 3709, Durham, NC 27710, USA *Author for correspondence (e-mail: Dan_Kiehart@cellbio.duke.edu)