Live imaging has revolutionized the analysis of developmental biology over the last few years. The ability to track in real time the dynamic processes that occur at tissue and cellular levels gives a much clearer view of development, and allows greater temporal resolution, than is possible with fixed tissue. Drosophila imaginal discs are a particularly important model of many aspects of development, but their small size and location inside the larva and pupa has prevented live imaging techniques from extensively being used in their study. Here, we introduce the use of viscous culture medium to enable high resolution imaging of imaginal disc development. As a proof of principle, we have analyzed the transformation that occurs during metamorphosis of the wing imaginal disc into the mature wing and report several previously unobserved stages of this model of organogenesis. These imaging methods are especially useful to study the complex and dynamic changes that occur during morphogenesis, but we show that they can also be used to analyze other developmental and cellular events. Moreover, our viscous medium creates a platform for future adaptation of other tissue culture conditions to allow imaging of a wide range of developmental events and systems.wing | eversion | organogenesis | epithelia
The eyegone (eyg) gene is known to be involved in the development of the eye structures of Drosophila. We show that eyg and its related gene, twin of eyegone (toe), are also expressed in part of the anterior compartment of the adult mesothorax (notum). We report experiments concerning the role of these genes in the notum. In the absence of eyg function the anterior-central region does not develop, whereas ectopic activity of either eyg or toe induces the formation of the anterior-central pattern in the posterior or lateral region of the notum. These results demonstrate that eyg and toe play a role in the genetic subdivision of the notum, although the experiments indicate that eyg exerts the principal function. However, by itself the Eyg product cannot induce the formation of notum patterns; its thoracic function requires co-expression with the Iroquois (Iro) genes. We show that the restriction of eyg activity to the anterior-central region of the wing disc is achieved by the antagonistic regulatory activities of the Iro and pnr genes, which promote eyg expression, and those of the Hh and Dpp pathways, which act as repressors. We argue that eyg is a subordinate gene of the Iro genes, and that pnr mediates their thoracic patterning function. The activity of eyg gives rise to a new notum subdivision that acts upon the pre-extant one generated by the Iro genes and pnr. As a result the notum becomes subdivided into four distinct genetic domains.
The motor protein non-muscle myosin II is a major driver of the movements that sculpt three dimensional organs from two dimensional epithelia. The machinery of morphogenesis is well established but the logic of its control remains unclear in complex organs. Here we use live imaging and ex vivo culture to report a dual role of myosin II in regulating the development of the Drosophila wing. First, myosin II drives the contraction of a ring of cells that surround the squamous peripodial epithelium, providing the force to fold the whole disc through about 90°. Second, myosin II is needed to allow the squamous cells to expand and then retract at the end of eversion. The combination of genetics and live imaging allows us to describe and understand the tissue dynamics, and the logic of force generation needed to transform a relatively simple imaginal disc into a more complex and three-dimensional adult wing.
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