A mosaic of independent innovations involving eyes shut are critical for the evolutionary transition from fused to open rhabdoms

A mosaic of independent innovations involving eyes shut are critical for the evolutionary transition from fused to open rhabdoms
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DOI:
10.1016/j.ydbio.2018.09.016
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发表时间:
2018-11-15
影响因子:
2.7
通讯作者:
Zelhof,Andrew C.
Zelhof,Andrew C.
中科院分区:
生物学3区
文献类型:
--
作者:
Mahato,Simpla;Nie,Jing;Zelhof,Andrew C.

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进化生物学中的一个基本问题是,在遵守功能限制的同时,如何修改发育过程以产生形态创新。在这里,我们通过研究同位复眼小眼融合和开放纹状体之间转换的细胞机制来解决这个问题,这是基于神经叠加的视觉系统发展所需的关键步骤。利用果蝇和小鼠分别作为全变态昆虫融合和开放随机形态的代表,我们确定了这一创新发生所需的三个变化。首先,在开放纹状体的类群中,细胞外基质蛋白EYS的表达模式从机械感觉神经元扩展到光感受器细胞。其次,EYS同源物获得了一个新的氨基末端延伸,导致切割的信号序列内部化。这种氨基末端的延伸不会干扰机械感觉神经元的切割或功能,但它确实允许将EYS蛋白特异性地靶向顶端光感受器膜。最后,在EYS和Prominin同源物的子集之间进化了一种特定的相互作用,这是开发开放的、但不是融合的重组体所必需的。总而言之,我们的发现描绘了一个案例研究,其中一组分子新颖性的进化催生了适应性光感受器细胞排列的起源。
A fundamental question in evolutionary biology is how developmental processes are modified to produce morphological innovations while abiding by functional constraints. Here we address this question by investigating the cellular mechanism responsible for the transition between fused and open rhabdoms in ommatidia of apposition compound eyes; a critical step required for the development of visual systems based on neural superposition. UtilizingDrosophilaandTriboliumas representatives of fused and open rhabdom morphology in holometabolous insects respectively, we identified three changes required for this innovation to occur. First, the expression pattern of the extracellular matrix protein Eyes Shut (EYS) was co-opted and expanded from mechanosensory neurons to photoreceptor cells in taxa with open rhabdoms. Second, EYS homologs obtained a novel extension of the amino terminus leading to the internalization of a cleaved signal sequence. This amino terminus extension does not interfere with cleavage or function in mechanosensory neurons, but it does permit specific targeting of the EYS protein to the apical photoreceptor membrane. Finally, a specific interaction evolved between EYS and a subset of Prominin homologs that is required for the development of open, but not fused, rhabdoms. Together, our findings portray a case study wherein the evolution of a set of molecular novelties has precipitated the origin of an adaptive photoreceptor cell arrangement.