Fe-Based Nanomaterial-Induced Root Nodulation Is Modulated by Flavonoids to Improve Soybean (Glycine max) Growth and Quality.

Abstract

Innovative technology to increase efficient nitrogen (N) use while avoiding environmental damages is needed because of the increasing food demand of the rapidly growing global population. Soybean (Glycine max) has evolved a complex symbiosis with N-fixing bacteria that forms nodules to fix N. Herein, foliar application of 10 mg L-1 Fe7(PO4)6 and Fe3O4 nanomaterials (NMs) (Fe-based NMs) promoted soybean growth and root nodulation, thus improving the yield and quality over that of the unexposed control, EDTA-control, and 1 and 5 mg L-1 NMs. Mechanistically, flavonoids, key signaling molecules at the initial signaling steps in nodulation, were increased by more than 20% upon exposure to 10 mg L-1 Fe-based NMs, due to enhanced key enzyme (phenylalanine ammonia-lyase, PAL) activity and up-regulation of flavonoid biosynthetic genes (GmPAL, GmC4H, Gm4CL, and GmCHS). Accumulated flavonoids were secreted to the rhizosphere, recruiting rhizobia for colonization. Fe7(PO4)6 NMs increased Allorhizobium by 87.3%, and Fe3O4 NMs increased Allorhizobium and Mesorhizobium by 142.2% and 34.9%, leading to increased root nodules by 50.0% and 35.4% over the unexposed control, respectively. Leghemoglobin content was also noticeably improved by 8.2-46.5% upon Fe-based NMs. The higher levels of nodule number and leghemoglobin content resulted in enhanced N content by 15.5-181.2% during the whole growth period. Finally, the yield (pod number and grain biomass) and quality (flavonoids, soluble protein, and elemental nutrients) were significantly increased more than 14% by Fe-based NMs. Our study provides an effective nanoenabled strategy for inducing root nodules to increase N use efficiency, and then both yield and quality of soybean.