Zelhof Andrew C, Hardy Robert W, Becker Ann, Zuker Charles S
Howard Hughes Medical Institute and Department of Neurobiology, University of California at San Diego, La Jolla, California 92093-0649, USA.
Nature. 2006 Oct 12;443(7112):696-9. doi: 10.1038/nature05128. Epub 2006 Oct 1.
Eyes differ markedly in the animal kingdom, and are an extreme example of the evolution of multiple anatomical solutions to light detection and image formation. A salient feature of all photoreceptor cells is the presence of a specialized compartment (disc outer segments in vertebrates, and microvillar rhabdomeres in insects), whose primary role is to accommodate the millions of light receptor molecules required for efficient photon collection. In insects, compound eyes can have very different inner architectures. Fruitflies and houseflies have an open rhabdom system, in which the seven rhabdomeres of each ommatidium are separated from each other and function as independent light guides. In contrast, bees and various mosquitoes and beetle species have a closed system, in which rhabdomeres within each ommatidium are fused to each other, thus sharing the same visual axis. To understand the transition between open and closed rhabdom systems, we isolated and characterized the role of Drosophila genes involved in rhabdomere assembly. Here we show that Spacemaker, a secreted protein expressed only in the eyes of insects with open rhabdom systems, acts together with Prominin and the cell adhesion molecule Chaoptin to choreograph the partitioning of rhabdomeres into an open system. Furthermore, the complete loss of spacemaker (spam) converts an open rhabdom system to a closed one, whereas its targeted expression to photoreceptors of a closed system markedly reorganizes the architecture of the compound eyes to resemble an open system. Our results provide a molecular atlas for the construction of microvillar assemblies and illustrate the critical effect of differences in a single structural protein in morphogenesis.
眼睛在动物界中差异显著，是针对光检测和图像形成的多种解剖学解决方案进化的一个极端例子。所有光感受器细胞的一个显著特征是存在一个特殊的区室（脊椎动物中的盘状外段，昆虫中的微绒毛视杆），其主要作用是容纳高效收集光子所需的数百万个光受体分子。在昆虫中，复眼可以有非常不同的内部结构。果蝇和家蝇具有开放视杆系统，其中每个小眼的七个视杆彼此分离并作为独立的光导发挥作用。相比之下，蜜蜂以及各种蚊子和甲虫物种具有封闭系统，其中每个小眼内的视杆相互融合，从而共享相同的视轴。为了理解开放和封闭视杆系统之间的转变，我们分离并表征了果蝇中参与视杆组装的基因的作用。我们在此表明，仅在具有开放视杆系统的昆虫眼睛中表达的分泌蛋白Spacemaker，与Prominin和细胞粘附分子Chaoptin共同作用，精心编排视杆在开放系统中的划分。此外，spacemaker（spam）的完全缺失会将开放视杆系统转变为封闭视杆系统，而将其靶向表达至封闭系统的光感受器会显著重组复眼的结构，使其类似于开放系统。我们的结果为微绒毛组装的构建提供了分子图谱，并说明了单一结构蛋白差异在形态发生中的关键作用。
