The Root Foraging Response under Low Nitrogen Depends on DWARF1-Mediated Brassinosteroid Biosynthesis

Root developmental plasticity enables plants to adapt to limiting or fluctuating nutrient conditions in the soil. When grown under nitrogen (N) deficiency, plants develop a more exploratory root system by increasing primary and lateral root length. However, mechanisms underlying this so-called foraging response remain poorly understood. We performed a genome-wide association study in Arabidopsis (Arabidopsis thaliana) and we show here that noncoding variations of the brassinosteroid (BR) biosynthesis gene DWARF1 (DWF1) lead to variation of the DWF1 transcript level that contributes to natural variation of root elongation under low N. In addition to DWF1, other central BR biosynthesis genes upregulated under low N include CONSTITUTIVE PHOTOMORPHOGENIC DWARF, DWF4, and BRASSINOSTEROID-6-OXIDASE 2 Phenotypic characterization of knockout and knockdown mutants of these genes showed significant reduction of their root elongation response to low N, suggesting a systemic stimulation of BR biosynthesis to promote root elongation. Moreover, we show that low N-induced root elongation is associated with aboveground N content and that overexpression of DWF1 significantly improves plant growth and overall N accumulation. Our study reveals that mild N deficiency induces key genes in BR biosynthesis and that natural variation in BR synthesis contributes to the root foraging response, complementing the impact of enhanced BR signaling observed recently. Furthermore, these results suggest a considerable potential of BR biosynthesis to genetically engineer plants with improved N uptake.