Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection.

Identification and characterisation of serotonin signalling in the potato cyst nematode Globodera pallida reveals new targets for crop protection.
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DOI:
10.1371/journal.ppat.1008884
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发表时间:
2020-10
期刊:
影响因子:
6.7
通讯作者:
Holden-Dye L
Holden-Dye L
中科院分区:
医学1区
文献类型:
--
作者:
Crisford A;Calahorro F;Ludlow E;Marvin JMC;Hibbard JK;Lilley CJ;Kearn J;Keefe F;Johnson P;Harmer R;Urwin PE;O'Connor V;Holden-Dye L

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植物寄生线虫是一种侵袭植物根部并对作物造成广泛危害的微小病原体。我们使用化学生物学的方法来定义它们寄生行为的机制:我们发现利血平,一种抑制囊泡单胺转运蛋白(VMAT)的植物生物碱,有效地削弱了马铃薯孢囊线虫Globodera pallida进入寄主植物根的能力。我们证明这是由于5-羟色胺能信号的抑制,而5-羟色胺能信号是激活用于访问宿主根的口针所必需的。受此启发,我们确定了包括利血平靶标VMAT、5-羟色胺合成酶、G蛋白偶联受体SER-7和5-羟色胺门控氯离子通道MOD-1的苍白球藻5-羟色胺信号的核心分子成分。我们克隆了这些分子中的每一个,并通过与相应的线虫突变体互补来确认它们的功能同一性,从而绘制出了苍白线虫的5-羟色胺能信号。测试这些信号分子中每一个的化学抑制剂对寄生和根入侵所需的离散亚行为的影响的补充方法加强了5-羟色胺的关键作用。因此,靶向5-羟色胺信号通路为防治植物寄生线虫提供了一条很有前途的新途径。印度蛇根是一种草药,由灌木劳沃菲亚蛇的根制成,几个世纪以来一直被用于镇静作用。我们发现蛇根的主要活性成分利血平是一种潜在的强大的作物保护剂,因为它保护植物的根免受微小的植物寄生线虫的攻击。利血平的药理作用众所周知:它通过消耗神经系统中一种特定的情绪调节化学物质生物胺来发挥作用。我们发现,在线虫中,利血平禁用了生物胺信号,而胺5-羟色胺的丢失则停止了寄生生命周期。我们在土豆胞囊线虫Globodera pallida中确定了5-羟色胺信号通路的关键成分,并表明针对这些位置的化学物质也抑制了线虫入侵其宿主植物的能力。因此,天然存在的植物根部生物碱利血平为作物保护提供了新的靶点。
Plant parasitic nematodes are microscopic pathogens that invade plant roots and cause extensive damage to crops. We have used a chemical biology approach to define mechanisms underpinning their parasitic behaviour: We discovered that reserpine, a plant alkaloid that inhibits the vesicular monoamine transporter (VMAT), potently impairs the ability of the potato cyst nematode Globodera pallida to enter the host plant root. We show this is due to an inhibition of serotonergic signalling that is essential for activation of the stylet which is used to access the host root. Prompted by this we identified core molecular components of G. pallida serotonin signalling encompassing the target of reserpine, VMAT; the synthetic enzyme for serotonin, tryptophan hydroxylase; the G protein coupled receptor SER-7 and the serotonin-gated chloride channel MOD-1. We cloned each of these molecular components and confirmed their functional identity by complementation of the corresponding C. elegans mutant thus mapping out serotonergic signalling in G. pallida. Complementary approaches testing the effect of chemical inhibitors of each of these signalling elements on discrete sub-behaviours required for parasitism and root invasion reinforce the critical role of serotonin. Thus, targeting the serotonin signalling pathway presents a promising new route to control plant parasitic nematodes. Indian snakeroot is an herbal medicine prepared from the roots of the shrub Rauwolfia serpentina that has been used for centuries for its calming action. We have found that the major active constituent of snakeroot, reserpine, is a potentially powerful crop protectant as it protects the roots of plants from attack by microscopic plant parasitic nematodes. The pharmacology of reserpine is well known: it works by depleting a specific class of mood regulating chemical in the nervous system, the biogenic amines. We show that in the nematode, reserpine disables biogenic amine signalling and that loss of the amine serotonin halts the parasitic life cycle. We identified key components of the serotonin signalling pathway in the potato cyst nematode Globodera pallida and show that chemicals that target these sites also inhibit the ability of the nematode to invade its host plant. Therefore, the naturally occurring plant root alkaloid reserpine has provided insight into new targets for crop protection.