Coordination of Wing and Whole-Body Development at Developmental Milestones Ensures Robustness against Environmental and Physiological Perturbations

Development produces correctly patterned tissues under a wide range of conditions that alter the rate of development in the whole body. We propose two hypotheses through which tissue patterning could be coordinated with whole-body development to generate this robustness. Our first hypothesis states that tissue patterning is tightly coordinated with whole-body development over time. The second hypothesis is that tissue patterning aligns at developmental milestones. To distinguish between our two hypotheses, we developed a staging scheme for the wing imaginal discs of Drosophila larvae using the expression of canonical patterning genes, linking our scheme to three whole-body developmental events: moulting, larval wandering and pupariation. We used our scheme to explore how the progression of pattern changes when developmental time is altered either by changing temperature or by altering the timing of hormone synthesis that drives developmental progression. We found the expression pattern in the wing disc always aligned at moulting and pupariation, indicating that these key developmental events represent milestones. Between these milestones, the progression of pattern showed greater variability in response to changes in temperature and alterations in physiology. Furthermore, our data showed that discs from wandering larvae showed greater variability in patterning stage. Thus for wing disc patterning, wandering does not appear to be a developmental milestone. Our findings reveal that tissue patterning remains robust against environmental and physiological perturbations by aligning at developmental milestones. Furthermore, our work provides an important glimpse into how the development of individual tissues is coordinated with the body as a whole.在能够改变全身发育速率的多种条件下，生物体的发育仍可产生模式构建正确的组织。我们提出两种假说，用以解释组织模式形成如何与全身发育协同，从而实现这一发育鲁棒性。第一种假说指出，组织模式形成随时间进程与全身发育紧密协同。第二种假说则提出，组织模式形成会在发育里程碑处实现对齐。 为区分这两种假说，我们以果蝇（Drosophila）幼虫的翅成虫盘（wing imaginal discs）为研究对象，基于经典模式形成基因（canonical patterning genes）的表达特征建立了分期方案，并将该方案与三类全身发育事件相关联：蜕皮（moulting）、幼虫游走期（larval wandering）与化蛹（pupariation）。我们利用该分期方案，探究了当发育时间通过改变温度，或改变驱动发育进程的激素合成时序而被改变时，模式形成的进展情况。 我们发现，翅成虫盘的基因表达模式始终在蜕皮与化蛹节点处对齐，这表明这些关键发育事件即为发育里程碑。在这些里程碑之间，模式形成的进展对温度变化与生理状态改变的响应表现出更高的变异性。此外，我们的数据显示，处于幼虫游走期的幼虫的成虫盘，其模式形成分期的变异性更高。因此，就翅成虫盘的模式形成而言，幼虫游走期似乎并非发育里程碑。 我们的研究结果揭示，组织模式形成通过在发育里程碑处对齐，得以抵御环境与生理扰动，从而保持鲁棒性。此外，本研究为理解单个组织的发育如何与全身发育协同提供了重要见解。