Maintaining symbiotic homeostasis: how do plants engage with beneficial microorganisms while at the same time restricting pathogens?  

Thoms et al., 2021

That plants recruit beneficial microbes while simultaneously restricting pathogens is critical to their survival. Plants must exclude pathogens; however, the majority of land plants are able to form mutualistic symbioses with arbuscular mycorrhizal fungi. Plants also associate with the complex microbial communities that form the microbiome. The outcome of each symbiotic interaction—whether a specific microbe is pathogenic, commensal or mutualistic—relies on the specific interplay of host and microbial genetics and the environment. Here, we discuss how plants use metabolites as a gate to select which microbes can be symbiotic. Once present, we discuss how plants integrate multiple inputs to initiate programs of immunity or mutualistic symbiosis, and how this paradigm may be expanded to the microbiome. Finally, we discuss how environmental signals are integrated with immunity to fine tune a thermostat that determines whether a plant engages in mutualism, resistance to pathogens, and shapes associations with the microbiome. Collectively, we propose that the plant immune thermostat is set to select for and tolerate a largely non-harmful microbiome while receptor-mediated decision making allows plants to detect and dynamically respond to the presence of potential pathogens or mutualists. 

 

This review discusses three principles by which plants may select for or restrict potential mutualists or pathogens. (A) Plants use selective metabolites (purple) to recruit or select for beneficial microbes (blue) and select against pathogens (gray). (B) Dual receptor recognition allows for precisely distinguishing potential pathogens or mutualists prior to energy investment in an immune or symbiotic response. MAMPs are common between pathogens and mutualists and so are not sufficient for a plant to  determine wither a microbe is friend or foe; however, MAMPs can provide information about the identity of a microbe. Coupling perception of MAMPs with LCOs, effectors, or DAMPs has the potential to trigger a strong and specific immunity or symbiotic program. (C) Integration of intrinsic and extrinsic signals with immune homeostasis allows plants to fine-tune decision making in symbiosis and dynamically shape symbiotic interactions over a plant’s life. This may allow for fine-tuning of microbiome community structure as well as changing a threshold for  strong immunity and symbiosis responses. 

 

To decide whether to engage in immunity or symbiosis, a plant must identify the type of microbe it is interacting with, and whether that microbe is mutualistic or pathogenic. Robust activation of a specific pathway depends on the combined input of MAMPs and one or more lifestyle associated factor [e.g. DAMPs/effectors/lipochitooligosaccharides (LCOs)]. In this example, chitin informs the plant that the symbiont is a fungus, and LCOs or effectors inform the plant whether it is a mutualist (blue components/arrows) or pathogenic (red components/arrows). The central boxes represent basal immunity pathways and common symbiotic pathways, which include the respective signaling cascades, post-translational modifications, and gene induction required for initiation of an immune or mutualistic response. At the bottom are the microbe-specific responses for resistance against or mutualism with a specific type of microbe. Activated pathways are indicated by white boxes and inactive pathwaysare shown in grey. Dotted lines indicate weak signaling and activation, while solid lines reflect stronger interactions. Wide arrows represent either a synergistic or additive response.

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