A balance of metabolism and diffusion articulates a gibberellin hormone gradient in the Arabidopsis root

Abstract

The plant hormone gibberellin (GA4) regulates numerous developmental processes. Within the root, GA4 controls growth, in part, by controlling the extent of cell elongation. The nlsGPS1 FRET biosensor revealed a GA4 gradient within the Arabidopsis root growth zones, with GA4 levels correlating with cell length. We developed a multiscale mathematical model to understand how biosynthesis, catabolism and transport create the GA4 distribution within the root growth zones. The model showed that phloem delivery of the biosynthetic intermediate GA12 contributes to higher levels of bioactive GA4 in the elongation zone, with the GA4 synthesis pattern being further modified by local GA12 synthesis in the quiescent centre region and the spatial distribution of biosynthesis enzymes (GA20ox and GA3ox). Model predictions revealed that whilst GA20ox and GA3ox transcript is present throughout the growth zones, these enzymes are inactive in the dividing cells, which explains steep GA4 gradients observed in GA20ox and GA3ox over-expression lines, and improves agreement between model predictions and data in wildtype, ga20ox and ga3ox lines. The model revealed that the GA4 gradient also depends a balance of diffusion through plasmodesmata and catabolism. Both model predictions and biosensor data demonstrated that plasmodesmatal diffusion enables a more gradual GA4 gradient, with higher diffusion antagonizing the GA4 gradient. Model predictions suggested that catabolism limits GA4 levels, which we validated via biosensor imaging in the ga2oxhept mutant. We concluded that GA4 distribution mediates root growth programming via local GA4 synthesis combining with diffusion and catabolism to create a spatial gradient that provides positional information and patterns cell elongation.