title: Modifications of Sphingolipid Content Affect Tolerance to Hemibiotrophic and Necrotrophic Pathogens by Modulating Plant Defense Responses in Arabidopsis.
abstract: Sphingolipids are emerging as second messengers in programmed cell death and plant defense mechanisms. However, their role in plant defense is far from being understood, especially against necrotrophic pathogens. Sphingolipidomics and plant defense responses during pathogenic infection were evaluated in the mutant of long-chain base phosphate (LCB-P) lyase, encoded by the dihydrosphingosine-1-phosphate lyase1 (AtDPL1) gene and regulating long-chain base/LCB-P homeostasis. Atdpl1 mutants exhibit tolerance to the necrotrophic fungus Botrytis cinerea but susceptibility to the hemibiotrophic bacterium Pseudomonas syringae pv tomato (Pst). Here, a direct comparison of sphingolipid profiles in Arabidopsis (Arabidopsis thaliana) during infection with pathogens differing in lifestyles is described. In contrast to long-chain bases (dihydrosphingosine [d18:0] and 4,8-sphingadienine [d18:2]), hydroxyceramide and LCB-P (phytosphingosine-1-phosphate [t18:0-P] and 4-hydroxy-8-sphingenine-1-phosphate [t18:1-P]) levels are higher in Atdpl1-1 than in wild-type plants in response to B. cinerea. Following Pst infection, t18:0-P accumulates more strongly in Atdpl1-1 than in wild-type plants. Moreover, d18:0 and t18:0-P appear as key players in Pst- and B. cinerea-induced cell death and reactive oxygen species accumulation. Salicylic acid levels are similar in both types of plants, independent of the pathogen. In addition, salicylic acid-dependent gene expression is similar in both types of B. cinerea-infected plants but is repressed in Atdpl1-1 after treatment with Pst. Infection with both pathogens triggers higher jasmonic acid, jasmonoyl-isoleucine accumulation, and jasmonic acid-dependent gene expression in Atdpl1-1 mutants. Our results demonstrate that sphingolipids play an important role in plant defense, especially toward necrotrophic pathogens, and highlight a novel connection between the jasmonate signaling pathway, cell death, and sphingolipids.
authors.affiliation: Unité de Recherche Vigne et Vin de Champagne Equipe d'Accueil 4707, Laboratoire Stress Défenses et Reproduction des Plantes, Structure Fédérative de Recherche Condorcet Fédération de Recherche, Centre National de la Recherche Scientifique 3417, Université de Reims Champagne-Ardenne, F-51687 Reims cedex 2, France (M.M.-R., S.D., C.C., F.B., S.D.-C.); andCenter for Plant Science Innovation and Department of Biochemistry, University of Nebraska, Lincoln, Nebraska 68588 (D.L.B., J.M.).
authors.forename: Maryline
authors.initials: M
authors.lastname: Magnin-Robert
authors.affiliation: Unité de Recherche Vigne et Vin de Champagne Equipe d'Accueil 4707, Laboratoire Stress Défenses et Reproduction des Plantes, Structure Fédérative de Recherche Condorcet Fédération de Recherche, Centre National de la Recherche Scientifique 3417, Université de Reims Champagne-Ardenne, F-51687 Reims cedex 2, France (M.M.-R., S.D., C.C., F.B., S.D.-C.); andCenter for Plant Science Innovation and Department of Biochemistry, University of Nebraska, Lincoln, Nebraska 68588 (D.L.B., J.M.).
authors.forename: Doriane
authors.initials: D
authors.lastname: Le Bourse
authors.affiliation: Unité de Recherche Vigne et Vin de Champagne Equipe d'Accueil 4707, Laboratoire Stress Défenses et Reproduction des Plantes, Structure Fédérative de Recherche Condorcet Fédération de Recherche, Centre National de la Recherche Scientifique 3417, Université de Reims Champagne-Ardenne, F-51687 Reims cedex 2, France (M.M.-R., S.D., C.C., F.B., S.D.-C.); andCenter for Plant Science Innovation and Department of Biochemistry, University of Nebraska, Lincoln, Nebraska 68588 (D.L.B., J.M.).
authors.forename: Jonathan
authors.initials: J
authors.lastname: Markham
authors.affiliation: Unité de Recherche Vigne et Vin de Champagne Equipe d'Accueil 4707, Laboratoire Stress Défenses et Reproduction des Plantes, Structure Fédérative de Recherche Condorcet Fédération de Recherche, Centre National de la Recherche Scientifique 3417, Université de Reims Champagne-Ardenne, F-51687 Reims cedex 2, France (M.M.-R., S.D., C.C., F.B., S.D.-C.); andCenter for Plant Science Innovation and Department of Biochemistry, University of Nebraska, Lincoln, Nebraska 68588 (D.L.B., J.M.).
authors.forename: Stéphan
authors.initials: S
authors.lastname: Dorey
authors.affiliation: Unité de Recherche Vigne et Vin de Champagne Equipe d'Accueil 4707, Laboratoire Stress Défenses et Reproduction des Plantes, Structure Fédérative de Recherche Condorcet Fédération de Recherche, Centre National de la Recherche Scientifique 3417, Université de Reims Champagne-Ardenne, F-51687 Reims cedex 2, France (M.M.-R., S.D., C.C., F.B., S.D.-C.); andCenter for Plant Science Innovation and Department of Biochemistry, University of Nebraska, Lincoln, Nebraska 68588 (D.L.B., J.M.).
authors.forename: Christophe
authors.initials: C
authors.lastname: Clément
authors.affiliation: Unité de Recherche Vigne et Vin de Champagne Equipe d'Accueil 4707, Laboratoire Stress Défenses et Reproduction des Plantes, Structure Fédérative de Recherche Condorcet Fédération de Recherche, Centre National de la Recherche Scientifique 3417, Université de Reims Champagne-Ardenne, F-51687 Reims cedex 2, France (M.M.-R., S.D., C.C., F.B., S.D.-C.); andCenter for Plant Science Innovation and Department of Biochemistry, University of Nebraska, Lincoln, Nebraska 68588 (D.L.B., J.M.).
authors.forename: Fabienne
authors.identifier: http://orcid.org/0000-0002-7142-1035
authors.initials: F
authors.lastname: Baillieul
authors.affiliation: Unité de Recherche Vigne et Vin de Champagne Equipe d'Accueil 4707, Laboratoire Stress Défenses et Reproduction des Plantes, Structure Fédérative de Recherche Condorcet Fédération de Recherche, Centre National de la Recherche Scientifique 3417, Université de Reims Champagne-Ardenne, F-51687 Reims cedex 2, France (M.M.-R., S.D., C.C., F.B., S.D.-C.); andCenter for Plant Science Innovation and Department of Biochemistry, University of Nebraska, Lincoln, Nebraska 68588 (D.L.B., J.M.) sandrine.cordelier@univ-reims.fr.
authors.forename: Sandrine
authors.initials: S
authors.lastname: Dhondt-Cordelier
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000276:immunology* / Q000382:microbiology / Q000502:physiology; D020171:Botrytis / Q000502:physiology; D016923:Cell Death; D003517:Cyclopentanes / Q000378:metabolism; D007532:Isoleucine / Q000031:analogs & derivatives / Q000378:metabolism; D009154:Mutation; D054883:Oxylipins / Q000378:metabolism; D010935:Plant Diseases / Q000276:immunology* / Q000382:microbiology; D010937:Plant Growth Regulators / Q000378:metabolism*; D044224:Pseudomonas syringae / Q000502:physiology; D017382:Reactive Oxygen Species / Q000378:metabolism; D020156:Salicylic Acid / Q000378:metabolism; D015398:Signal Transduction; D013107:Sphingolipids / Q000378:metabolism*; D013110:Sphingosine / Q000031:analogs & derivatives / Q000378:metabolism
chemical_list: C577618:4-hydroxy-8-sphingenine; D003517:Cyclopentanes; D054883:Oxylipins; D010937:Plant Growth Regulators; D017382:Reactive Oxygen Species; D013107:Sphingolipids; C532883:jasmonoyl-isoleucine; C117422:phytosphingosine-1-phosphate; D007532:Isoleucine; C060504:dihydrosphingosine 1-phosphate; C011006:jasmonic acid; D013110:Sphingosine; D020156:Salicylic Acid; C005682:safingol