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Transcriptome landscape of a bacterial pathogen under plant immunity

Significance Plants have evolved a powerful innate immune system to defend against microbial pathogens. Despite extensive studies, how plant immunity ultimately inhibits bacterial pathogen growth is largely unknown, due to difficulties in profiling bacterial responses in planta. In this study, we established two methods for in planta bacterial transcriptome analysis using RNA sequencing. By analyzing 27 combinations of plant immunity mutants and Pseudomonas syringae strains, we succeeded in the identification of specific bacterial transcriptomic signatures that are influenced by plant immune activation. In addition, we found that overexpression of an immune-responsive P. syringae sigma factor gene involved in iron regulation could partially counter bacterial growth restriction during plant immunity. This study illuminates the enigmatic mechanisms of bacterial growth inhibition by plant immunity. Plant pathogens can cause serious diseases that impact global agriculture. The plant innate immunity, when fully activated, can halt pathogen growth in plants. Despite extensive studies into the molecular and genetic bases of plant immunity against pathogens, the influence of plant immunity in global pathogen metabolism to restrict pathogen growth is poorly understood. Here, we developed RNA sequencing pipelines for analyzing bacterial transcriptomes in planta and determined high-resolution transcriptome patterns of the foliar bacterial pathogen Pseudomonas syringae in Arabidopsis thaliana with a total of 27 combinations of plant immunity mutants and bacterial strains. Bacterial transcriptomes were analyzed at 6 h post infection to capture early effects of plant immunity on bacterial processes and to avoid secondary effects caused by different bacterial population densities in planta. We identified specific “immune-responsive” bacterial genes and processes, including those that are activated in susceptible plants and suppressed by plant immune activation. Expression patterns of immune-responsive bacterial genes at the early time point were tightly linked to later bacterial growth levels in different host genotypes. Moreover, we found that a bacterial iron acquisition pathway is commonly suppressed by multiple plant immune-signaling pathways. Overexpression of a P. syringae sigma factor gene involved in iron regulation and other processes partially countered bacterial growth restriction during the plant immune response triggered by AvrRpt2. Collectively, this study defines the effects of plant immunity on the transcriptome of a bacterial pathogen and sheds light on the enigmatic mechanisms of bacterial growth inhibition during the plant immune response.