Department of Biology, The University of Western Ontario, London, Ontario, Canada N6A 5B7.
Instituto de Bioquímica Vegetal y Fotosíntesis, Consejo Superior de Investigaciones Científicas and Universidad de Sevilla, E-41092 Seville, Spain.
Plant Physiol. 2022 Aug 1;189(4):1961-1975. doi: 10.1093/plphys/kiac147.
Glucosinolates are antiherbivory chemical defense compounds in Arabidopsis (Arabidopsis thaliana). Specialist herbivores that feed on brassicaceous plants have evolved various mechanisms aimed at preventing the formation of toxic isothiocyanates. In contrast, generalist herbivores typically detoxify isothiocyanates through glutathione conjugation upon exposure. Here, we examined the response of an extreme generalist herbivore, the two-spotted spider mite Tetranychus urticae (Koch), to indole glucosinolates. Tetranychus urticae is a composite generalist whose individual populations have a restricted host range but have an ability to rapidly adapt to initially unfavorable plant hosts. Through comparative transcriptomic analysis of mite populations that have differential susceptibilities to Arabidopsis defenses, we identified β-cyanoalanine synthase of T. urticae (TuCAS), which encodes an enzyme with dual cysteine and β-cyanoalanine synthase activities. We combined Arabidopsis genetics, chemical complementation and mite reverse genetics to show that TuCAS is required for mite adaptation to Arabidopsis through its β-cyanoalanine synthase activity. Consistent with the β-cyanoalanine synthase role in detoxification of hydrogen cyanide (HCN), we discovered that upon mite herbivory, Arabidopsis plants release HCN. We further demonstrated that indole glucosinolates are sufficient for cyanide formation. Overall, our study uncovered Arabidopsis defenses that rely on indole glucosinolate-dependent cyanide for protection against mite herbivory. In response, Arabidopsis-adapted mites utilize the β-cyanoalanine synthase activity of TuCAS to counter cyanide toxicity, highlighting the mite's ability to activate resistant traits that enable this extreme polyphagous herbivore to exploit cyanogenic host plants.
硫代葡萄糖苷是拟南芥（Arabidopsis thaliana）中抗草食性的化学防御化合物。以十字花科植物为食的专食性草食动物进化出了各种机制，旨在防止有毒的异硫氰酸酯的形成。相比之下，一般的草食动物通常在暴露于异硫氰酸酯时通过谷胱甘肽结合来解毒。在这里，我们研究了一种极端的泛食性草食动物——二斑叶螨（Tetranychus urticae（Koch））对吲哚硫代葡萄糖苷的反应。二斑叶螨是一种复合的泛食性动物，其个体种群的寄主范围有限，但具有迅速适应最初不利的植物寄主的能力。通过对具有不同拟南芥防御能力的螨种群的比较转录组分析，我们鉴定出二斑叶螨的β-氰基丙氨酸合酶（TuCAS），它编码一种具有双半胱氨酸和β-氰基丙氨酸合酶活性的酶。我们结合拟南芥遗传学、化学互补和螨反向遗传学表明，TuCAS 通过其β-氰基丙氨酸合酶活性对螨适应拟南芥是必需的。与β-氰基丙氨酸合酶在氰化氢（HCN）解毒中的作用一致，我们发现，在螨取食后，拟南芥植物会释放 HCN。我们进一步证明，吲哚硫代葡萄糖苷足以形成氰化物。总的来说，我们的研究揭示了依赖吲哚硫代葡萄糖苷依赖氰化物来保护植物免受螨类取食的拟南芥防御机制。作为回应，适应拟南芥的螨虫利用 TuCAS 的β-氰基丙氨酸合酶活性来对抗氰化物毒性，这突出了螨虫激活抗性特征的能力，使这种极端的多食性草食动物能够利用含氰基的寄主植物。
