Shimoda Marine Research Center, University of Tsukuba, Shimoda, Japan.
PRESTO, JST, Kawaguchi, Japan.
PLoS Genet. 2022 Feb 10;18(2):e1010033. doi: 10.1371/journal.pgen.1010033. eCollection 2022 Feb.
To survive, organisms need to precisely respond to various environmental factors, such as light and gravity. Among these, light is so important for most life on Earth that light-response systems have become extraordinarily developed during evolution, especially in multicellular animals. A combination of photoreceptors, nervous system components, and effectors allows these animals to respond to light stimuli. In most macroscopic animals, muscles function as effectors responding to light, and in some microscopic aquatic animals, cilia play a role. It is likely that the cilia-based response was the first to develop and that it has been substituted by the muscle-based response along with increases in body size. However, although the function of muscle appears prominent, it is poorly understood whether ciliary responses to light are present and/or functional, especially in deuterostomes, because it is possible that these responses are too subtle to be observed, unlike muscle responses. Here, we show that planktonic sea urchin larvae reverse their swimming direction due to the inhibitory effect of light on the cholinergic neuron signaling>forward swimming pathway. We found that strong photoirradiation of larvae that stay on the surface of seawater immediately drives the larvae away from the surface due to backward swimming. When Opsin2, which is expressed in mesenchymal cells in larval arms, is knocked down, the larvae do not show backward swimming under photoirradiation. Although Opsin2-expressing cells are not neuronal cells, immunohistochemical analysis revealed that they directly attach to cholinergic neurons, which are thought to regulate forward swimming. These data indicate that light, through Opsin2, inhibits the activity of cholinergic signaling, which normally promotes larval forward swimming, and that the light-dependent ciliary response is present in deuterostomes. These findings shed light on how light-responsive tissues/organelles have been conserved and diversified during evolution.
为了生存,生物需要精确地响应各种环境因素,如光和重力。在这些因素中,光对地球上的大多数生命来说非常重要,以至于光反应系统在进化过程中变得异常发达,尤其是在多细胞动物中。光感受器、神经系统成分和效应器的组合使这些动物能够对光刺激做出反应。在大多数宏观动物中,肌肉作为对光做出反应的效应器发挥作用,而在一些微观水生动物中,纤毛则发挥作用。很可能是基于纤毛的反应首先发展起来的,并且随着体型的增大,它已经被基于肌肉的反应所取代。然而,尽管肌肉的功能似乎很突出,但人们对光引起的纤毛反应是否存在和/或起作用知之甚少,特别是在后口动物中,因为这些反应可能太微妙而无法观察到,不像肌肉反应。在这里,我们表明浮游海胆幼虫由于光对胆碱能神经元信号传导的抑制作用而改变其游动方向>向前游动途径。我们发现,强烈的光照射停留在海水面上的幼虫会立即导致幼虫向后游动而远离水面。当在幼虫臂中的间质细胞中表达的 Opsin2 被敲低时,幼虫在光照射下不会表现出向后游动。尽管 Opsin2 表达细胞不是神经元细胞,但免疫组织化学分析显示它们直接附着于被认为调节向前游动的胆碱能神经元。这些数据表明,光通过 Opsin2 抑制了通常促进幼虫向前游动的胆碱能信号传导的活性,并且光依赖性纤毛反应存在于后口动物中。这些发现揭示了在进化过程中,光反应组织/细胞器是如何被保守和多样化的。