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Functional Interplay Between Arabidopsis NADPH Oxidases and Heterotrimeric G Protein

¹Centro de Biotecnología y Genómica de Plantas (UPM-INIA), Universidad Politécnica de Madrid, Campus Montegancedo, Autopista M40 Km38, Pozuelo de Alarcón, 28223, Madrid, Spain; ²Departamento de Biotecnología, Escuela Superior Técnica de Ingenieros Agrónomos, UPM, Avda. Complutense, 28040, Madrid, Spain; ³Department of Biology and Department of Pharmacology, University of North Carolina, Chapel Hill, 32599-3280, U.S.A.; ⁴Howard Hughes Medical Institute, Department of Biology, Department of Microbiology and Immunology, Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, NC 27599-3280, U.S.A.

The plant NADPH oxidases produce reactive oxygen species (ROS) in response to pathogens that have diverse functions in different cellular contexts. Distinct phenotypic outcomes may derive from the interaction of NADPH oxidase-dependent ROS with other signaling components that mediate defense activation. We analyze the interaction between NADPH oxidases AtRbohD and AtRbohF and the Arabidopsis heterotrimeric G protein. The Gβ subunit (AGB1) of the heterotrimeric G protein is required for full disease resistance to different Pseudomonas syringae strains. Genetic studies reveal that, upon P. syringae infection, AGB1 and AtRbohD and AtRbohF can function in the same pathway, as the agb1 null allele is epistatic to the NADPH oxidase null alleles, combinatorial mutants display the agb1 phenotypes, and agb1 suppresses some of the atrbohD atrbohF double mutant phenotypes. In contrast, increased susceptibility to the necrotrophic fungus Plectosphaerella cucumerina displayed by agb1 and atrbohD atrbohF is enhanced in the agb1 atrbohD atrbohF triple mutant, suggesting that NADPH oxidase and heterotrimeric G proteins mediate different response pathways in response to this necrotrophic pathogen. The defense response mediated by AGB1 is independent of pathogen-dependent salicylic acid accumulation and signaling, as the agb1 sid2 (isochorismate synthase 2) double mutant showed enhanced disease susceptibility to P. syringae and Plectosphaerella cucumerina as compared with both single mutants. This study exemplifies the complex interplay between signaling events mediating defense activation, depending on the type of plant-pathogen interaction.