NAD Acts as an Integral Regulator of Multiple Defense Layers.
Pyridine nucleotides, such as NAD, are crucial redox carriers and have emerged as important signaling molecules in stress responses. Previously, we have demonstrated in Arabidopsis (Arabidopsis thaliana) that the inducible NAD-overproducing nadC lines are more resistant to an avirulent strain of Pseudomonas syringae pv tomato (Pst-AvrRpm1), which was associated with salicylic acid-dependent defense. Here, we have further characterized the NAD-dependent immune response in Arabidopsis. Quinolinate-induced stimulation of intracellular NAD in transgenic nadC plants enhanced resistance against a diverse range of (a)virulent pathogens, including Pst-AvrRpt2, Dickeya dadantii, and Botrytis cinerea Characterization of the redox status demonstrated that elevated NAD levels induce reactive oxygen species (ROS) production and the expression of redox marker genes of the cytosol and mitochondrion. Using pharmacological and reverse genetics approaches, we show that NAD-induced ROS production functions independently of NADPH oxidase activity and light metabolism but depends on mitochondrial respiration, which was increased at higher NAD. We further demonstrate that NAD primes pathogen-induced callose deposition and cell death. Mass spectrometry analysis reveals that NAD simultaneously induces different defense hormones and that the NAD-induced metabolic profiles are similar to those of defense-expressing plants after treatment with pathogen-associated molecular patterns. We thus conclude that NAD triggers metabolic profiles rather similar to that of pathogen-associated molecular patterns and discuss how signaling cross talk between defense hormones, ROS, and NAD explains the observed resistance to pathogens.
biOMICS Facility, Department of Animal and Plant Sciences, University of Sheffield, S10 2TN Sheffield, United Kingdom (P.P., J.T.); p.petriacq@sheffield.ac.uk.|AgroParisTech, 75121 Paris cedex 05, France (O.P.); p.petriacq@sheffield.ac.uk.|Research School of Biology, College of Medicine, Biology, and Environment, Australian National University, 2601 Australian Capital Territory, Australia (G.T.); and p.petriacq@sheffield.ac.uk.|Institute of Plant Sciences Paris-Saclay, Unité Mixte de Recherche 9213, Université Paris-Sud, Bâtiment 630, 91405 Orsay cedex, France (B.G.) p.petriacq@sheffield.ac.uk.
Pierre
0000-0001-8151-7420
P
Pétriacq
biOMICS Facility, Department of Animal and Plant Sciences, University of Sheffield, S10 2TN Sheffield, United Kingdom (P.P., J.T.).|AgroParisTech, 75121 Paris cedex 05, France (O.P.).|Research School of Biology, College of Medicine, Biology, and Environment, Australian National University, 2601 Australian Capital Territory, Australia (G.T.); and.|Institute of Plant Sciences Paris-Saclay, Unité Mixte de Recherche 9213, Université Paris-Sud, Bâtiment 630, 91405 Orsay cedex, France (B.G.).
Jurriaan
0000-0002-8512-2802
J
Ton
biOMICS Facility, Department of Animal and Plant Sciences, University of Sheffield, S10 2TN Sheffield, United Kingdom (P.P., J.T.).|AgroParisTech, 75121 Paris cedex 05, France (O.P.).|Research School of Biology, College of Medicine, Biology, and Environment, Australian National University, 2601 Australian Capital Territory, Australia (G.T.); and.|Institute of Plant Sciences Paris-Saclay, Unité Mixte de Recherche 9213, Université Paris-Sud, Bâtiment 630, 91405 Orsay cedex, France (B.G.).
Oriane
O
Patrit
biOMICS Facility, Department of Animal and Plant Sciences, University of Sheffield, S10 2TN Sheffield, United Kingdom (P.P., J.T.).|AgroParisTech, 75121 Paris cedex 05, France (O.P.).|Research School of Biology, College of Medicine, Biology, and Environment, Australian National University, 2601 Australian Capital Territory, Australia (G.T.); and.|Institute of Plant Sciences Paris-Saclay, Unité Mixte de Recherche 9213, Université Paris-Sud, Bâtiment 630, 91405 Orsay cedex, France (B.G.).
Guillaume
G
Tcherkez
biOMICS Facility, Department of Animal and Plant Sciences, University of Sheffield, S10 2TN Sheffield, United Kingdom (P.P., J.T.).|AgroParisTech, 75121 Paris cedex 05, France (O.P.).|Research School of Biology, College of Medicine, Biology, and Environment, Australian National University, 2601 Australian Capital Territory, Australia (G.T.); and.|Institute of Plant Sciences Paris-Saclay, Unité Mixte de Recherche 9213, Université Paris-Sud, Bâtiment 630, 91405 Orsay cedex, France (B.G.).
Bertrand
B
Gakière
D017360:Arabidopsis / Q000276:immunology* / Q000382:microbiology / Q000528:radiation effects; D016923:Cell Death / Q000528:radiation effects; D016002:Discriminant Analysis; D060467:Disease Resistance / Q000276:immunology; D042541:Intracellular Space / Q000378:metabolism; D016018:Least-Squares Analysis; D008027:Light; D008928:Mitochondria / Q000378:metabolism / Q000528:radiation effects; D008954:Models, Biological; D009243:NAD / Q000378:metabolism*; D019255:NADPH Oxidases / Q000378:metabolism; D009711:Nucleotides / Q000378:metabolism; D018384:Oxidative Stress / Q000528:radiation effects; D000069452:Pathogen-Associated Molecular Pattern Molecules / Q000378:metabolism; D010641:Phenotype; D010935:Plant Diseases / Q000276:immunology / Q000382:microbiology; D010937:Plant Growth Regulators / Q000378:metabolism; D057865:Plant Immunity / Q000528:radiation effects; D018515:Plant Leaves / Q000166:cytology / Q000378:metabolism / Q000528:radiation effects; D011725:Pyridines / Q000378:metabolism; D017382:Reactive Oxygen Species / Q000378:metabolism; D016897:Respiratory Burst / Q000528:radiation effects; D020156:Salicylic Acid / Q000378:metabolism
D009711:Nucleotides; D000069452:Pathogen-Associated Molecular Pattern Molecules; D010937:Plant Growth Regulators; D011725:Pyridines; D017382:Reactive Oxygen Species; D009243:NAD; D019255:NADPH Oxidases; C023666:pyridine; D020156:Salicylic Acid