Abstract
Plants and their associated microbiota share ecological and evolutionary traits that are considered to be inseparably woven. Their coexistence foresees the use of similar metabolic pathways, leading to the generation of molecules that can cross-regulate each other’s metabolism and ultimately influence plant phenotype. However, the extent to which the microbiota contributes to the overall plant metabolic landscape remains largely unexplored. Due to their early presence in the seed, seed-borne endophytic bacteria can intimately colonize the plant’s endosphere while conferring a series of phytobeneficial services to their host. Understanding the dynamics of these endophytic communities is a crucial step toward the formulation of microbial inoculants that can modulate the functionality of the plant-associated microbiota for improved plant fitness. In this work, wheat (Triticum aestivum) roots non-inoculated and inoculated with the bacterium Herbaspirillum seropedicae strain RAM10 were analyzed to explore the impact of inoculant–endophyte–wheat interrelationships on the regulation of tryptophan (Trp) metabolism in the endosphere environment. Root inoculation with H. seropedicae led to phylum-specific changes in the cultivable seed-borne endophytic community. This modulation shifted the metabolic potential of the community in light of its capacity to modulate the levels of key Trp-related metabolites involved in both indole-3-acetic acid (IAA) biosynthesis and in the kynurenine pathway. Our results support a mode of action of H. seropedicae relying on a shift in both the composition and functionality of the seed-borne endophytic community, which may govern important processes such as root growth. We finally provide a conceptual framework illustrating that interactions among roots, inoculants, and seed-borne endophytes are critical to fine-tuning the levels of IAA in the endosphere. Understanding the outcomes of these interactions is a crucial step toward the formulation of microbial inoculants based on their joint action with seed-borne endophytic communities to promote crop growth and health in a sustainable manner.
Highlights
Plant–microbe beneficial associations have been the focus of intensive research, given their potential as sustainable alternatives for agricultural production
The inoculant H. seropedicae was not recovered from inoculated roots, indicating that H. seropedicae persistence was not guaranteed over time, it still had an effect on the proliferation of the cultivable seed-borne endophytic community
Our results point toward a microbiome modulation effect, where H. seropedicae effect may rely on a two-component mode of action, consisting of a shift in the endosphere metabolic landscape, which leads to a change in the seed-borne endophytic community composition and to the modulation of the endospheric indole3-acetic acid (IAA) levels
Summary
Plant–microbe beneficial associations have been the focus of intensive research, given their potential as sustainable alternatives for agricultural production (reviewed in Gupta et al, 2021) In this context, the transition of seeds to seedlings represents one of the most critical stages of plant development, where microbial interactions taking place in these early stages can profoundly impact host ecology, health, and productivity (Nelson, 2018). Recent advances in plant-microbiome engineering have opened new perspectives for the promotion of plant health by exploiting the potential of seed-borne endophytes (Guo et al, 2021) In this context, understanding their contribution to plant phenotype is a crucial step for the design of promising microbial inoculants to improve plant growth and health through the manipulation of the microbiota functionality (Truyens et al, 2015; reviewed in Berg et al, 2021). Despite the beneficial effects of seed-borne endophytes, their metabolic contribution to plant phenotype and especially their functional modulation by bacterial inoculants remain largely unexplored
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