Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae

Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae
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DOI:
10.1073/pnas.1706865114
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发表时间:
2017-07-18
影响因子:
11.1
通讯作者:
Van Leeuwen, Thomas
Van Leeuwen, Thomas
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Bryon, Astrid;Kurlovs, Andre H.;Van Leeuwen, Thomas

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类胡萝卜素是动物体内​​许多鲜艳的黄色、橙色和红色的基础,并参与从视觉到免受压力的保护等过程。大多数动物从饮食中获取类胡萝卜素,因为类胡萝卜素的从头合成主要限于植物以及一些细菌和真菌。最近,蚜虫、蚜虫、红蜘蛛和瘿蚊的测序项目鉴定出与编码八氢番茄红素去饱和酶等类胡萝卜素生物合成蛋白的真菌序列同源的基因。类胡萝卜素生物合成基因向三个节肢动物谱系的水平基因转移的发现是前所未有的;然而,转移对于获得它们的节肢动物的相关性在很大程度上仍然是推测性的,对于以植物细胞内容物(已知的类胡萝卜素来源)为食的叶螨来说尤其如此。叶螨的色素沉着完全由类胡萝卜素引起。通过结合遗传方法,我们发现单个水平转移的八氢番茄红素去饱和酶的突变会导致二斑叶螨(Tetranychus urticae)以及柑橘红螨(Panonychus citri)的完全白化病。此外,我们还发现八氢番茄红素去饱和酶活性对于二斑玳瑁越冬菌株滞育的光周期诱导至关重要,这与该酶在提供光感知所需的维生素原 A 类胡萝卜素中的作用一致。因此,真菌来源的类胡萝卜素生物合成基因使一些螨虫能够放弃饮食中的类胡萝卜素,内源合成是其强烈色素沉着和进入滞育能力的基础,这是主要农业红蜘蛛害虫全球分布的关键。
Carotenoids underlie many of the vibrant yellow, orange, and red colors in animals, and are involved in processes ranging from vision to protection from stresses. Most animals acquire carotenoids from their diets because de novo synthesis of carotenoids is primarily limited to plants and some bacteria and fungi. Recently, sequencing projects in aphids and adelgids, spider mites, and gall midges identified genes with homology to fungal sequences encoding de novo carotenoid biosynthetic proteins like phytoene desaturase. The finding of horizontal gene transfers of carotenoid biosynthetic genes to three arthropod lineages was unprecedented; however, the relevance of the transfers for the arthropods that acquired them has remained largely speculative, which is especially true for spider mites that feed on plant cell contents, a known source of carotenoids. Pigmentation in spider mites results solely from carotenoids. Using a combination of genetic approaches, we show that mutations in a single horizontally transferred phytoene desaturase result in complete albinism in the two-spotted spider mite, Tetranychus urticae, as well as in the citrus red mite, Panonychus citri. Further, we show that phytoene desaturase activity is essential for photoperiodic induction of diapause in an overwintering strain of T. urticae, consistent with a role for this enzyme in provisioning provitamin A carotenoids required for light perception. Carotenoid biosynthetic genes of fungal origin have therefore enabled some mites to forgo dietary carotenoids, with endogenous synthesis underlying their intense pigmentation and ability to enter diapause, a key to the global distribution of major spider mite pests of agriculture.