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Effector-Triggered Immunity (ETI) is an important part of the plant immune system, allowing plants to sense and respond to harmful pathogen proteins known as “effectors.” Effectors can be sensed directly or indirectly by NLR (Nucleotide-binding Leucine-rich Repeat) proteins, many of which “guard” the plant proteins targeted by effectors. Although a few effector–target–NLR interactions have been characterized, a general understanding of how these molecular interactions give rise to a functioning immune system is lacking. Here, we present a physics-based model of ETI based on protein–protein interactions. We show that the simplest physical model consistent with the biology gives rise to a robust immune sensor and explains the empirical phenomenon of effector interference as a generic consequence of molecules competing for binding partners. Using the evolutionarily conserved ZAR1 defense gene as a model, we explain how more complex interaction networks integrate multiple pathogen signals into a single response. We then examine alternatives to a guarding architecture, including direct sensing, decoys, and blended “integrated decoy” strategies, and reveal that these sensing architectures obey functional trade-offs between their sensitivity, target protection, and proteomic cost. This allows a quantitative analysis of the trade-offs between different forms of ETI. We discuss these findings in the context of the evolutionary forces shaping the plant immune system. 

Abstract The evolutionary fate of multi-strain pathogens is shaped by host-pathogen ecological interactions. In bacterial pathogens of plants, enhanced strain characterization and advances in our understanding of molecular mechanisms underlying defense pathways open the door for revisiting the role of negative frequency-dependent selection (NFDS) in strain structure, including its interplay with genetic exchange. NFDS arising from specific defense is one potential mechanism for generating, maintaining, and structuring pathogen diversity. In plants, specific protection against microbial pathogens involves Resistance proteins (R-proteins) that recognize virulence factors (effectors) secreted by pathogens, typically to subvert the initial line of host defense. Here we formulate a stochastic computational co-evolution model that explicitly incorporates variable length R-gene and effector repertoires, and migration from their regional pools. We use this model to understand potential mechanisms shaping effector repertoire structure and associated strain coexistence in the generalist plant pathogenP. syringae. The demonstration of a modular structure in our numerical simulations motivates the analysis of genome sequences from 76 strains collected in the Midwestern US and 1104 strains from global sources. We find that effector repertories both locally and globally exhibit a modular structure, with higher similarity within than between clusters. The observed modules are consistent with the core genome phylogeny and are unexplained by plant host species, location of isolation, and genetic linkage between effectors. An extension of the model is needed to take into account the evidence for genetic exchange and the phylogenetic congruence of effector modules. We initialize the system with a phylogenetically congruent modular structure and include recombination rates decreasing as a function of phylogenetic distance. We show that NFDS can counter-balance the effects of mixing due to recombination and in so doing, contributes to the maintenance of strain structure. These findings indicate that the observed similarity clusters may constitute, in part, emergent niches arising from eco-evolutionary dynamics that contribute to strain coexistence. 

Abstract Gene duplication is increasingly recognized as an important mechanism for the origination of new genes, as revealed by comparative genomic analysis. However, how new duplicate genes contribute to phenotypic evolution remains largely unknown, especially in plants. Here, we identified the new gene EXOV, derived from a partial gene duplication of its parental gene EXOVL in Arabidopsis thaliana. EXOV is a species-specific gene that originated within the last 3.5 million years and shows strong signals of positive selection. Unexpectedly, RNA-sequencing analyses revealed that, despite its young age, EXOV has acquired many novel direct and indirect interactions in which the parental gene does not engage. This observation is consistent with the high, selection-driven substitution rate of its encoded protein, in contrast to the slowly evolving EXOVL, suggesting an important role for EXOV in phenotypic evolution. We observed significant differentiation of morphological changes for all phenotypes assessed in genome-edited and T-DNA insertional single mutants and in double T-DNA insertion mutants in EXOV and EXOVL. We discovered a substantial divergence of phenotypic effects by principal component analyses, suggesting neofunctionalization of the new gene. These results reveal a young gene that plays critical roles in biological processes that underlie morphological evolution in A. thaliana.