Rapid evolution of bacterial mutualism in the plant rhizosphere

Abstract

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.

Having the ‘right’ microbiome matters for host trait expression and the strength of mutualism between duckweeds and microbes

“…Host genotypes may affect the relative growth and success of different taxonomic groups within inoculated communities, resulting in different assembled microbiomes from the same source microbial communities (Lebeis et al, 2015; Jackrel et al, 2021; Wippel et al, 2021; Grieneisen et al, 2021). Differential assembly across host genotypes could result from top-down host selection of different microbes (Lebeis et al, 2015), or from adaptation of microbes to local hosts in colonization ability (Li et al, 2021). Abiotic environments can also alter microbiome assembly (Wang et al, 2021), as microbiome members often have differential tolerance to stressors, including zinc (Davis et al, 2004; Jain et al, 2020), which could account for zinc-dependent effects of microbiomes on duckweed fitness and traits.…”

Rhizosphere microbiome: Functional compensatory assembly for plant fitness

“…For instance, the development of high-yielding varieties and the agronomic management of modern agriculture inadvertently modified the root-microbe interactions in maize, in which fewer microorganisms responsible for nitrogen (N) acquisition but more members contributing to N losses were recruited in the rhizosphere of recently developed cultivars [35] . In contrast, adaptive evolution by improving the competitiveness for root exudates or enhancing the tolerance to the plant-secreted antimicrobial metabolites of a nonplant-associated microbe may promote its established reciprocal symbiosis relationship with the host plant [36] .…”

Selection and Characterization of Burkholderia spp. for Their Plant-Growth Promoting Effects and Influence on Maize Seed Germination

“…Most of these interactions occur in the soil-plant interface using specific niches such as the rhizosphere, endosphere and rhizoplane (1,2,8). The rhizosphere consists of the root zone directly influenced by plant exudates, but the microorganisms inhabiting these regions may also interfere in both plant development and soil fertility (5,9). Moreover, endophytic bacteria (endosphere) occur in all plant species and contribute to plant development by providing microbiological compounds capable to protect the plant, stimulate plant growth and nutrient absorption (4,10).…”

“…Moreover, endophytic bacteria (endosphere) occur in all plant species and contribute to plant development by providing microbiological compounds capable to protect the plant, stimulate plant growth and nutrient absorption (4,10). The root epiphytic bacteria, which are inhabitants of the root surface (rhizoplane) have also a crucial role in stimulating plant development (3,9).…”