Wheat Root and Rhizosphere Microbiome Structures and Functions Along Plant Growth

Abstract Background Roots select their associated microbiome and affect its composition and activities through exudates that provide a nutrient-rich environment based on distance from the root. Root-exudation patterns depend on the plant's developmental stage. We followed field-grown wheat from emergence to spike maturation and compared the structure and functions of the microbiomes in two niches: adjacent, root-associated bacteria and the rhizosphere. The effects of growth stage on root-associated and rhizospheric communities structure and functions were investigated to enhance our understanding of plant–microbe interactions. Results A significant impact of wheat developmental stage during the transition from vegetative growth to spike formation was observed on structure and functions of both root-associated and rhizosphere microbiomes. On the root surface, abundance of the well-known wheat colonizers Proteobacteria and Actinobacteria decreased and increased, respectively, during spike formation, whereas abundance of Bacteroidetes was independent of spike formation. Three microbiome functional clusters were specifically associated with root proximity: (1) biofilm and sensorial movement; (2) antibiotic production and resistance; and (3) carbon biosynthesis, degradation and transporters, and amino acid biosynthesis and transporters. Interestingly, in the root-associated microbiome, genes related to all of these functions were influenced by spike formation. Abundance of genes related to nine other functions (lipopolysaccharide transporter and biosynthesis, beta-lactam resistance, metabolism of methane, alanine-aspartate-glutamate and arginine-proline, and biosynthesis of peptidoglycan, lysine and enediyne antibiotics) was significantly influenced by spike formation in both roots and rhizosphere. All of these genes were abundant in the rhizosphere, more so before spike formation when root exudation is high, supporting the notion that some of the root exudates are not fully utilized by the root-associated bacteria and subsequently diffuse into the surrounding soil, creating the rhizosphere. Conclusions We demonstrated functional division in the microbiome of the wheat root zone in both time and space: pre- and post-spike formation and root-associated vs. rhizospheric niches. The responses of the root microbiome were driven by both the plant and the microbial physiology and activities, both of which respond to environmental cues. These findings shed light on the dynamics of plant–microbe and microbe–microbe interactions in the root zone.