title: Dual and Opposing Roles of Xanthine Dehydrogenase in Defense-Associated Reactive Oxygen Species Metabolism in Arabidopsis.
abstract: 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.
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850 Hunan Provincial Key Laboratory for Germplasm Innovation and Utilization of Crop, Hunan Agricultural University, Changsha 410128, China Rice Research Institute, Sichuan Agricultural University, Chengdu 611130, China.
authors.forename: Xianfeng
authors.initials: X
authors.lastname: Ma
authors.affiliation: Rice Research Institute, Sichuan Agricultural University, Chengdu 611130, China.
authors.forename: Wenming
authors.identifier: 0000-0003-4066-4875
authors.initials: W
authors.lastname: Wang
authors.affiliation: Department of Plant Biology, Braunschweig University of Technology, 38106 Braunschweig, Germany.
authors.forename: Florian
authors.identifier: 0000-0002-3450-2354
authors.initials: F
authors.lastname: Bittner
authors.affiliation: Department of Plant Biology, Braunschweig University of Technology, 38106 Braunschweig, Germany.
authors.forename: Nadine
authors.initials: N
authors.lastname: Schmidt
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850.
authors.forename: Robert
authors.initials: R
authors.lastname: Berkey
authors.affiliation: Rice Research Institute, Sichuan Agricultural University, Chengdu 611130, China.
authors.forename: Lingli
authors.initials: L
authors.lastname: Zhang
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850.
authors.forename: Harlan
authors.initials: H
authors.lastname: King
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850.
authors.forename: Yi
authors.identifier: 0000-0002-1566-098X
authors.initials: Y
authors.lastname: Zhang
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850 College of Horticulture, Northwest A&F University, Yangling 712100, China.
authors.forename: Jiayue
authors.initials: J
authors.lastname: Feng
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850 College of Horticulture, Northwest A&F University, Yangling 712100, China.
authors.forename: Yinqiang
authors.initials: Y
authors.lastname: Wen
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850.
authors.forename: Liqiang
authors.initials: L
authors.lastname: Tan
authors.affiliation: Department of Chemistry and Biochemistry, University of Maryland, College Park, Maryland 20742.
authors.forename: Yue
authors.initials: Y
authors.lastname: Li
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850.
authors.forename: Qiong
authors.initials: Q
authors.lastname: Zhang
authors.affiliation: Hunan Provincial Key Laboratory for Germplasm Innovation and Utilization of Crop, Hunan Agricultural University, Changsha 410128, China.
authors.forename: Ziniu
authors.identifier: 0000-0002-7791-798X
authors.initials: Z
authors.lastname: Deng
authors.affiliation: Hunan Provincial Key Laboratory for Germplasm Innovation and Utilization of Crop, Hunan Agricultural University, Changsha 410128, China The Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences, Beijing 100081, China xiongxy@hunau.net xiao@umd.edu.
authors.forename: Xingyao
authors.initials: X
authors.lastname: Xiong
authors.affiliation: Institute of Biosciences and Biotechnology Research and Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20850 xiongxy@hunau.net xiao@umd.edu.
authors.forename: Shunyuan
authors.identifier: 0000-0003-1348-4879
authors.initials: S
authors.lastname: Xiao
mesh_terms: D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics / Q000378:metabolism* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001203:Ascomycota / Q000472:pathogenicity; D060467:Disease Resistance / Q000235:genetics / Q000502:physiology; D054884:Host-Pathogen Interactions / Q000235:genetics / Q000502:physiology; D010935:Plant Diseases / Q000382:microbiology; D017382:Reactive Oxygen Species / Q000378:metabolism; D014968:Xanthine Dehydrogenase / Q000235:genetics / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; D017382:Reactive Oxygen Species; D014968:Xanthine Dehydrogenase