Magnaporthe oryzae nucleoside diphosphate kinase is required for metabolic homeostasis and redox-mediated host innate immunity suppression.,Molecular Microbiology

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Magnaporthe oryzae nucleoside diphosphate kinase is required for metabolic homeostasis and redox-mediated host innate immunity suppression.
Molecular Microbiology ( IF 2.6 ) Pub Date : 2020-09-16 , DOI: 10.1111/mmi.14580
Raquel O Rocha ₁ , Richard A Wilson ₁

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The fungus Magnaporthe oryzae causes blast, the most devastating disease of cultivated rice. After penetrating the leaf cuticle, M. oryzae grows as a biotroph in intimate contact with living rice epidermal cells before necrotic lesions develop. Biotrophic growth requires maintaining metabolic homeostasis while suppressing plant defenses, but the metabolic connections and requirements involved are largely unknown. Here, we characterized the M. oryzae nucleoside diphosphate kinase‐encoding gene NDK1 and discovered it was essential for facilitating biotrophic growth by suppressing the host oxidative burst—the first line of plant defense. NDK enzymes reversibly transfer phosphate groups from tri‐ to diphosphate nucleosides. Correspondingly, intracellular nucleotide pools were perturbed in M. oryzae strains lacking NDK1 through targeted gene deletion, compared to WT. This affected metabolic homeostasis: TCA, purine and pyrimidine intermediates, and oxidized NADP⁺, accumulated in Δndk1. cAMP and glutathione were depleted. ROS accumulated in Δndk1 hyphae. Functional appressoria developed on rice leaf sheath surfaces, but Δndk1 invasive hyphal growth was restricted and redox homeostasis was perturbed, resulting in unsuppressed host oxidative bursts that triggered immunity. We conclude Ndk1 modulates intracellular nucleotide pools to maintain redox balance via metabolic homeostasis, thus quenching the host oxidative burst and suppressing rice innate immunity during biotrophy.

中文翻译：

Magnaporthe oryzae 核苷二磷酸激酶是代谢稳态和氧化还原介导的宿主先天免疫抑制所必需的。

真菌Magnaporthe oryzae会引起稻瘟病，这是栽培水稻中最具破坏性的病害。穿透叶表皮后，米曲霉作为生物营养物生长，在坏死病变发展之前与活的水稻表皮细胞密切接触。生物营养生长需要在抑制植物防御的同时维持代谢稳态，但所涉及的代谢联系和要求在很大程度上是未知的。在这里，我们表征了米曲霉核苷二磷酸激酶编码基因NDK1并发现它对于通过抑制宿主氧化爆发（植物防御的第一道防线）来促进生物营养生长至关重要。NDK 酶可逆地将磷酸基团从三磷酸核苷转移到二磷酸核苷。相应地，与 WT 相比，通过靶向基因缺失，在缺乏NDK1 的米曲霉菌株中细胞内核苷酸库受到干扰。这影响了代谢稳态：TCA、嘌呤和嘧啶中间体以及氧化的 NADP ⁺，在 Δ ndk1 中积累。cAMP 和谷胱甘肽被耗尽。ROS在Δndk1菌丝中积累。在水稻叶鞘表面发育的功能性压抑菌，但Δndk1侵入性菌丝生长受到限制，氧化还原稳态受到干扰，导致不受抑制的宿主氧化爆发引发免疫。我们得出结论，Ndk1 通过代谢稳态调节细胞内核苷酸库以维持氧化还原平衡，从而在生物营养期间抑制宿主氧化爆发并抑制水稻先天免疫。

更新日期：2020-09-16

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