title: Loss of ceramide kinase in Arabidopsis impairs defenses and promotes ceramide accumulation and mitochondrial H2O2 bursts.
abstract: Arabidopsis thaliana plants that lack ceramide kinase, encoded by ACCELERATED CELL DEATH5 (ACD5), display spontaneous programmed cell death late in development and accumulate substrates of ACD5. Here, we compared ceramide accumulation kinetics, defense responses, ultrastructural features, and sites of reactive oxygen species (ROS) production in wild-type and acd5 plants during development and/or Botrytis cinerea infection. Quantitative sphingolipid profiling indicated that ceramide accumulation in acd5 paralleled the appearance of spontaneous cell death, and it was accompanied by autophagy and mitochondrial ROS accumulation. Plants lacking ACD5 differed significantly from the wild type in their responses to B. cinerea, showing earlier and higher increases in ceramides, greater disease, smaller cell wall appositions (papillae), reduced callose deposition and apoplastic ROS, and increased mitochondrial ROS. Together, these data show that ceramide kinase greatly affects sphingolipid metabolism and the site of ROS accumulation during development and infection, which likely explains the developmental and infection-related cell death phenotypes. The acd5 plants also showed an early defect in restricting B. cinerea germination and growth, which occurred prior to the onset of cell death. This early defect in B. cinerea restriction in acd5 points to a role for ceramide phosphate and/or the balance of ceramides in mediating early antifungal responses that are independent of cell death.
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Fang-Cheng
authors.initials: FC
authors.lastname: Bi
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Zhe
authors.initials: Z
authors.lastname: Liu
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Jian-Xin
authors.initials: JX
authors.lastname: Wu
authors.affiliation: Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, Illinois 60637.
authors.forename: Hua
authors.initials: H
authors.lastname: Liang
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Xue-Li
authors.initials: XL
authors.lastname: Xi
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Ce
authors.initials: C
authors.lastname: Fang
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Tie-Jun
authors.initials: TJ
authors.lastname: Sun
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Jian
authors.initials: J
authors.lastname: Yin
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Guang-Yi
authors.initials: GY
authors.lastname: Dai
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Chan
authors.initials: C
authors.lastname: Rong
authors.affiliation: Department of Molecular Genetics and Cell Biology, The University of Chicago, Chicago, Illinois 60637.
authors.forename: Jean T
authors.initials: JT
authors.lastname: Greenberg
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China.
authors.forename: Wei-Wei
authors.initials: WW
authors.lastname: Su
authors.affiliation: State Key Laboratory of Biocontrol, Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, P.R. China yaonan@mail.sysu.edu.cn.
authors.forename: Nan
authors.identifier: http://orcid.org/0000-0002-2045-5462
authors.initials: N
authors.lastname: Yao
mesh_terms: D017209:Apoptosis / Q000235:genetics; D017360:Arabidopsis / Q000235:genetics / Q000276:immunology / Q000378:metabolism* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D001343:Autophagy; D020171:Botrytis / Q000276:immunology / Q000502:physiology; D002518:Ceramides / Q000096:biosynthesis*; D006861:Hydrogen Peroxide / Q000378:metabolism*; D007700:Kinetics; D008928:Mitochondria / Q000378:metabolism*; D017853:Phosphotransferases (Alcohol Group Acceptor) / Q000235:genetics / Q000378:metabolism / Q000502:physiology*; D017382:Reactive Oxygen Species / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D002518:Ceramides; D017382:Reactive Oxygen Species; D006861:Hydrogen Peroxide; D017853:Phosphotransferases (Alcohol Group Acceptor); C000598951:ACD5 protein, Arabidopsis