Dual and Opposing Roles of Xanthine Dehydrogenase in Defense-Associated Reactive Oxygen Species Metabolism in Arabidopsis

Dual and Opposing Roles of Xanthine Dehydrogenase in Defense-Associated Reactive Oxygen Species Metabolism in Arabidopsis
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DOI:
10.1105/tpc.15.00880
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发表时间:
2016-05-01
期刊:
影响因子:
11.6
通讯作者:
Xiao, Shunyuan
Xiao, Shunyuan
中科院分区:
生物学1区
文献类型:
--
作者:
Ma, Xianfeng;Wang, Wenming;Xiao, Shunyuan

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虽然植物产生活性氧(ROS)用于胁迫信号传导和病原体防御,但它们需要去除在胁迫反应期间诱导的过量ROS以最小化氧化损伤。植物如何调整这种平衡,满足这种相互冲突的需求呢?在这里,我们表明,黄嘌呤脱氢酶1(XDH1)在拟南芥似乎发挥空间相反的作用,以达到这一目的。通过大规模的遗传筛选,我们确定了三个错义突变XDH1损害XDH1的酶功能,从而影响由抗白粉病8(RPW8)介导的白粉病抗性在表皮细胞和叶肉细胞中形成富含黄嘌呤的自发荧光物体。进一步的分析表明,在叶表皮细胞中,XDH 1可能作为氧化酶,沿着NADPH氧化酶RbohD和RbohF,产生超氧化物,超氧化物歧化为H2O2。由此产生的丰富的H2O2在真菌吸器复合物内感染的表皮细胞有助于限制吸器,从而有助于RPW8依赖性和RPW8独立的白粉病抗性。相比之下,在叶肉细胞中,XDH 1进行黄嘌呤脱氢酶活性,在局部和系统组织中产生尿酸,以从胁迫叶绿体中除去H2O2,从而保护植物免受胁迫诱导的氧化损伤。因此,XDH1在拟南芥防御反应中起着空间特异性的双重和相反的作用,调节ROS代谢。
While plants produce reactive oxygen species (ROS) for stress signaling and pathogen defense, they need to remove excessive ROS induced during stress responses in order to minimize oxidative damage. How can plants fine-tune this balance and meet such conflicting needs? Here, we show that XANTHINE DEHYDROGENASE1 (XDH1) in Arabidopsis thaliana appears to play spatially opposite roles to serve this purpose. Through a large-scale genetic screen, we identified three missense mutations in XDH1 that impair XDH1's enzymatic functions and consequently affect the powdery mildew resistance mediated by RESISTANCE TO POWDERY MILDEW8 (RPW8) in epidermal cells and formation of xanthine-enriched autofluorescent objects in mesophyll cells. Further analyses revealed that in leaf epidermal cells, XDH1 likely functions as an oxidase, along with the NADPH oxidases RbohD and RbohF, to generate superoxide, which is dismutated into H2O2. The resulting enrichment of H2O2 in the fungal haustorial complex within infected epidermal cells helps to constrain the haustorium, thereby contributing to RPW8-dependent and RPW8-independent powdery mildew resistance. By contrast, in leaf mesophyll cells, XDH1 carries out xanthine dehydrogenase activity to produce uric acid in local and systemic tissues to scavenge H2O2 from stressed chloroplasts, thereby protecting plants from stress-induced oxidative damage. Thus, XDH1 plays spatially specified dual and opposing roles in modulation of ROS metabolism during defense responses in Arabidopsis.