Data from: 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 had greater variability in their 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.

发育过程可在多种可改变全身发育速率的条件下，生成模式构建正确的组织。本研究提出两种假说，用以阐释组织模式形成如何与全身发育协同，从而实现这一发育稳健性。第一种假说认为，组织模式形成过程会随时间推移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，我们借助经典模式形成基因的表达情况，建立了果蝇幼虫翅成虫盘（wing imaginal discs）的分期方案，并将该方案与三类全身发育事件——蜕皮（moulting）、幼虫游走期（larval wandering）及化蛹（pupariation）——进行了关联。随后，我们利用该分期方案，探究了通过改变温度或调控驱动发育进程的激素合成时机来改变发育时长时，模式形成的进展情况。研究发现，翅成虫盘的基因表达模式始终在蜕皮和化蛹阶段实现对齐，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及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，处于游走期的幼虫其翅成虫盘的模式形成阶段具有更大的变异性。因此，对于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。本研究结果揭示，组织模式形成通过在发育里程碑处实现对齐，可抵御环境与生理扰动，维持发育稳健性。此外，本研究为理解个体组织的发育如何与全身发育协同提供了重要见解。