title: Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens.
abstract: In plants, autophagy has been assigned 'pro-death' and 'pro-survival' roles in controlling programmed cell death associated with microbial effector-triggered immunity. The role of autophagy in basal immunity to virulent pathogens has not been addressed systematically, however. Using several autophagy-deficient (atg) genotypes, we determined the function of autophagy in basal plant immunity. Arabidopsis mutants lacking ATG5, ATG10 and ATG18a develop spreading necrosis upon infection with the necrotrophic fungal pathogen, Alternaria brassicicola, which is accompanied by the production of reactive oxygen intermediates and by enhanced hyphal growth. Likewise, treatment with the fungal toxin fumonisin B1 causes spreading lesion formation in atg mutant genotypes. We suggest that autophagy constitutes a 'pro-survival' mechanism that controls the containment of host tissue-destructive microbial infections. In contrast, atg plants do not show spreading necrosis, but exhibit marked resistance against the virulent biotrophic phytopathogen, Pseudomonas syringae pv. tomato. Inducible defenses associated with basal plant immunity, such as callose production or mitogen-activated protein kinase activation, were unaltered in atg genotypes. However, phytohormone analysis revealed that salicylic acid (SA) levels in non-infected and bacteria-infected atg plants were slightly higher than those in Col-0 plants, and were accompanied by elevated SA-dependent gene expression and camalexin production. This suggests that previously undetected moderate infection-induced rises in SA result in measurably enhanced bacterial resistance, and that autophagy negatively controls SA-dependent defenses and basal immunity to bacterial infection. We infer that the way in which autophagy contributes to plant immunity to different pathogens is mechanistically diverse, and thus resembles the complex role of this process in animal innate immunity.
authors.affiliation: Center for Plant Molecular Biology, Eberhard Karls University of Tübingen, 72076 Tübingen, Germany.
authors.forename: Heike D
authors.initials: HD
authors.lastname: Lenz
authors.forename: Eva
authors.initials: E
authors.lastname: Haller
authors.forename: Eric
authors.initials: E
authors.lastname: Melzer
authors.forename: Karina
authors.initials: K
authors.lastname: Kober
authors.forename: Karl
authors.initials: K
authors.lastname: Wurster
authors.forename: Mark
authors.initials: M
authors.lastname: Stahl
authors.forename: Diane C
authors.initials: DC
authors.lastname: Bassham
authors.forename: Richard D
authors.initials: RD
authors.lastname: Vierstra
authors.forename: Jane E
authors.initials: JE
authors.lastname: Parker
authors.forename: Jaqueline
authors.initials: J
authors.lastname: Bautor
authors.forename: Antonio
authors.initials: A
authors.lastname: Molina
authors.forename: Viviana
authors.initials: V
authors.lastname: Escudero
authors.forename: Takayuki
authors.initials: T
authors.lastname: Shindo
authors.forename: Renier A L
authors.initials: RA
authors.lastname: van der Hoorn
authors.forename: Andrea A
authors.initials: AA
authors.lastname: Gust
authors.forename: Thorsten
authors.initials: T
authors.lastname: Nürnberger
mesh_terms: D000528:Alternaria / Q000276:immunology / Q000472:pathogenicity; D017360:Arabidopsis / Q000235:genetics / Q000276:immunology* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000378:metabolism*; D001343:Autophagy / Q000235:genetics / Q000276:immunology*; D000071187:Autophagy-Related Protein 5; D000071183:Autophagy-Related Proteins; D005030:Ethylenes / Q000378:metabolism; D037341:Fumonisins / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D005816:Genetic Complementation Test; D056426:Genetic Loci; D058685:Genetic Pleiotropy; D007113:Immunity, Innate; D007211:Indoles / Q000378:metabolism; D010744:Phosphoric Monoester Hydrolases / Q000378:metabolism*; D010937:Plant Growth Regulators / Q000378:metabolism; D018515:Plant Leaves / Q000378:metabolism / Q000382:microbiology; D044224:Pseudomonas syringae / Q000276:immunology / Q000472:pathogenicity; D020156:Salicylic Acid / Q000378:metabolism; D013844:Thiazoles / Q000378:metabolism; D000094162:Phytoalexins
chemical_list: D029681:Arabidopsis Proteins; D000071187:Autophagy-Related Protein 5; D000071183:Autophagy-Related Proteins; D005030:Ethylenes; D037341:Fumonisins; D007211:Indoles; D010744:Phosphoric Monoester Hydrolases; D010937:Plant Growth Regulators; D020156:Salicylic Acid; D013844:Thiazoles; C529532:ATG10 protein, Arabidopsis; C502739:ATG18a protein, Arabidopsis; C102405:camalexin; D000094162:Phytoalexins; C056933:fumonisin B1; C036216:ethylene; C518662:Atg5 protein, Arabidopsis