Rhizosphere engineering for improved plant–beneficial microbe interactions: Concepts and some remaining questions

The rhizosphere, often defined as the narrow layer of soil around plant roots, is a hotbed of microbial activity and is enriched with plant-derived metabolites that shape the root-associated microbiome. Several species of free-living rhizosphere microbes (known as rhizobacteria) have been identified in laboratory and small-scale experiments that enhance plant growth and adaptation to challenging environments. However, efforts to utilize these beneficial microbes on large scales have not always produced the anticipated results. A key bottleneck is the low rhizosphere competence of many of these rhizobacteria, described as their inability to effectively outcompete other soil-resident microbes and to colonize and thrive in the rhizosphere. Yet, root exudates contain metabolites that select for beneficial microbes, suggesting that the rhizosphere could be engineered to enable beneficial microbes applied in the field overcome their low rhizosphere competence and ultimately improve plant performance. This Review summarizes our current knowledge of how root exudates modulate root–microbe associations and discusses some outstanding questions, namely: (i) whether root exudation profiles could be rationally engineered to enhance the accumulation of specific metabolites in the rhizosphere to promote plant–beneficial microbe interactions, and the challenges that may come with this endeavour, and (ii) whether root exudation can be temporally engineered to benefit the plant at different developmental stages. Opportunities for rhizosphere engineering based on the dynamic nature of root exudate compositions are briefly discussed. Thus, this Review largely focuses on the significant promise of rhizosphere engineering to promote effective plant–beneficial microbe associations for improved plant performance and yield, while highlighting some potential pitfalls. • Rhizobacteria have shown great promise in enabling sustainable crop agriculture. • Low rhizosphere competence of rhizobacteria have hindered their widespread adoption. • Root exudate engineering can theoretically improve rhizosphere competence. • Root exudates can be enriched for beneficial metabolites, but there are pitfalls. • Temporal regulation of metabolite release may be a useful approach to rhizosphere engineering.