Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina

Distinct shape-shifting regimes of bowl-shaped cell sheets – embryonic inversion in the multicellular green alga Pleodorina
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碗形细胞片的独特变形机制——多细胞绿藻Pleodorina的胚胎倒转

DOI:
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发表时间:
2016
影响因子:
--
通讯作者:
A. Hallmann
A. Hallmann
中科院分区:
生物学4区
文献类型:
--
作者:
Stephanie S Höhn;A. Hallmann

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多细胞藻类 Pleodorina 的生物体复杂性介于其单细胞近缘衣藻和多细胞近缘团藻之间,不同细胞类型之间显示出完全的分工。沃尔沃辛绿色微藻形成一组与团藻目(绿藻门)中团藻属密切相关的属。多细胞 volocine 藻类的胚胎由单层细胞组成,根据物种的不同,该单层细胞可以是碗形的,也可以是球形的。在胚胎发生过程中,多细胞沃尔沃辛胚胎将其细胞单层右侧翻转以暴露其鞭毛。这个过程称为“反转”,是后生动物上皮折叠的简单模型。虽然球形团胚胎的发育一直是详细研究的主题,但碗形胚胎的倒转过程却知之甚少。因此,目前还不清楚球体的反转是如何从不太复杂的过程演化而来的。在这项研究中,我们描述了 64 至 128 细胞 volocine 物种 Pleodorina californica 最初碗形胚胎的倒转。我们重点关注细胞片层的运动模式、细胞形状的变化以及连接细胞的细胞质桥(CB)定位的变化。使用延时光学显微镜记录活胚胎的发育。此外,通过光学和透射电子显微镜分析了整个倒置过程中和连续发育阶段的固定和切片胚胎。我们生成了已识别细胞形状的三维模型,包括 CB 的定位。与有关细胞数量较低的 volocine 胚胎的描述相反,加州 P. californica 的胚胎细胞经历非同时且不均匀的细胞形状变化。在加州 P. californica 中,细胞楔入与 CB 重新定位到基底细胞尖端相结合,解释了倒转过程中细胞片的卷曲。在生物体复杂性较低的沃尔沃素属中,细胞形状的变化和CB的重新定位与苜蓿相比不太明显,而在沃尔沃克斯属的所有成员中则更为明显。这一发现支持在分化的多细胞进化过程中,随着细胞数量和生物体复杂性的增加,细胞形状变化和CB重新定位的时间和空间调节的重要性越来越大。
The multicellular volvocine alga Pleodorina is intermediate in organismal complexity between its unicellular relative, Chlamydomonas, and its multicellular relative, Volvox, which shows complete division of labor between different cell types. The volvocine green microalgae form a group of genera closely related to the genus Volvox within the order Volvocales (Chlorophyta). Embryos of multicellular volvocine algae consist of a cellular monolayer that, depending on the species, is either bowl-shaped or comprises a sphere. During embryogenesis, multicellular volvocine embryos turn their cellular monolayer right-side out to expose their flagella. This process is called ‘inversion’ and serves as simple model for epithelial folding in metazoa. While the development of spherical Volvox embryos has been the subject of detailed studies, the inversion process of bowl-shaped embryos is less well understood. Therefore, it has been unclear how the inversion of a sphere might have evolved from less complicated processes. In this study we characterized the inversion of initially bowl-shaped embryos of the 64- to 128-celled volvocine species Pleodorina californica. We focused on the movement patterns of the cell sheet, cell shape changes and changes in the localization of cytoplasmic bridges (CBs) connecting the cells. The development of living embryos was recorded using time-lapse light microscopy. Moreover, fixed and sectioned embryos throughout inversion and at successive stages of development were analyzed by light and transmission electron microscopy. We generated three-dimensional models of the identified cell shapes including the localization of CBs. In contrast to descriptions concerning volvocine embryos with lower cell numbers, the embryonic cells of P. californica undergo non-simultaneous and non-uniform cell shape changes. In P. californica, cell wedging in combination with a relocation of the CBs to the basal cell tips explains the curling of the cell sheet during inversion. In volvocine genera with lower organismal complexity, the cell shape changes and relocation of CBs are less pronounced in comparison to P. californica, while they are more pronounced in all members of the genus Volvox. This finding supports an increasing significance of the temporal and spatial regulation of cell shape changes and CB relocations with both increasing cell number and organismal complexity during evolution of differentiated multicellularity.
DOI: 10.1093/oxfordjournals.molbev.a040710
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影响因子: 10.7
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