Single-cell morphometrics reveals ancestral principles of notochord development

Single-cell morphometrics reveals ancestral principles of notochord development
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单细胞形态测量揭示脊索发育的祖先原理

DOI:
10.1101/2020.07.08.193813
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发表时间:
2020
期刊:
Development (Cambridge, England)
影响因子:
--
通讯作者:
Èlia Benito
Èlia Benito
中科院分区:
--
文献类型:
--
作者:
Toby G. R. Andrews;Wolfram Pönisch;E. Paluch;B. Steventon;Èlia Benito

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在发育过程中,胚胎组织是由其组成细胞的动态行为形成的,这些细胞的集体行动在空间和时间上受到严格的调节。为了了解这些细胞行为以及它们是如何进化的,有必要开发定量方法来绘制形态发生图,以便在不同的组织和生物体之间进行比较。考虑到这一点,在这里,我们试图调查脊索发育的祖先的原则,通过建立一个定量的肖像脊索形态发生在文昌鱼胚胎-脊索门的基部分支成员。为此,我们开发了一个单细胞形态测量管道,以全面分类数千个脊索细胞的形态,并将它们同时投影到一个称为morphospace的通用数学空间中。这种方法揭示了细胞类型特定形状轨迹的复杂模式,类似于使用单细胞基因组方法获得的那些。通过空间映射单细胞形状轨迹在整个分段脊索,我们发现的空间和时间变化的证据,在发展动态。这些变化包括形态发生的时间梯度分布在前后轴上,不同形态的轨迹发散,以及不同轨迹收敛到共同形态上。通过几何建模,我们还确定了细胞形状调节和生长之间的拮抗关系,使收敛延伸发生在两个步骤中。首先,通过允许生长来平衡细胞嵌入期间前后细胞长度的损失。其次,一旦细胞已经插入并与轴向中线对齐,通过允许生长进一步增加细胞长度,从而促进组织伸长的第二阶段。最后,我们表明,除了一个复杂的协调个人的细胞行为,后除了从增殖的祖细胞是必不可少的文昌鱼,以前只在脊椎动物中描述的机制,完全脊索伸长。这种新的方法来量化形态的比较研究铺平了道路,和机制的解释出现的形式超过发展和进化的时间尺度。
During development, embryonic tissues are formed by the dynamic behaviours of their constituent cells, whose collective actions are tightly regulated in space and time. To understand such cell behaviours and how they have evolved, it is necessary to develop quantitative approaches to map out morphogenesis, so comparisons can be made across different tissues and organisms. With this idea in mind, here we sought to investigate ancestral principles of notochord development, by building a quantitative portrait of notochord morphogenesis in the amphioxus embryo – a basally-branching member of the chordate phylum. To this end, we developed a single-cell morphometrics pipeline to comprehensively catalogue the morphologies of thousands of notochord cells, and to project them simultaneously into a common mathematical space termed morphospace. This approach revealed complex patterns of cell-type specific shape trajectories, akin to those obtained using single-cell genomic approaches. By spatially mapping single-cell shape trajectories in whole segmented notochords, we found evidence of spatial and temporal variation in developmental dynamics. Such variations included temporal gradients of morphogenesis spread across the anterior-posterior axis, divergence of trajectories to different morphologies, and the convergence of different trajectories onto common morphologies. Through geometric modelling, we also identified an antagonistic relationship between cell shape regulation and growth that enables convergent extension to occur in two steps. First, by allowing growth to counterbalance loss of anterior-posterior cell length during cell intercalation. Secondly, by allowing growth to further increase cell length once cells have intercalated and aligned to the axial midline, thereby facilitating a second phase of tissue elongation. Finally, we show that apart from a complex coordination of individual cellular behaviours, posterior addition from proliferating progenitors is essential for full notochord elongation in amphioxus, a mechanism previously described only in vertebrates. This novel approach to quantifying morphogenesis paves the way towards comparative studies, and mechanistic explanations for the emergence of form over developmental and evolutionary time scales.
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期刊: Development
影响因子: 4.6
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DOI: --
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DOI: 10.1242/dev.122.9.2599
发表时间: 1996
期刊: Development (Cambridge, England)
影响因子: --
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