A revised understanding of Tribolium morphogenesis further reconciles short and long germ development.

A revised understanding of Tribolium morphogenesis further reconciles short and long germ development.
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DOI:
10.1371/journal.pbio.2005093
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发表时间:
2018-07
期刊:
影响因子:
9.8
通讯作者:
Benton MA
Benton MA
中科院分区:
生物学1区
文献类型:
--
作者:
Benton MA

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在黑腹果蝇中,胚带直接在卵表面形成,仅由胚胎组织组成。相比之下,大多数昆虫胚胎经历了一系列复杂的组织重排,产生一个浓缩的,多层的胚带。胚带的腹侧是胚胎,而背侧被认为是一种叫做羊膜的胚外组织。虽然这种组织结构已经被接受了几十年,并已在昆虫中广泛报道,但其准确性尚未在任何物种中直接测试。使用活细胞跟踪和差分细胞标记在短的胚芽甲虫赤拟谷盗,我表明,以前被认为是羊膜的大部分细胞实际上引起大部分的胚胎。这一过程通过细胞的背腹流动发生,并有助于胚带延伸(GBE)。此外,我表明,真正的'羊膜'细胞在赤拟谷盗起源于一个小区域的胚盘。总之,我的研究结果表明,Tribolium的短胚胚和果蝇的长胚胚的发育比以前提出的更相似。背腹细胞流也发生在果蝇GBE,我认为,流动是由一组保守的基本形态发生事件在这两个物种。此外,我提出的修订后的赤拟谷盗命运图比经典的赤拟谷盗命运图更类似于果蝇。最后,我的研究结果表明,细胞化胚盘和短/中间胚芽胚带的组织结构之间没有质的差异。因此,相同的组织模式化机制可以在整个细胞化胚盘和胚带阶段持续发挥作用,并且随着进化时间的推移很容易在它们之间转移。在许多动物中,胚胎中的某些细胞群并不直接有助于成年结构的形成。相反,这些支持和促进发育的所谓“胚外组织”在出生/孵化之前就被丢弃并退化。大多数昆虫物种的胚胎被认为有两种类型的胚外组织:包裹整个胚胎和蛋黄的浆膜,以及只覆盖一半胚胎的羊膜。关于羊膜的描述已经被广泛报道了超过一个世纪,但缺乏对该组织的详细研究。在这里,我使用成像和跟踪技术来研究甲虫赤拟谷盗胚胎中的羊膜发育。与我们目前的理解相反,我表明,大多数细胞以前被认为是羊膜的一部分,构成了胚胎的大区域。此外,我表明,这些细胞作为一个整体组织“流动”,并有助于胚胎的伸长,只有相对少量的细胞形成实际的羊膜。这种相似之处,在果蝇,黑腹果蝇的研究胚带,表明,尽管表现出实质性的差异,在整体结构,甲虫和苍蝇的胚胎共享一套保守的形态发生过程。
In Drosophila melanogaster, the germband forms directly on the egg surface and solely consists of embryonic tissue. In contrast, most insect embryos undergo a complicated set of tissue rearrangements to generate a condensed, multilayered germband. The ventral side of the germband is embryonic, while the dorsal side is thought to be an extraembryonic tissue called the amnion. While this tissue organisation has been accepted for decades and has been widely reported in insects, its accuracy has not been directly tested in any species. Using live cell tracking and differential cell labelling in the short germ beetle Tribolium castaneum, I show that most of the cells previously thought to be amnion actually give rise to large parts of the embryo. This process occurs via the dorsal-to-ventral flow of cells and contributes to germband extension (GBE). In addition, I show that true ‘amnion’ cells in Tribolium originate from a small region of the blastoderm. Together, my findings show that development in the short germ embryos of Tribolium and the long germ embryos of Drosophila is more similar than previously proposed. Dorsal-to-ventral cell flow also occurs in Drosophila during GBE, and I argue that the flow is driven by a conserved set of underlying morphogenetic events in both species. Furthermore, the revised Tribolium fate map that I present is far more similar to that of Drosophila than the classic Tribolium fate map. Lastly, my findings show that there is no qualitative difference between the tissue structure of the cellularised blastoderm and the short/intermediate germ germband. As such, the same tissue patterning mechanisms could function continuously throughout the cellularised blastoderm and germband stages, and easily shift between them over evolutionary time. In many animals, certain groups of cells in the embryo do not directly contribute to the formation of adult structures. Instead, these so-called ‘extraembryonic tissues’ that support and facilitate development are discarded and degenerate prior to birth/hatching. Embryos of most insect species are thought to have two types of extraembryonic tissues: the serosa, which encapsulates the entire embryo and yolk, and the amnion, which covers only half of the embryo. Descriptions of the amnion have been widely reported for over a century, but detailed studies of this tissue are lacking. Here I used imaging and tracking techniques to investigate amnion development in the beetle Tribolium castaneum embryo. In contrast to our current understanding, I show that most cells previously thought to be part of the amnion constitute large regions of the embryo. In addition, I show that these cells ‘flow’ as a whole tissue and contribute to the elongation of the embryo, and only a relatively small number of cells form the actual amnion. This resemblance to the well-studied germband in the fruit fly, Drosophila melanogaster, shows that despite exhibiting substantial differences in the overall structure, embryos of beetles and flies share a conserved set of morphogenetic processes.
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