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

Abstract

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.

Transcriptomic and Metabolomic Approaches Deepen Our Knowledge of Plant–Endophyte Interactions

“…The relationship between pathogens and hosts is not unlike an 'arms race' that reciprocally drives the immune system (mentioned above) and resistance to escalate because of the wide adaptability and heightened virulence of plant pathogens (Stringlis and Pieterse, 2021;Wang et al, 2021). However, plants could recruit some mutualistic microbes as partners to enhance their own immunity and to suppress pathogen infection.…”

Type III secretion system effector subnetworks elicit distinct host immune responses to infection

“…The repertoire of effectors affects the inflammatory response and consequently the disease severity [37,41,42]; the expression of specific effectors such as EspM (absent in the prototype E2348/69 strain) and NleB have been linked to EPEC and EHEC isolates causing outbreaks and severe disease in humans [43][44][45]. As new experimental results feed the dataset, the model is expected to increase in complexity and prediction power, allowing translation of different effector compositions into immune responses and other infection outcomes, as well as identification of likely roles for effectors of unknown function.…”

Logistics of defense: The contribution of endomembranes to plant innate immunity

“…Pathogens reside in different spaces in the plant. For example, bacterial pathogens like Pseudomonas and Xanthomonas live outside the cell in the apoplast, while some filamentous pathogens (e.g., oomycetes and fungi) penetrate the host cell, and some pathogens (e.g., Ralstonia and certain Xanthomonas species) colonize the plant vasculature ( Xin et al, 2018 ; Wang et al, 2021a ; Kemen and Jones, 2012 ; Wang et al, 2019b ; Peeters et al, 2013 ) ( Box 1 and Box 2 ). Whether residing in extracellular spaces or invading cells, pathogens establish physical contact with host cells to either dampen immune response or to facilitate nutrient uptake with the goal of enabling their own growth.…”