Complementary roles for auxin and auxin signalling revealed by reverse engineering lateral root stable prebranch site formation.

Priming is the process through which periodic elevations in auxin signalling prepattern future sites for lateral root formation, called prebranch sites. Thus far, the extent to which elevations in auxin concentration and/or auxin signalling are required for priming and prebranch site formation has remained a matter of debate. Recently, we discovered a reflux-and-growth mechanism for priming generating periodic elevations in auxin concentration that subsequently dissipate. Here, we reverse engineer a mechanism for prebranch site formation that translates these transient elevations into a persistent increase in auxin signalling, resolving the prior debate into a two-step process of auxin concentration-mediated initial signal and auxin signalling capacity-mediated memorization. A crucial aspect of the prebranch site formation mechanism is its activation in response to time-integrated rather than instantaneous auxin signalling. The proposed mechanism is demonstrated to be consistent with prebranch site auxin signalling dynamics, lateral inhibition, and symmetry-breaking mechanisms and perturbations in auxin homeostasis.

A reflux-and-growth mechanism explains oscillatory patterning of lateral root branching sites.

Modular, repetitive structures are a key component of complex multicellular body plans across the tree of life. Typically, these structures are prepatterned by temporal oscillations in gene expression or signaling. Although a clock-and-wavefront mechanism was identified and plant leaf phyllotaxis arises from a Turing-type patterning for vertebrate somitogenesis and arthropod segmentation, the mechanism underlying lateral root patterning has remained elusive. To resolve this enigma, we combined computational modeling with in planta experiments. Intriguingly, auxin oscillations automatically emerge in our model from the interplay between a reflux-loop-generated auxin loading zone and stem-cell-driven growth dynamics generating periodic cell-size variations. In contrast to the clock-and-wavefront mechanism and Turing patterning, the uncovered mechanism predicts both frequency and spacing of lateral-root-forming sites to positively correlate with root meristem growth. We validate this prediction experimentally. Combined, our model and experimental results support that a reflux-and-growth patterning mechanism underlies lateral root priming.

Modeling of Root Nitrate Responses Suggests Preferential Foraging Arises From the Integration of Demand, Supply and Local Presence Signals.

A plants' fitness to a large extent depends on its capacity to adapt to spatio-temporally varying environmental conditions. One such environmental condition to which plants display extensive phenotypic plasticity is soil nitrate levels and patterns. In response to heterogeneous nitrate distribution, plants show a so-called preferential foraging response. Herein root growth is enhanced in high nitrate patches and repressed in low nitrate locations beyond a level that can be explained from local nitrate sensing. Although various molecular players involved in this preferential foraging behavior have been identified, how these together shape root system adaptation has remained unresolved. Here we use a simple modeling approach in which we incrementally incorporate the known molecular pathways to investigate the combination of regulatory mechanisms that underly preferential root nitrate foraging. Our model suggests that instead of involving a growth suppressing supply signal, growth reduction on the low nitrate side may arise from reduced root foraging and increased competition for carbon. Additionally, our work suggests that the long distance CK signaling involved in preferential root foraging may function as a supply signal modulating demand signaling strength. We illustrate how this integration of demand and supply signals prevents excessive preferential foraging under conditions in which demand is not met by sufficient supply and a more generic foraging in search of nitrate should be maintained.