Auxin‐Producing <i>Pseudomonas</i> Recruited by Root Flavonoids Increases Rice Rhizosheath Formation through the Bacterial Histidine Kinase Under Soil Drying

Rhizosheath formation is facilitated by root hair length, root exudates, the soil microbes, which collectively enhance plant resistance to drought. This process partly results from the complex interaction between root exudates and microbes, a relationship that remains poorly understood. The roles of root exudates and microbes in rhizosheath formation in rice under soil drying (SD) conditions are investigated. In tetraploid rice, rhizosheath formation under SD is approximately 70% greater than in diploid rice. Inoculation of diploid rice with the rhizosheath soil microbiota from tetraploid rice significantly enhanced rhizosheath formation under SD. The bacterial genus Pseudomonas is identified as the key taxon promoting rhizosheath formation in tetraploid rice under SD. Tetraploid rice exhibits significantly higher root flavonoid concentration than diploid rice under SD. Overexpression of the chalcone synthase gene (OsCHS1), a key gene involved in flavonoid biosynthesis, led to a significant increase in the abundance of Pseudomonadaceae in diploid rice. Pseudomonas nitroreducens, isolated from the rhizosheath of tetraploid rice, demonstrates chemotactic attraction to flavonoids, but this behavior is not observed in histidine kinase mutant ΔcheA. Diploid and tetraploid rice inoculated with P. nitroreducens and IAA biosynthesis complemented strain ΔiaaM-c formed larger rhizosheath under SD than those inoculated with its IAA biosynthesis mutant ΔiaaM. These results suggest that auxin-producing Pseudomonas, recruited by root flavonoids, enhances rice rhizosheath formation through the bacterial histidine kinase under SD. This finding may facilitate the improvement of environmental adaptation in polyploidy crops by regulating their interactions with beneficial soil microorganisms.