Toll Genes Have an Ancestral Role in Axis Elongation

Toll Genes Have an Ancestral Role in Axis Elongation
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DOI:
10.1016/j.cub.2016.04.055
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发表时间:
2016-06-20
期刊:
影响因子:
9.2
通讯作者:
Roth, Siegfried
Roth, Siegfried
中科院分区:
生物学1区
文献类型:
--
作者:
Benton, Matthew A.;Pechmann, Matthias;Roth, Siegfried

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发育过程中使用的关键形态发生过程之一是相邻细胞之间受控的插入。这一过程已被纳入一系列发育事件中,并且它也是两侧对称动物的每个主要群体中发生的事件的基础:胚胎沿前后轴伸长[1]。在果蝇中,Pare 等人最近发现了这一过程的一个新组成部分,他们表明三个 Toll 基因共同发挥作用,在种带延伸过程中驱动细胞嵌入 [2]。这一发现提出了这样一个问题:Toll 基因的这种作用是果蝇的进化新颖性还是胚胎形态发生的一般机制。在这里,我们表明 Toll 基因在轴伸长中的功能实际上在节肢动物中广泛保守。首先,我们从功能上证明了赤拟谷盗甲虫细胞嵌入需要两个 Toll 基因。然后,我们证明这些基因属于先前未描述的 Toll 亚科,并且该亚科的成员在跨越整个门的其他六种节肢动物物种的胚胎中表现出条纹表达(如在谷盗中所见和先前在果蝇中报道的[3-5])。最后,我们发现其中两个 Toll 基因是蜘蛛 Parasteatoda tepidariorum(最基础分支节肢动物谱系的成员)的前后胚胎伸长过程中正常形态发生所必需的。根据我们的发现,我们假设 Toll 基因在所有节肢动物最后一个共同祖先(存在于 5.5 亿年前)的胚胎伸长中具有形态发生功能。
One of the key morphogenetic processes used during development is the controlled intercalation of cells between their neighbors. This process has been co-opted into a range of developmental events, and it also underlies an event that occurs in each major group of bilaterians: elongation of the embryo along the anterior-posterior axis [1]. In Drosophila, a novel component of this process was recently discovered by Pare et al., who showed that three Toll genes function together to drive cell intercalation during germband extension [2]. This finding raises the question of whether this role of Toll genes is an evolutionary novelty of flies or a general mechanism of embryonic morphogenesis. Here we show that the Toll gene function in axis elongation is, in fact, widely conserved among arthropods. First, we functionally demonstrate that two Toll genes are required for cell intercalation in the beetle Tribolium castaneum. We then show that these genes belong to a previously undescribed Toll subfamily and that members of this subfamily exhibit striped expression (as seen in Tribolium and previously reported in Drosophila [3-5]) in embryos of six other arthropod species spanning the entire phylum. Last, we show that two of these Toll genes are required for normal morphogenesis during anterior-posterior embryo elongation in the spider Parasteatoda tepidariorum, a member of the most basally branching arthropod lineage. From our findings, we hypothesize that Toll genes had a morphogenetic function in embryo elongation in the last common ancestor of all arthropods, which existed over 550 million years ago.