Department of Physics, University of California, Santa Barbara, CA, 93106, USA.
California NanoSystems Institute, University of California, Santa Barbara, CA, 93106, USA.
Sci Rep. 2021 Apr 21;11(1):8591. doi: 10.1038/s41598-021-87672-3.
Shaping embryonic tissues into their functional morphologies requires cells to control the physical state of the tissue in space and time. While regional variations in cellular forces or cell proliferation have been typically assumed to be the main physical factors controlling tissue morphogenesis, recent experiments have revealed that spatial variations in the tissue physical (fluid/solid) state play a key role in shaping embryonic tissues. Here we theoretically study how the regional control of fluid and solid tissue states guides morphogenetic flows to shape the extending vertebrate body axis. Our results show that both the existence of a fluid-to-solid tissue transition along the anteroposterior axis and the tissue surface tension determine the shape of the tissue and its ability to elongate unidirectionally, with large tissue tensions preventing unidirectional elongation and promoting blob-like tissue expansions. We predict both the tissue morphogenetic flows and stresses that enable unidirectional axis elongation. Our results show the existence of a sharp transition in the structure of morphogenetic flows, from a flow with no vortices to a flow with two counter-rotating vortices, caused by a transition in the number and location of topological defects in the flow field. Finally, comparing the theoretical predictions to quantitative measurements of both tissue flows and shape during zebrafish body axis elongation, we show that the observed morphogenetic events can be explained by the existence of a fluid-to-solid tissue transition along the anteroposterior axis. These results highlight the role of spatiotemporally-controlled fluid-to-solid transitions in the tissue state as a physical mechanism of embryonic morphogenesis.
塑造胚胎组织的功能形态需要细胞控制组织在空间和时间上的物理状态。虽然细胞力或细胞增殖的区域变化通常被认为是控制组织形态发生的主要物理因素，但最近的实验表明，组织物理（流体/固体）状态的空间变化在塑造胚胎组织方面起着关键作用。在这里，我们从理论上研究了如何通过区域控制流体和固体组织状态来引导形态发生流来塑造伸展的脊椎动物体轴。我们的结果表明，沿前后轴存在从流体到固体组织的转变以及组织表面张力决定了组织的形状及其单向伸长的能力，大的组织张力阻止单向伸长并促进块状组织扩展。我们预测了能够实现单向轴伸长的组织形态发生流和应力。我们的结果表明，形态发生流的结构存在一个明显的转变，从没有涡旋的流转变为具有两个反向旋转涡旋的流，这是由于流场中拓扑缺陷的数量和位置的转变引起的。最后，将理论预测与斑马鱼体轴伸长过程中组织流和形状的定量测量进行比较，我们表明，观察到的形态发生事件可以用沿前后轴的流体到固体组织转变的存在来解释。这些结果强调了时空控制的流体到固体转变在组织状态中的作用，这是胚胎形态发生的物理机制。
