Mutualistic interaction between arbuscular mycorrhiza fungi and soybean roots enhances drought resistant through regulating glucose exudation and rhizosphere expansion

Abstract

Glucose is one of the low molecular weight components of root exudates to mediate the cross-talk between plants and microbes, but less is known about their contribution to drought resistance of plants and root-associated microbiome. To fill this knowledge gap, we optimized the visualization of glucose exudation and coupled it with another in situ tool – soil zymography ‒ as well as destructive analysis of enzyme kinetics (β-glucosidase; acid phosphomonoesterase) and microbial biomass. This helped identify how microbial functionality ‒ affected by drought and P limitation ‒ will show more resistance in the hotspots of soybean rhizosphere (grown in the rhizoboxes for 10 weeks) associated with arbuscular mycorrhizal fungi (AMF) symbiosis than those without AMF. Drought reduced glucose exudation, mainly allocated to root tips, and narrowed the rhizosphere enzymatic hotspot by three times. However, AMF inoculation enhanced glucose exudation compared to non-mycorrhizal plants and enlarged enzymatic hotspot area by 53% under drought condition. Despite the 50% reduction in β-glucosidase and acid phosphomonoesterase activities owing to water deficit, AMF symbiont triggered up to 36% enzyme activities in correlation with the non-mycorrhizal ones. Therefore, the drought resistance of these two enzymes was enhanced by up to 63% in mycorrhizal plants. The biomass of microbial phosphorus increased by 45% under drought AMF-conditioned plants. We conclude that the cooperation between soybean and AMF induced the formation of favorable microsites around the root, specifically in overlapping localities between rhizosphere and mycorrhizosphere, characterized by enhanced glucose release, increasing rhizosphere expansion, high enzyme activities and shortened substrate turnover time. This, in turn, contributed to the stronger resistance of microbial functions (e.g., enzyme expression) to drought stress in the rhizosphere hotspots. Thus, in response to AMF inoculation and consequent high glucose availability, rhizosphere microorganisms increased P mining rate in those hotspots remaining active despite water scarcity.