title: Neonicotinoid insecticides induce salicylate-associated plant defense responses.
abstract: Neonicotinoid insecticides control crop pests based on their action as agonists at the insect nicotinic acetylcholine receptor, which accepts chloropyridinyl- and chlorothiazolyl-analogs almost equally well. In some cases, these compounds have also been reported to enhance plant vigor and (a)biotic stress tolerance, independent of their insecticidal function. However, this mode of action has not been defined. Using Arabidopsis thaliana, we show that the neonicotinoid compounds, imidacloprid (IMI) and clothianidin (CLO), via their 6-chloropyridinyl-3-carboxylic acid and 2-chlorothiazolyl-5-carboxylic acid metabolites, respectively, induce salicylic acid (SA)-associated plant responses. SA is a phytohormone best known for its role in plant defense against pathogens and as an inducer of systemic acquired resistance; however, it can also modulate abiotic stress responses. These neonicotinoids effect a similar global transcriptional response to that of SA, including genes involved in (a)biotic stress response. Furthermore, similar to SA, IMI and CLO induce systemic acquired resistance, resulting in reduced growth of a powdery mildew pathogen. The action of CLO induces the endogenous synthesis of SA via the SA biosynthetic enzyme ICS1, with ICS1 required for CLO-induced accumulation of SA, expression of the SA marker PR1, and fully enhanced resistance to powdery mildew. In contrast, the action of IMI does not induce endogenous synthesis of SA. Instead, IMI is further bioactivated to 6-chloro-2-hydroxypyridinyl-3-carboxylic acid, which is shown here to be a potent inducer of PR1 and inhibitor of SA-sensitive enzymes. Thus, via different mechanisms, these chloropyridinyl- and chlorothiazolyl-neonicotinoids induce SA responses associated with enhanced stress tolerance.
authors.affiliation: Environmental Chemistry and Toxicology Laboratory, Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720, USA.
authors.forename: Kevin A
authors.initials: KA
authors.lastname: Ford
authors.forename: John E
authors.initials: JE
authors.lastname: Casida
authors.forename: Divya
authors.initials: D
authors.lastname: Chandran
authors.forename: Alexander G
authors.initials: AG
authors.lastname: Gulevich
authors.forename: Rachel A
authors.initials: RA
authors.lastname: Okrent
authors.forename: Kathleen A
authors.initials: KA
authors.lastname: Durkin
authors.forename: Richmond
authors.initials: R
authors.lastname: Sarpong
authors.forename: Eric M
authors.initials: EM
authors.lastname: Bunnelle
authors.forename: Mary C
authors.initials: MC
authors.lastname: Wildermuth
mesh_terms: D017360:Arabidopsis / Q000276:immunology* / Q000382:microbiology; D001203:Ascomycota / Q000187:drug effects*; D002851:Chromatography, High Pressure Liquid; D018506:Gene Expression Regulation, Plant / Q000187:drug effects* / Q000276:immunology; D006146:Guanidines / Q000737:chemistry / Q000276:immunology / Q000494:pharmacology*; D007093:Imidazoles / Q000737:chemistry / Q000276:immunology / Q000494:pharmacology*; D007306:Insecticides / Q000737:chemistry / Q000276:immunology / Q000494:pharmacology*; D013058:Mass Spectrometry; D015394:Molecular Structure; D000073943:Neonicotinoids; D009574:Nitro Compounds / Q000737:chemistry / Q000276:immunology / Q000494:pharmacology*; D020133:Reverse Transcriptase Polymerase Chain Reaction; D020156:Salicylic Acid / Q000276:immunology* / Q000378:metabolism; D013844:Thiazoles / Q000737:chemistry / Q000276:immunology / Q000494:pharmacology*
chemical_list: D006146:Guanidines; D007093:Imidazoles; D007306:Insecticides; D000073943:Neonicotinoids; D009574:Nitro Compounds; D013844:Thiazoles; C480342:clothianidin; C082359:imidacloprid; D020156:Salicylic Acid