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 <i>Arabidopsis</i> 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 (<i>V</i>_max), as well as the N-dose at which one-half of <i>V</i>_max was achieved (<i>K</i>_m) for 1,153 N-dose-responsive genes. Since transcription factors (TFs) 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 (<i>V</i>_max), <i>K</i>_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.