Nutrient dose-responsive transcriptome changes driven by Michaelis Menten kinetics underlie plant growth rates

Abstract

An increase in nutrient dose leads to proportional increases in crop biomass and agricultural yield. However, the molecular underpinnings of this nutrient dose-response are largely unknown. To investigate, we assayed changes in the Arabidopsis root transcriptome to different doses of nitrogen (N) a key plant nutrient as a function of time. By these means, we found that rate changes of genome-wide transcript levels in response to N-dose could be explained by a simple kinetic principle: the Michaelis-Menten (MM) model. Fitting the MM model allowed us to estimate the maximum rate of transcript change (V-max), as well as the N-dose at which one-half of V-max was achieved (K-m) for 1,153 N-dose-responsive genes. Since transcription factors (TF5) can act in part as the catalytic agents that determine the rates of transcript change, we investigated their role in regulating N-dose-responsive MM-modeled genes. We found that altering the abundance of TGA1, an early N -responsive TF, perturbed the maximum rates of N-dose transcriptomic responses (V-max), K-m, as well as the rate of N-dose-responsive plant growth. We experimentally validated that MM -modeled N-dose-responsive genes included both direct and indirect TGA1 targets, using a root cell TF assay to detect TF binding and/or TF regulation genome-wide. Taken together, our results support a molecular mechanism of transcriptional control that allows an increase in N-dose to lead to a proportional change in the rate of genome-wide expression and plant growth.

An increase in nutrient dose leads to proportional increases in crop biomass and agricultural yield. However, the molecular underpinnings of this nutrient dose-response are largely unknown. To investigate, we assayed changes in the Arabidopsis root transcriptome to different doses of nitrogen (N) a key plant nutrient as a function of time. By these means, we found that rate changes of genome-wide transcript levels in response to N-dose could be explained by a simple kinetic principle: the Michaelis-Menten (MM) model. Fitting the MM model allowed us to estimate the maximum rate of transcript change (V-max), as well as the N-dose at which one-half of V-max was achieved (K-m) for 1,153 N-dose-responsive genes. Since transcription factors (TF5) can act in part as the catalytic agents that determine the rates of transcript change, we investigated their role in regulating N-dose-responsive MM-modeled genes. We found that altering the abundance of TGA1, an early N -responsive TF, perturbed the maximum rates of N-dose transcriptomic responses (V-max), K-m, as well as the rate of N-dose-responsive plant growth. We experimentally validated that MM -modeled N-dose-responsive genes included both direct and indirect TGA1 targets, using a root cell TF assay to detect TF binding and/or TF regulation genome-wide. Taken together, our results support a molecular mechanism of transcriptional control that allows an increase in N-dose to lead to a proportional change in the rate of genome-wide expression and plant growth.