Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation

Author summary Plants thrive in highly heterogenous soils. How they compute a multitude of contrasting stimuli and mount an adaptive response without a centralized information processing unit is an intriguing question. For instance, below ground, roots can sense and respond to the single or multiple nutrient stresses, and adjust its growth rate accordingly. Nevertheless, the genetic architecture of root growth responses under single and combined stress remains poorly understood. To fill this gap in our understanding about such crucial phenomenon for plant survival, we explored the natural variation of root growth rate (RGR) in Arabidopsis grown under single and combined nutritional stress, including deficiencies of iron (-Fe), zinc (-Zn), phosphate and iron (-P-Fe) and phosphate and zinc (-P-Zn). Our GWAS revealed distinct genetic architectures underlying root growth responses to single or combined nutrient stresses. By integrating GWAS and coexpression networks, we identified and validated genes controlling the variation of root growth to combined nutrient-deficiency, namely VARIANT IN METHYLATION 1, FORMIN-LIKE-PROTEIN-6 and VOLTAGE-DEPENDENT ANION-SELECTIVE CHANNEL PROTEIN 3. Our findings provide a framework to accelerate future research aiming at better understanding how plants sense and respond to multiple environmental inputs, and promise to help designing new agronomical and biotechnological strategies to improve root growth.