A simple machine is a basic of device that takes mechanical advantage to apply force. Animals and plants self-assemble through the operation of a wide variety of simple machines. Embryos of different species actuate these simple machines to drive the geometric transformations that convert a disordered mass of cells into organized structures with discrete identities and function. These transformations are intrinsically coupled to sequential and overlapping steps of self-organization and self-assembly. The processes of self-organization have been explored through the molecular composition of cells and tissues and their information networks. By contrast, efforts to understand the simple machines underlying self-assembly must integrate molecular composition with the physical principles of mechanics. This primer is concerned with effort to elucidate the operation of these machines, focusing on the \"problem\" of morphogenesis. Advances in understanding self-assembly will ultimately connect molecular-, subcellular-, cellular- and meso-scale functions of plants and animals and their ability to interact with larger ecologies and environmental influences.

The fusion of epithelial sheets is an essential and conserved morphogenetic event that requires the maintenance of tissue continuity. This is secured by membrane-bound or diffusible signals that instruct the epithelial cells, in a coordinated fashion, to change shapes and adhesive properties and when, how and where to move. Here we show that during Dorsal Closure (DC) in Drosophila, the Jun kinase (JNK) signaling pathway modulates integrins expression and ensures tissue endurance. An excess of JNK activity, as an outcome of a failure in the negative feedback implemented by the dual-specificity phosphatase Puckered (Puc), promotes the loss of integrins [the ß-subunit Myospheroid (Mys)] and amnioserosa detachment. Likewise, integrins signal back to the pathway to regulate the duration and strength of JNK activity. Mys is necessary for the regulation of JNK activity levels and in its absence, puc expression is downregulated and JNK activity increases.

Rab11, a small Ras like GTPase marking the recycling endosomes, plays instrumental roles in Drosophila embryonic epithelial morphogenesis where an array of reports testify its importance in the maintenance of cyto-architectural as well as functional attributes of the concerned cells. Proper Rab11 functions ensure a precise regulation of developmentally active cell signaling pathways which in turn promote the expression of morphogens and other physico-chemical cues which finally forge an embryo out of a single layer of cells. Earlier reports have established that Rab11 functions are vital for fly embryonic development where amorphic mutants such as EP3017 homozygotes show a fair degree of epithelial defects along with incomplete dorsal closure. Here, we present a detailed account of the effects of Rab11 loss of function in the dorso-lateral epithelium which resulted in severe dorsal closure defects along with an elevated JNK-Dpp expression. We further observed that the dorso-lateral epithelial cells undergo epithelial to mesenchymal transition as well as apoptosis in Rab11 mutants with elevated expression levels of MMP1 and Caspase-3, where Caspase-3 contributes to the Rab11 knockout phenotype contrary to the knockdown mutants or hypomorphs. Interestingly, the elevated expressions of the core JNK-Dpp signaling could be rescued with a simultaneous knockdown of wingless in the Rab11 knockout mutants suggesting a genetic interaction of Rab11 with the Wingless pathway during dorsal closure, an ideal model of epithelial wound healing.

Apical constriction powers amnioserosa contraction during Drosophila dorsal closure. The nucleation, movement and dispersal of apicomedial actomyosin complexes generates pulsed apical constrictions during early closure. Persistent apicomedial and circumapical actomyosin complexes drive unpulsed constrictions that follow. Here, we show that the microtubule end-binding proteins EB1 and Patronin pattern constriction dynamics and contraction kinetics by coordinating the balance of actomyosin forces in the apical plane. We find that microtubule growth from moving Patronin platforms governs the spatiotemporal dynamics of apicomedial myosin through the regulation of RhoGTPase signaling by transient EB1-RhoGEF2 interactions. We uncover the dynamic reorganization of a subset of short non-centrosomally nucleated apical microtubules that surround the coalescing apicomedial myosin complex, trail behind it as it moves and disperse as the complex dissolves. We demonstrate that apical microtubule reorganization is sensitive to Patronin levels. Microtubule depolymerization compromised apical myosin enrichment and altered constriction dynamics. Together, our findings uncover the importance of reorganization of an intact apical microtubule meshwork, by moving Patronin platforms and growing microtubule ends, in enabling the spatiotemporal modulation of actomyosin contractility and, through it, apical constriction.

The conservation of gene networks that specify and differentiate distinct tissues has long been a subject of great interest to evolutionary developmental biologists, but the question of how pre-existing tissue-specific developmental trajectories merge is rarely asked. During the radiation of flies, two extraembryonic epithelia, known as serosa and amnion, evolved into one, called amnioserosa. This unique extraembryonic epithelium is found in fly species of the group Schizophora, including the genetic model organism Drosophila melanogaster, and has been studied in depth. Close relatives of this group develop a serosa and a rudimentary amnion. The scuttle fly Megaselia abdita has emerged as an excellent model organism to study this extraembryonic tissue organization. In this review, development and functions of the extraembryonic tissue complements of Drosophila and Megaselia are compared. It is concluded that the amnioserosa combines cells, genetic pathway components and functions that were previously associated either with serosa development or amnion development. The composite developmental trajectory of the amnioserosa raises the question of whether merging tissue-specific gene networks is a common evolutionary process. This article is part of the theme issue \'Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom\'.

Dorsal closure is a prominent morphogenetic process during Drosophila embryogenesis, which involves two epithelial tissues, that is, the squamous amnioserosa and the columnar lateral epidermis. Non-muscle myosin II-driven constriction in the amnioserosa leads to a decrease in the apical surface area and pulls on the adjacent lateral epidermis, which subsequently moves dorsally. The pull by the amnioserosa becomes obvious in an elongation of the epidermal cells, especially of those in the first row. The contribution of the epidermal cell elongation has remained unclear to dorsal closure. Cell elongation may be a mere passive consequence or an active response to the pulling by the amnioserosa. Here, we found that the lateral epidermis actively responds. We analyzed tensions within tissues and cell junctions by laser ablation before and during dorsal closure, the elliptical and dorsal closure stages, respectively. Furthermore, we genetically and optochemically induced chronic and acute cell contraction, respectively. In this way, we found that tension in the epidermis increased during dorsal closure. A correspondingly increased tension was not observed at individual junctions, however. Junctional tension even decreased during dorsal closure in the epidermis. We strikingly observed a strong increase of the microtubule amount in the epidermis, while non-muscle myosin II increased in both tissues. Our data suggest that the epidermis actively antagonizes the pull from the amnioserosa during dorsal closure and the increased microtubules might help the epidermis bear part of the mechanical force.

Dorsal closure is a late embryogenesis process required to seal the epidermal hole on the dorsal side of the Drosophila embryo. This process involves the coordination of several forces generated in the epidermal cell layer and in the amnioserosa cells, covering the hole. Ultimately, these forces arise due to cytoskeletal rearrangements that induce changes in cell shape and result in tissue movement. While a number of cytoskeleton regulatory proteins have already been linked to dorsal closure, here we expand this list by demonstrating that four of the six Drosophila formin type actin assembly factors are needed to bring about the proper fusion of the epithelia. An analysis of the morphological and dynamic properties of dorsal closure in formin mutants revealed a differential contribution for each formin, although we found evidence for functional redundancies as well. Therefore, we propose that the four formins promote the formation of several, and only partly identical, actin structures each with a specific role in the mechanics of dorsal closure.

Cellular forces translate into epithelial deformations to shape animal organisms. To set the proper deformations, these forces are modulated in space and time during development. However, several studies have recently highlighted that, in addition to forces, tissue mechanical properties are also actively controlled in space and time to determine the final tissue shape. In this review, we present the different ways used by epithelial tissues to regulate their mechanics and deformability. The choice of one or combination of modes to control mechanical properties is context dependent. Thus, we will first present our current knowledge on tissue mechanical properties, the cellular strategies to modulate them, and the methods used to assess them. We will then present a few examples in which control of epithelial mechanical properties impacts morphogenesis.

Tissues build complex structures like lumens and microvilli to carry out their functions. Most of the mechanisms used to build these structures rely on cells remodelling their apical plasma membranes, which ultimately constitute the specialised compartments. In addition to apical remodelling, these shape changes also depend on the proper attachment of the basal plasma membrane to the extracellular matrix (ECM). The ECM provides cues to establish apicobasal polarity, and it also transduces forces that allow apical remodelling. However, physical crosstalk mechanisms between basal ECM attachment and the apical plasma membrane remain understudied, and the ones described so far are very diverse, which highlights the importance of identifying the general principles. Here, we review apicobasal crosstalk of two well-established models of membrane remodelling taking place during Drosophila melanogaster embryogenesis: amnioserosa cell shape oscillations during dorsal closure and subcellular tube formation in tracheal cells. We discuss how anchoring to the basal ECM affects apical architecture and the mechanisms that mediate these interactions. We analyse this knowledge under the scope of other morphogenetic processes and discuss what aspects of apicobasal crosstalk may represent widespread phenomena and which ones are used to build subsets of specialised compartments.

Steroid hormones influence diverse biological processes throughout the animal life cycle, including metabolism, stress resistance, reproduction, and lifespan. In insects, the steroid hormone, 20-hydroxyecdysone (20E), is the central hormone regulator of molting and metamorphosis, and plays roles in tissue morphogenesis. For example, amnioserosa contraction, which is a major driving force in Drosophila dorsal closure (DC), is defective in embryos mutant for 20E biosynthesis. Here, we show that 20E signaling modulates the transcription of several DC participants in the amnioserosa and other dorsal tissues during late embryonic development, including zipper, which encodes for non-muscle myosin. Canonical ecdysone signaling typically involves the binding of Ecdysone receptor (EcR) and Ultraspiracle heterodimers to ecdysone-response elements (EcREs) within the promoters of responsive genes to drive expression. During DC, however, we provide evidence that 20E signaling instead acts in parallel to the JNK cascade via a direct interaction between EcR and the AP-1 transcription factor subunit, Jun, which together binds to genomic regions containing AP-1 binding sites but no EcREs to control gene expression. Our work demonstrates a novel mode of action for 20E signaling in Drosophila that likely functions beyond DC, and may provide further insights into mammalian steroid hormone receptor interactions with AP-1.