Wolff C, Schröder R, Schulz C, Tautz D, Klingler M
Zoologisches Institut der Universität München, Luisenstrasse 14, Germany.
Development. 1998 Sep;125(18):3645-54. doi: 10.1242/dev.125.18.3645.
In short germ embryos, the germ rudiment forms at the posterior ventral side of the egg, while the anterior-dorsal region becomes the extra-embryonic serosa. It is difficult to see how an anterior gradient like that of bicoid in Drosophila could in these embryos be directly involved in patterning of the germ rudiment. Moreover, since it has not yet been possible to recover a bicoid homologue from any species outside the diptera, it has been speculated that the anterior bicoid gradient could be a late addition during insect evolution. We addressed this question by analysing the regulation of potential target genes of bicoid in the short germ embryo of Tribolium castaneum. We demonstrate that homologues of caudal and hunchback from Tribolium are regulated by Drosophila bicoid. In Drosophila, maternal caudal RNA is translationally repressed by bicoid. We find that Tribolium caudal RNA is also translationally repressed by bicoid, when it is transferred into Drosophila embryos under a maternal promoter. This strongly suggests that a functional bicoid homologue must exist in Tribolium. The second target gene, hunchback, is transcriptionally activated by bicoid in Drosophila. Transfer of the regulatory region of Tribolium hunchback into Drosophila also results in regulation by early maternal factors, including bicoid, but in a pattern that is more reminiscent of Tribolium hunchback expression, namely in two early blastoderm domains. Using enhancer mapping constructs and footprinting, we show that caudal activates the posterior of these domains via a specific promoter. Our experiments suggest that a major event in the evolutionary transition from short to long germ embryogenesis was the switch from activation of the hunchback gap domain by caudal to direct activation by bicoid. This regulatory switch can explain how this domain shifted from a posterior location in short germ embryos to its anterior position in long germ insects, and it also suggest how an anterior gradient can pattern the germ rudiment in short germ embryos, i.e. by regulating the expression of caudal.
在短胚型胚胎中，胚原基在卵的后腹侧形成，而前背侧区域则成为胚外浆膜。很难想象果蝇中像双尾那样的前梯度在这些胚胎中如何直接参与胚原基的模式形成。此外，由于尚未能够从双翅目以外的任何物种中找到双尾同源物，因此有人推测前双尾梯度可能是昆虫进化过程中的后期添加物。我们通过分析在赤拟谷盗短胚型胚胎中双尾潜在靶基因的调控来解决这个问题。我们证明，赤拟谷盗的尾和驼背同源物受果蝇双尾调控。在果蝇中，母源尾RNA被双尾翻译抑制。我们发现，当在母源启动子下将赤拟谷盗尾RNA转入果蝇胚胎时，它也被双尾翻译抑制。这强烈表明赤拟谷盗中必须存在功能性的双尾同源物。第二个靶基因驼背，在果蝇中被双尾转录激活。将赤拟谷盗驼背的调控区域转入果蝇也会导致受包括双尾在内的早期母源因子调控，但模式更类似于赤拟谷盗驼背的表达，即在两个早期胚盘区域。使用增强子定位构建体和足迹分析，我们表明尾通过特定启动子激活这些区域的后部。我们的实验表明，从短胚型到长胚型胚胎发育的进化转变中的一个主要事件是从尾激活驼背间隙结构域转变为双尾直接激活。这种调控转换可以解释这个结构域如何从短胚型胚胎中的后部位置转移到长胚型昆虫中的前部位置，并且还表明前梯度如何在短胚型胚胎中对胚原基进行模式形成，即通过调控尾的表达。
