In order to shape a tissue, individual cell-based mechanical forces have to be integrated into a global force pattern. Over the last decades, the importance of actomyosin contractile arrays, which are the key constituents of various morphogenetic processes, has been established for many tissues. Recent studies have demonstrated that the microtubule cytoskeleton mediates folding and elongation of the epithelial sheet during Drosophila morphogenesis, placing microtubule mechanics on par with actin-based processes. While these studies establish the importance of both cytoskeletal systems during cell and tissue rearrangements, a mechanistic understanding of their functional hierarchy is currently missing. Here, we dissect the individual roles of these two key generators of mechanical forces during epithelium elongation in the developing Drosophila wing. We show that wing extension, which entails columnar-to-cuboidal cell shape remodeling in a cell-autonomous manner, is driven by anisotropic cell expansion caused by the remodeling of the microtubule cytoskeleton from apico-basal to planarly polarized. Importantly, cell and tissue elongation is not associated with Myosin activity. Instead, Myosin II exhibits a homeostatic role, as actomyosin contraction balances polarized microtubule-based forces to determine the final cell shape. Using a reductionist model, we confirm that pairing microtubule and actomyosin-based forces is sufficient to recapitulate cell elongation and the final cell shape. These results support a hierarchical mechanism whereby microtubule-based forces in some epithelial systems prime actomyosin-generated forces.

为了塑造组织，必须将基于单个细胞的机械力整合到整体力模式中。在过去的几十年里，肌动球蛋白收缩阵列对于许多组织来说是重要的，它是各种形态发生过程的关键组成部分。最近的研究表明，微管细胞骨架在果蝇形态发生过程中介导上皮片的折叠和伸长，使微管力学与基于肌动蛋白的过程相当。虽然这些研究确立了细胞骨架系统在细胞和组织重排过程中的重要性，但目前缺乏对其功能层次结构的机械理解。在这里，我们剖析了果蝇翅膀发育过程中上皮伸长过程中这两个关键机械力发生器的各自作用。我们发现，翼延伸需要以细胞自主的方式从柱状细胞形状重塑到立方体细胞形状，这是由微管细胞骨架从顶端基底到平面极化重塑引起的各向异性细胞扩张所驱动的。重要的是，细胞和组织伸长与肌球蛋白活性无关。相反，肌球蛋白 II 表现出稳态作用，因为肌动球蛋白收缩平衡基于极化微管的力，以确定最终的细胞形状。使用还原论模型，我们确认微管和基于肌动球蛋白的力的配对足以重现细胞伸长和最终的细胞形状。这些结果支持了一种分层机制，其中一些上皮系统中基于微管的力主要是肌动球蛋白产生的力。