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.

Volatile compounds from beneficial rhizobacteria Bacillus spp. promote periodic lateral root development in Arabidopsis

“…In this study, we demonstrated that B. amyloliquefaciens VCs significantly enhanced the signal intensity of the DR5:Luciferase expression in the OZ (Figure 3e) and subsequently formed prebranch sites in shorter period (Figure 3c). It is suggested that meristem activity can influence the oscillation frequency (Berg & Tusscher, 2018). Likewise, we observed an enhanced expression of CYCB1 in the meristematic zone of B. amyloliquefaciens…”

Cadmium stress suppresses lateral root formation by interfering with the root clock

“…On the other hand, a recent computational approach suggested that root meristem activity also influences oscillation frequency (Thea van den Berg & ten Tusscher, ). A growing meristem with constant cell division ensures the replacement velocity of cells in the elongation zone/OZ, where auxin pulses are loaded by transporters to trigger oscillations for LR formation.…”

The dynamic nature and regulation of the root clock

“…DR5. DR5 (DIRECT REPEAT5) is a highly active and widespread reporter of auxin transcriptional response, which consists of 7-9 auxin response elements (AuxREs) containing tandem direct repeats of 11 base pairs that include the auxin-responsive TGTCTC element found in the soybean GH3 promoter (Ulmasov et al, 1997). These elements are crucial in the control on gene expression downstream of the TIR1/AFB-AUX/IAA-ARF signaling module.…”

“…Several DR5 reporter versions have been developed. Typically, Luciferase and GUS are transcriptionally fused under the control of the promoter described by Ulmasov et al (1997). Those constructs are herein below mentioned as DR5:Luciferase and DR5:GUS, respectively.…”