Escalation in the host-pathogen arms race: A host resistance response corresponds to a heightened bacterial virulence response

Author summary The arms race between plants and pathogens is a complex process. To dissect the plant defense and pathogen virulence responses simultaneously, we used sorghum and Xanthomonas vasicola pv. holcicola, as a model pathosystem. We performed dual RNA-seq on infected sorghum with a range of disease phenotypes. Our characterization of this pathosystem demonstrates that genes related to the plant defense and pathogen virulence responses are most highly induced during a resistance interaction. We observed a similar pattern of escalation in Arabidopsis infected with Pseudomonas syringae. These observations support a conceptual model of fluidity between the different stages of plant immunity and pathogen virulence. The zig-zag model of host-pathogen interaction describes the relative strength of defense response across a spectrum of pathogen-induced plant phenotypes. A stronger defense response results in increased resistance. Here, we investigate the strength of pathogen virulence during disease and place these findings in the context of the zig-zag model. Xanthomonas vasicola pv. holcicola (Xvh) causes sorghum bacterial leaf streak. Despite being widespread, this disease has not been described in detail at the molecular level. We divided diverse sorghum genotypes into three groups based on disease symptoms: water-soaked lesions, red lesions, and resistance. Bacterial growth assays confirmed that these three phenotypes represent a range of resistance and susceptibility. To simultaneously reveal defense and virulence responses across the spectrum of disease phenotypes, we performed dual RNA-seq on Xvh-infected sorghum. Consistent with the zig-zag model, the expression of plant defense-related genes was strongest in the resistance interaction. Surprisingly, bacterial virulence genes related to the type III secretion system (T3SS) and type III effectors (T3Es) were also most highly expressed in the resistance interaction. This expression pattern was observed at multiple time points within the sorghum-Xvh pathosystem. Further, a similar expression pattern was observed in Arabidopsis infected with Pseudomonas syringae for effector-triggered immunity via AvrRps4 but not AvrRpt2. Specific metabolites were able to repress the Xvh virulence response in vitro and in planta suggesting a possible signaling mechanism. Taken together, these findings reveal multiple permutations of the continually evolving host-pathogen arms race from the perspective of host defense and pathogen virulence responses.

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