Lateral root priming synergystically arises from root growth and auxin transport dynamics

Abstract

The root system is a major determinant of plant fitness. Its capacity to supply the plant with sufficient water and nutrients strongly depends on root system architecture, which arises from the repeated branching off of lateral roots. A critical first step in lateral root formation is priming, which prepatterns sites competent of forming a lateral root. Priming is characterized by temporal oscillations in auxin, auxin signalling and gene expression in the root meristem, which through growth become transformed into a spatially repetitive pattern of competent sites. Previous studies have demonstrated the importance of auxin synthesis, transport and perception for the amplitude of these oscillations and their chances of producing an actual competent site. Additionally, repeated lateral root cap apoptosis was demonstrated to be strongly correlated with repetitive lateral root priming. Intriguingly, no single mutation has been identified that fully abolishes lateral root formation, and thusfar the mechanism underlying oscillations has remained unknown. In this study, we investigated the impact of auxin reflux loop properties combined with root growth dynamics on priming, using a computational approach. To this end we developed a novel multi-scale root model incorporating a realistic root tip architecture and reflux loop properties as well as root growth dynamics. Excitingly, in this model, repetitive auxin elevations automatically emerge. First, we show that root tip architecture and reflux loop properties result in an auxin loading zone at the start of the elongation zone, with preferential auxin loading in narrow vasculature cells. Second, we demonstrate how meristematic root growth dynamics causes regular alternations in the sizes of cells arriving at the elongation zone, which subsequently become amplified during cell expansion. These cell size differences translate into differences in cellular auxin loading potential. Combined, these properties result in temporal and spatial fluctuations in auxin levels in vasculature and pericycle cells. Our model predicts that temporal priming frequency predominantly depends on cell cycle duration, while cell cycle duration together with meristem size control lateral root spacing.