(Homo)glutathione deficiency impairs root-knot nematode development in Medicago truncatula.

(Homo)glutathione deficiency impairs root-knot nematode development in Medicago truncatula.
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DOI:
10.1371/journal.ppat.1002471
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发表时间:
2012-01
期刊:
影响因子:
6.7
通讯作者:
Frendo P
Frendo P
中科院分区:
医学1区
文献类型:
--
作者:
Baldacci-Cresp F;Chang C;Maucourt M;Deborde C;Hopkins J;Lecomte P;Bernillon S;Brouquisse R;Moing A;Abad P;Hérouart D;Puppo A;Favery B;Frendo P

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根结线虫(RKN)是必需的植物寄生蠕虫,与寄主植物建立并维持密切的关系。在相容的相互作用过程中,RKN 诱导根细胞再分化为线虫生长和繁殖所必需的多核和肥大的巨细胞。这些代谢活跃的摄食细胞构成了线虫的唯一营养来源。谷胱甘肽 (GSH) 和高谷胱甘肽 (hGSH) 代谢的详细分析证明了这些化合物对于蒺藜苜蓿线虫感染成功的重要性。我们报道了 GSH 和 hGSH 的定量以及基因表达分析,表明新生胆器官中的 (h)GSH 代谢与未感染根中的不同。 (h)GSH 含量的耗尽会损害线虫卵团的形成并改变性别比例。此外,基因表达和代谢组学分析表明,(h)GSH 耗尽的虫瘿中淀粉和 γ-氨基丁酸代谢以及苹果酸和葡萄糖含量发生了显着改变。有趣的是,这些修饰并未发生在 (h)GSH 耗尽的根中。这些不同的结果表明,(h)GSH 在巨细胞代谢的调节中具有关键作用。这些特定植物调控元件的发现可能会导致针对线虫的新害虫管理策略的开发。寄生线虫是引起植物、动物和人类重大疾病的微小蠕虫。在相容性相互作用过程中,根结线虫(RKN)诱导虫瘿的形成,其中根细胞重新分化为多核和肥大的巨细胞对于线虫的生长和繁殖至关重要。谷胱甘肽 (GSH) 是一种参与植物发育、植物微生物相互作用和非生物胁迫反应的主要抗氧化剂分子,在植物与 RKN 相互作用过程中对其重要性进行了分析。我们的分析表明,虫瘿发育和功能的特点是适应谷胱甘肽代谢,谷胱甘肽含量的消耗会损害线虫的繁殖和性别比例的改变。这种表型与碳代谢的特定改变有关,这种改变不会发生在未感染的根中,表明这种新形成的器官具有特殊的代谢。植物与 RKN 相互作用过程中的首次代谢组学分析强调了 GSH 在这种致病相互作用中发挥的调节作用,并完成了我们对 GSH 在植物与病原体相互作用过程中作用的设想。先前在不利的线虫摄食条件下观察到 RKN 性别比例改变,表明 GSH-氧化还原系统可能是自然条件下虫瘿适应性的通用传感器。
Root-knot nematodes (RKN) are obligatory plant parasitic worms that establish and maintain an intimate relationship with their host plants. During a compatible interaction, RKN induce the redifferentiation of root cells into multinucleate and hypertrophied giant cells essential for nematode growth and reproduction. These metabolically active feeding cells constitute the exclusive source of nutrients for the nematode. Detailed analysis of glutathione (GSH) and homoglutathione (hGSH) metabolism demonstrated the importance of these compounds for the success of nematode infection in Medicago truncatula. We reported quantification of GSH and hGSH and gene expression analysis showing that (h)GSH metabolism in neoformed gall organs differs from that in uninfected roots. Depletion of (h)GSH content impaired nematode egg mass formation and modified the sex ratio. In addition, gene expression and metabolomic analyses showed a substantial modification of starch and γ-aminobutyrate metabolism and of malate and glucose content in (h)GSH-depleted galls. Interestingly, these modifications did not occur in (h)GSH-depleted roots. These various results suggest that (h)GSH have a key role in the regulation of giant cell metabolism. The discovery of these specific plant regulatory elements could lead to the development of new pest management strategies against nematodes. Parasitic nematodes are microscopic worms that cause major diseases of plants, animals and humans. During compatible interactions, root-knot nematodes (RKN) induce the formation of galls in which redifferentiation of root cells into multinucleate and hypertrophied giant cells is essential for nematode growth and reproduction. The importance of glutathione (GSH), a major antioxidant molecule involved in plant development, in plant microbe interaction and in abiotic stress response, was analyzed during the plant-RKN interaction. Our analyses demonstrated that the gall development and functioning are characterized by an adapted GSH metabolism and that depletion of GSH content impairs nematode reproduction and modified sex ratio. This phenotype is linked to specific modifications of carbon metabolism which do not occur in uninfected roots indicating a peculiar metabolism of this neoformed organ. This first metabolomic analysis during the plant-RKN interaction highlights the regulatory role played by GSH in this pathogenic interaction and completes our vision of the role of GSH during plant-pathogen interactions. RKN sex ratio modification has previously been observed under unfavorable nematode feeding conditions suggesting that the GSH-redox system could be a general sensor of gall fitness in natural conditions.
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期刊: PHYTOPATHOLOGY
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