Even in homogeneous conditions, plants facing a soilborne pathogen tend to show a binary outcome with individuals either remaining fully healthy or developing severe to lethal disease symptoms. As the rhizosphere microbiome is a major determinant of plant health, we postulated that such a binary outcome may result from an early divergence in the rhizosphere microbiome assembly that may further cascade into varying disease suppression abilities. We tested this hypothesis by setting up a longitudinal study of tomato plants growing in a natural but homogenized soil infested with the soilborne bacterial pathogen Ralstonia solanacearum. Starting from an originally identical species pool, individual rhizosphere microbiome compositions rapidly diverged into multiple configurations during the plant vegetative growth. This variation in community composition was strongly associated with later disease development during the later fruiting state. Most interestingly, these patterns also significantly predicted disease outcomes 2 weeks before any difference in pathogen density became apparent between the healthy and diseased groups. In this system, a total of 135 bacterial OTUs were associated with persistent healthy plants. Five of these enriched OTUs (Lysinibacillus, Pseudarthrobacter, Bordetella, Bacillus, and Chryseobacterium) were isolated and shown to reduce disease severity by 30.4–100% when co-introduced with the pathogen. Overall, our results demonstrated that an initially homogenized soil can rapidly diverge into rhizosphere microbiomes varying in their ability to promote plant protection. This suggests that early life interventions may have significant effects on later microbiome states, and highlights an exciting opportunity for microbiome diagnostics and plant disease prevention.

The plant hormone ethylene is one of the central regulators of plant development and stress resistance. Optimal ethylene signaling is essential for plant fitness and is under strong selection pressure. Plants upregulate ethylene production in response to stress, and this hormone triggers defense mechanisms. Due to the pleiotropic effects of ethylene, adjusting stress responses to maximize resistance, while minimizing costs, is a central determinant of plant fitness. Ethylene signaling is influenced by the plant-associated microbiome. We therefore argue that the regulation, physiology, and evolution of the ethylene signaling can best be viewed as the interactive result of plant genotype and associated microbiota. In this article, we summarize the current knowledge on ethylene signaling and recapitulate the multiple ways microorganisms interfere with it. We present ethylene signaling as a model system for holobiont-level evolution of plant phenotype: this cascade is tractable, extremely well studied from both a plant and a microbial perspective, and regulates fundamental components of plant life history. We finally discuss the potential impacts of ethylene modulation microorganisms on plant ecology and evolution. We assert that ethylene signaling cannot be fully appreciated without considering microbiota as integral regulatory actors, and we more generally suggest that plant ecophysiology and evolution can only be fully understood in the light of plant-microbiome interactions.

While beneficial plant-microbe interactions are common in nature, direct evidence for the evolution of bacterial mutualism is scarce. Here we use experimental evolution to causally show that initially plant-antagonistic Pseudomonas protegens bacteria evolve into mutualists in the rhizosphere of Arabidopsis thaliana within six plant growth cycles (6 months). This evolutionary transition is accompanied with increased mutualist fitness via two mechanisms: (i) improved competitiveness for root exudates and (ii) enhanced tolerance to the plant-secreted antimicrobial scopoletin whose production is regulated by transcription factor MYB72. Crucially, these mutualistic adaptations are coupled with reduced phytotoxicity, enhanced transcription of MYB72 in roots, and a positive effect on plant growth. Genetically, mutualism is associated with diverse mutations in the GacS/GacA two-component regulator system, which confers high fitness benefits only in the presence of plants. Together, our results show that rhizosphere bacteria can rapidly evolve along the parasitism-mutualism continuum at an agriculturally relevant evolutionary timescale.

Plant growth depends on a range of functions provided by their associated rhizosphere microbiome, including nutrient mineralization, hormone co-regulation and pathogen suppression. Improving the ability of plant-associated microbiomes to deliver these functions is thus important for developing robust and sustainable crop production. However, it is yet unclear how beneficial effects of probiotic microbial inoculants can be optimized and how their effects are mediated. Here, we sought to enhance tomato plant growth by targeted introduction of probiotic bacterial consortia consisting of up to eight plant-associated Pseudomonas strains. We found that the effect of probiotic consortium inoculation was richness-dependent: consortia that contained more Pseudomonas strains reached higher densities in the tomato rhizosphere and had clearer beneficial effects on multiple plant growth characteristics. Crucially, these effects were best explained by changes in the resident community diversity, composition and increase in the relative abundance of initially rare taxa, instead of introduction of plant-beneficial traits into the existing community along with probiotic consortia. Together, our results suggest that beneficial effects of microbial introductions can be driven indirectly through effects on the diversity and composition of the resident plant rhizosphere microbiome.