Olesnicky Eugenia C, Brent Ava E, Tonnes Lori, Walker Megan, Pultz Mary Anne, Leaf David, Desplan Claude
New York University, Department of Biology, New York, NY 10003, USA.
Development. 2006 Oct;133(20):3973-82. doi: 10.1242/dev.02576. Epub 2006 Sep 13.
One of the earliest steps of embryonic development is the establishment of polarity along the anteroposterior axis. Extensive studies of Drosophila embryonic development have elucidated mechanisms for establishing polarity, while studies with other model systems have found that many of these molecular components are conserved through evolution. One exception is Bicoid, the master organizer of anterior development in Drosophila and higher dipterans, which is not conserved. Thus, the study of anteroposterior patterning in insects that lack Bicoid can provide insight into the evolution of the diversity of body plan patterning networks. To this end, we have established the long germ parasitic wasp Nasonia vitripennis as a model for comparative studies with Drosophila. Here we report that, in Nasonia, a gradient of localized caudal mRNA directs posterior patterning, whereas, in Drosophila, the gradient of maternal Caudal protein is established through translational repression by Bicoid of homogeneous caudal mRNA. Loss of caudal function in Nasonia results in severe segmentation defects. We show that Nasonia caudal is an activator of gap gene expression that acts far towards the anterior of the embryo, placing it atop a cascade of early patterning. By contrast, activation of gap genes in flies relies on redundant functions of Bicoid and Caudal, leading to a lack of dramatic action on gap gene expression: caudal instead plays a limited role as an activator of pair-rule gene expression. These studies, together with studies in short germ insects, suggest that caudal is an ancestral master organizer of patterning, and that its role has been reduced in higher dipterans such as Drosophila.
胚胎发育最早的步骤之一是沿前后轴建立极性。对果蝇胚胎发育的广泛研究阐明了建立极性的机制，而对其他模型系统的研究发现，许多这些分子成分在进化过程中是保守的。一个例外是双尾蛋白，它是果蝇和高等双翅目昆虫前部发育的主要组织者，并不保守。因此，对缺乏双尾蛋白的昆虫前后模式形成的研究可以为身体计划模式形成网络多样性的进化提供见解。为此，我们已将长胚寄生蜂丽蝇蛹集金小蜂作为与果蝇进行比较研究的模型。在此我们报告，在丽蝇蛹集金小蜂中，局部化的尾mRNA梯度指导后部模式形成，而在果蝇中，母体尾蛋白的梯度是通过双尾蛋白对均匀分布的尾mRNA的翻译抑制来建立的。丽蝇蛹集金小蜂中尾功能的丧失会导致严重的节段缺陷。我们表明，丽蝇蛹集金小蜂的尾是间隙基因表达的激活剂，它在胚胎前部很远的位置起作用，将其置于早期模式形成的级联之上。相比之下，果蝇中间隙基因的激活依赖于双尾蛋白和尾的冗余功能，导致对间隙基因表达缺乏显著作用：尾反而作为配对规则基因表达的激活剂发挥有限的作用。这些研究以及对短胚昆虫的研究表明，尾是模式形成的祖先主要组织者，并且其作用在果蝇等高等双翅目昆虫中已经减弱。
