Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea

Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea
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DOI:
10.1111/j.1365-313x.2009.03912.x
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发表时间:
2009-09-01
期刊:
影响因子:
7.2
通讯作者:
Draper, John
Draper, John
中科院分区:
生物学1区
文献类型:
--
作者:
Parker, David;Beckmann, Manfred;Draper, John

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生物营养和半生物营养真菌病原体同时抑制植物防御和隔离宿主营养的机制尚不清楚。利用代谢物指纹图谱,我们发现稻瘟病的致病因子稻瘟病病菌(Magnaporthe grisea)在植物定植过程中动态地重新编程寄主代谢。稻瘟病菌在大麦、水稻和短茅中感染时,代谢变化的模式相同。GC-MS的目标代谢物分析证实了一组保守代谢物的调节。在症状前的组织中,苹果酸盐和多胺积累,而不是被用来产生防御性活性氧,并且与氧化还原应激改善相关的代谢物水平在各细胞区室中急剧增加。nadp -苹果酸酶的活性和活性氧的产生都局限于病原体的渗透位点,并且在相容相互作用中都被抑制。观察到草酸途径产生奎宁酸的早期转移,以及非聚合木质素前体的积累。这些数据与稻瘟病杆菌对防御性苯丙素代谢的调节以及易感宿主无法产生超敏反应或产生木质化乳头(两者都涉及活性氧)来限制病原体入侵的观点一致。稻瘟病菌菌丝3天后在植物组织中的快速增殖与该病原菌对营养物质的获取和利用加快有关。将光同化物转化为甘露醇和甘油用于固碳和渗透物的生产似乎可以推动菌丝的生长。综上所述,我们的研究结果表明真菌病原体在不同的寄主物种中采用共同的代谢重编程策略来抑制植物防御并定植植物组织。
The mechanisms by which biotrophic and hemi-biotrophic fungal pathogens simultaneously subdue plant defences and sequester host nutrients are poorly understood. Using metabolite fingerprinting, we show that Magnaporthe grisea, the causal agent of rice blast disease, dynamically re-programmes host metabolism during plant colonization. Identical patterns of metabolic change occurred during M. grisea infections in barley, rice and Brachypodium distachyon. Targeted metabolite profiling by GC-MS confirmed the modulation of a conserved set of metabolites. In pre-symptomatic tissues, malate and polyamines accumulated, rather than being utilized to generate defensive reactive oxygen species, and the levels of metabolites associated with amelioration of redox stress in various cellular compartments increased dramatically. The activity of NADP-malic enzyme and generation of reactive oxygen species were localized to pathogen penetration sites, and both appeared to be suppressed in compatible interactions. Early diversion of the shikimate pathway to produce quinate was observed, as well as accumulation of non-polymerized lignin precursors. These data are consistent with modulation of defensive phenylpropanoid metabolism by M. grisea and the inability of susceptible hosts to mount a hypersensitive reaction or produce lignified papillae (both involving reactive oxygen species) to restrict pathogen invasion. Rapid proliferation of M. grisea hyphae in plant tissue after 3 days was associated with accelerated nutrient acquisition and utilization by the pathogen. Conversion of photoassimilate into mannitol and glycerol for carbon sequestration and osmolyte production appear to drive hyphal growth. Taken together, our results suggest that fungal pathogens deploy a common metabolic re-programming strategy in diverse host species to suppress plant defence and colonize plant tissue.