Molecular logic behind the three-way stochastic choices that expand butterfly colour vision.

Molecular logic behind the three-way stochastic choices that expand butterfly colour vision.
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DOI:
10.1038/nature18616
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发表时间:
2016-07-14
期刊:
影响因子:
64.8
通讯作者:
Desplan C
Desplan C
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Perry M;Kinoshita M;Saldi G;Huo L;Arikawa K;Desplan C

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蝴蝶广泛依赖颜色视觉来适应自然界。大多数物种在三种随机分布的小眼(单位眼)中表达广泛的颜色敏感视紫红质。果蝇的视网膜只有两种主要类型,其中命运由二元随机决定控制,在R7感光细胞中表达转录因子无刺(SS)。我们调查了蝴蝶是如何产生三种随机分布的小眼类型的,导致了更多样化的视网膜马赛克,这为额外的颜色比较和扩大的颜色视觉范围提供了基础。我们发现,日本黄燕尾(Papilio xutus,Papilionidae)和彩蝶(Vanessa cardui,Nymphalidae)在每个小眼内都有第二个R7样光感受器。在每个R7样细胞中,SS的独立随机表达导致蓝色(SS-ON)或UV(SS-OFF)视紫红质的表达。在Papilio中,两个R7中的Blue/Blue、Blue/UV或UV/UV的这些选择与其余光感受器中额外的视紫红质的表达相协调,共同定义了三种类型的小眼。使用CRISPR/Cas9敲除ss导致R7样细胞中蓝色命运的丢失,并将视网膜转换为UV/UV型小眼的均质区域,具有所有相应的特征。因此,SS表达的三种可能结果决定了蝴蝶的三种小眼类型。这种发育策略允许在Papilio中部署另一种对红色敏感的视紫红质,从而允许扩展的颜色视觉与更丰富的受体种类一起进化。这一机制出奇地简单,它利用两个二元随机决定,再加上地方协调,可能被证明是产生更多多样化发展成果的一般手段。
Butterflies rely on color vision extensively to adapt to the natural world. Most species express a broad range of color sensitive Rhodopsins in three stochastically distributed types of ommatidia (unit eyes). The retinas of Drosophila deploy just two main types, where fate is controlled by the binary stochastic decision to express the transcription factor Spineless (Ss) in R7 photoreceptors. We investigated how butterflies instead generate three stochastically distributed ommatidial types, resulting in a more diverse retinal mosaic that provides the basis for additional color comparisons and an expanded range of color vision. We show that the Japanese Yellow Swallowtail (Papilio xuthus, Papilionidae) and the Painted Lady (Vanessa cardui, Nymphalidae) have a second R7-like photoreceptor in each ommatidium. Independent stochastic expression of Ss in each R7-like cell results in expression of a Blue (Ss-ON) or a UV (Ss-OFF) Rhodopsin. In Papilio, these choices of Blue/Blue, Blue/UV, or UV/UV in the two R7s are coordinated with expression of additional Rhodopsins in the remaining photoreceptors, and together define the three types of ommatidia. Knocking out ss using CRISPR/Cas9 leads to the loss of the Blue fate in R7-like cells and transforms retinas into homogeneous fields of UV/UV-type ommatidia, with all corresponding features. Hence, the three possible outcomes of Ss expression define the three ommatidial types in butterflies. This developmental strategy allowed the deployment of an additional red-sensitive Rhodopsin in Papilio, allowing for the evolution of expanded color vision with a richer variety of receptors. This surprisingly simple mechanism that makes use of two binary stochastic decisions coupled with local coordination may prove to be a general means of generating an increased diversity of developmental outcomes.