Modulation of the Wheat Seed-Borne Bacterial Community by Herbaspirillum seropedicae RAM10 and Its Potential Effects for Tryptophan Metabolism in the Root Endosphere

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.

Genome-wide analysis of transmembrane 9 superfamily genes in wheat (Triticum aestivum) and their expression in the roots under nitrogen limitation and Bacillus amyloliquefaciens PDR1 treatment conditions

“…Studies have demonstrated that wheat cultivation is closely associated with bacterial communities that play crucial roles in its growth and immunity against diseases ( Carril et al., 2021 ; Wang et al., 2021 ; Youseif et al., 2021 ). Among these bacterial communities, plant-growth-promoting bacteria (PGPB) are of utmost importance for various plant functions such as phosphorus (P) solubilization, phytohormone production, nitrogen (N) fixation, and siderophore synthesis.…”

The Plant Growth-Promoting Potential of Halotolerant Bacteria Is Not Phylogenetically Determined: Evidence from Two Bacillus megaterium Strains Isolated from Saline Soils Used to Grow Wheat

“…One important approach is to make use of plant growth-promoting bacteria (PGPB). PGPB can improve crop production with multiple modes of action such as the synthesis of growth-promoting substances (including phytohormones such as auxins, strigolactones, and nitric oxide), improved plant nutrition, and resistance to biotic and abiotic stresses [ 18 , 20 , 21 , 22 , 23 ], including the stimulation of plant defence [ 24 , 25 ]. Indeed, the benefits of PGPB for a plant may occur along the plant’s life cycle as they may improve plant germination, survival, health, growth, reproduction, and productivity under optimal and adverse conditions.…”

Root inoculation with Herbaspirillum seropedicae RAM10 reveals structural and functional shifts in the wheat seed-borne microbiota associated with improved plant phenotype

“…Different H. seropedicae strains display a wide repertoire of protein secretion systems, type IV pili, as well as genes involved in plant surface adhesion, indicating its potential to actively colonize the endosphere environment [13,14]. However, its microbiota modulatory capacity has been previously explored through culture-based methods and only considering the bacterial community [15]. In this work, both 16S and ITS metabarcoding analyses were employed to test the hypothesis that H. seropedicae inoculation will lead to structural shifts in the wheat seed-borne endophytic microbiota.…”