Henry Jonathan Q, Lyons Deirdre C, Perry Kimberly J, Osborne C Cornelia
University of Illinois, Department of Cell&Developmental Biology, 601 S. Goodwin Ave., Urbana, IL 61801, United States.
Scripps Institution of Oceanography, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093, United States.
Dev Biol. 2017 Nov 15;431(2):282-296. doi: 10.1016/j.ydbio.2017.09.003. Epub 2017 Sep 6.
During development in metazoan embryos, the fundamental embryonic axes are established by organizing centers that influence the fates of nearby cells. Among the spiralians, a large and diverse branch of protostome metazoans, studies have shown that an organizer sets up the dorsal-ventral axis, which arises from one of the four basic cell quadrants during development (the dorsal, D quadrant). Studies in a few species have also revealed variation in terms of how and when the D quadrant and the organizer are established. In some species the D quadrant is specified conditionally, via cell-cell interactions, while in others it is specified autonomously, via asymmetric cell divisions (such as those involving the formation of polar lobes). The third quartet macromere (3D) typically serves as the spiralian organizer; however, other cells born earlier or later in the D quadrant lineage can serve as the organizer, such as the 2d micromere in the annelid Capitella teleta or the 4d micromere in the mollusc Crepidula fornicata. Here we present work carried out in the snail C. fornicata to show that establishment of a single D quadrant appears to rely on a combination of both autonomous (via inheritance of the polar lobe) and conditional mechanisms (involving induction via the progeny of the first quartet micromeres). Through systematic ablation of cells, we show that D quadrant identity is established between 5th and 6th cleavage stages, as it is in other spiralians that use conditional specification. Subsequently, following the next cell cycle, organizer activity takes place soon after the birth of the 4d micromere. Therefore, unlike the case in other spiralians that use conditional specification, the specification of the D quadrant and the activity of the dorso-ventral organizer are temporally and spatially uncoupled. We also present data on organizer function in naturally-occurring and experimentally-induced twin embryos, which possess multiple D quadrants. We show that supernumerary D quadrants can arise in C. fornicata (either spontaneously or following polar lobe removal); when multiple D quadrants are present these do not exhibit effective organizer activity. We conclude that the polar lobe is not required for D quadrant specification, though it could play a role in effective organizer activity. We also tested whether the inheritance of the small polar lobe by the D quadrant is associated with the ability to laterally inhibit neighboring quadrants by direct contact in order to normally prevent supernumerary organizers from arising. Finally, we discuss the variation of spiralian organizers in a phylogenetic context.
在后生动物胚胎发育过程中，基本的胚胎轴是由影响附近细胞命运的组织中心建立的。在原口动物后生动物的一个庞大且多样的分支——螺旋动物中，研究表明一个组织者建立了背腹轴，该轴在发育过程中源自四个基本细胞象限之一（背侧，D象限）。对一些物种的研究还揭示了D象限和组织者在建立方式和时间方面的差异。在一些物种中，D象限是通过细胞间相互作用有条件地指定的，而在其他物种中，它是通过不对称细胞分裂（如涉及极叶形成的那些分裂）自主指定的。第三四分体大卵裂球（3D）通常作为螺旋动物的组织者；然而，在D象限谱系中更早或更晚产生的其他细胞也可以作为组织者，例如环节动物小头虫中的2d小卵裂球或软体动物有沟帽贝中的4d小卵裂球。在这里，我们展示了在蜗牛有沟帽贝中进行的工作，以表明单个D象限的建立似乎依赖于自主机制（通过极叶的遗传）和条件机制（涉及通过第一四分体小卵裂球的后代进行诱导）的结合。通过系统地消融细胞，我们表明D象限身份在第5次和第6次卵裂阶段之间建立，就像在其他使用条件指定的螺旋动物中一样。随后，在下一个细胞周期之后，组织者活性在4d小卵裂球产生后不久发生。因此，与其他使用条件指定的螺旋动物不同，D象限的指定和背腹组织者的活性在时间和空间上是不耦合的。我们还展示了在自然发生的和实验诱导的双胚胎中组织者功能的数据，这些双胚胎拥有多个D象限。我们表明，在有沟帽贝中可以出现额外的D象限（自发地或在去除极叶之后）；当存在多个D象限时，它们不会表现出有效的组织者活性。我们得出结论，极叶对于D象限的指定不是必需的，尽管它可能在有效的组织者活性中起作用。我们还测试了D象限对小极叶的遗传是否与通过直接接触横向抑制相邻象限以正常防止多余组织者出现的能力相关。最后，我们在系统发育背景下讨论螺旋动物组织者的变异。
