Glucose Release Controlled by Sugar Transporters in Wheat Plant Modulates Microbial Growth and Enzyme Activity Around the Root

Soil microbial communities are the main regulators of ecosystem services and are vital for carbon and nutrient cycling. Root exudates play a crucial role in shaping soil microbial assembly and hence, influencing biogeochemical processes that impact plant growth. Here, we hypothesized that continuous wheat cultivation would lead to lower glucose release, resulting in lower microbial growth, activity, and biomass. For the first time in situ glucose imaging was optimized for studying these interactions in the field - using installed root windows in the first (W1) and third (W3) wheat after break crop plots. Root and leaf samples were collected to determine the expression of sugar transporter genes using transcriptomics. Soil microbial respiration (characterized by Substrate Induced Growth Respiration (SIGR)) and enzyme kinetics (measured by fluorometric microplate assays of 4-methylumbelliferone (MUF) and 7-amino-4-methyl coumarin (AMC)) were measured in rhizosphere, root affected and bulk soil samples to assess C, N, and P acquisition.

W3 had the lowest proportion of hotspots for glucose release with 1.35 % of the total soil surface area, indicating a 17.7 % decline compared to W1. Also, we found that the expressions of functional orthologous genes of SWEET1a in wheat roots were significantly upregulated in W3 compared to W1. Furthermore, total microbial biomass dropped by 11.8 and 4.8 % in W3 in the rhizosphere and bulk soils compared to W1, respectively. The growing microbial biomass in the rhizosphere soil of W1 was about five times higher than W3. For β-glucosidase activity, soil samples from W1 had a higher maximum velocity of enzyme activity (V_max) compared to W3 samples, in all studied compartments (rhizosphere, root affected and bulk soil samples). Lower glucose release in W3 highlights the importance of root exudates in shaping rhizosphere interactions and microbial community dynamics in response to continuous wheat cultivation. Also, differences in SWEET gene expression in wheat roots and leaves, indicates shifts in nutrient uptake and resource allocation strategies. This decline in glucose release observed under W3 compared to W1 underscores the significance of root exudates in shaping rhizosphere interactions.

Overall, the shift in glucose release is linked to altered root physiology and exudation processes, potentially reflecting the plant's strategy to create a less favorable environment for ambuscade and opportunistic pathogens. Hence, this study provides novel insights into the complex interactions between continuous wheat cultivation, root exudation, microbial dynamics, gene expression, and enzymatic activities.