Abstract

Plants are protected from pathogens not only by their own immunity but often also by colonizing commensal microbes. In Arabidopsis thaliana, a group of cryptically pathogenic Pseudomonas strains often dominates local populations. This group coexists in nature with commensal Pseudomonas strains that can blunt the deleterious effects of the pathogens in the laboratory. We have investigated the interaction between one of the Pseudomonas pathogens and 99 naturally co-occurring commensals, finding plant protection to be common among non-pathogenic Pseudomonas. While protective ability is enriched in one specific lineage, there is also a substantial variation for this trait among isolates of this lineage. These functional differences do not align with core-genome phylogenies, suggesting repeated gene inactivation or loss as causal. Using genome-wide association, we discovered that different bacterial genes are linked to plant protection in each lineage. We validated a protective role of several lineage-specific genes by gene inactivation, highlighting iron acquisition and biofilm formation as prominent mechanisms of plant protection in this Pseudomonas lineage. Collectively, our work illustrates the importance of functional redundancy in plant protective traits across an important group of commensal bacteria.

Highlights

  • The health of a plant depends to a large extent on its resident microbiota

  • In natural settings, the health of the ephemeral plant Arabidopsis thaliana is associated with many bacteria that reduce disease threats due to filamentous microbes [5]

  • In a parallel study with a Pseudomonas collection from an A. thaliana relative, commensal strains were shown to often outcompete pathogenic Pseudomonas syringae isolates sampled from the same plant [18]

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Summary

INTRODUCTION

The health of a plant depends to a large extent on its resident microbiota. The effect of individual microbes on plant health has been extensively investigated since the dawn of phytopathology [1], mainly focusing on pathogens, considering their profound effect on global agriculture and food supply [2]. Similar patterns have been found in controlled settings, with suppression of bacterial pathogens by other bacteria [8, 9] These protective agents can have several modes of action, including (i) activation of systemic defences that spread throughout the plant [10], (ii) outcompeting pathogens over nutrients [11, 12], and (iii) direct antibiosis [13, 14]. In a parallel study with a Pseudomonas collection from an A. thaliana relative, commensal strains were shown to often outcompete pathogenic Pseudomonas syringae isolates sampled from the same plant [18] These studies point to the importance of interactions among wild Pseudomonas strains in maintaining plant health. Contrasting activities, with one providing robust protection and the other having no effect, e.g., ATUE2 strains p11.F1 and p12

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