Putting Theory to the Test: Which Regulatory Mechanisms Can Drive Realistic Growth of a Root?

In recent years there has been a strong development of computational approaches to mechanistically understand organ growth regulation in plants. In this study, simulation methods were used to explore which regulatory mechanisms can lead to realistic output at the cell and whole organ scale and which other possibilities must be discarded as they result in cellular patterns and kinematic characteristics that are not consistent with experimental observations for the Arabidopsis thaliana primary root. To aid in this analysis, a ‘Uniform Longitudinal Strain Rule’ (ULSR) was formulated as a necessary condition for stable, unidirectional, symplastic growth. Our simulations indicate that symplastic structures are robust to differences in longitudinal strain rates along the growth axis only if these differences are small and short-lived. Whereas simple cell-autonomous regulatory rules based on counters and timers can produce stable growth, it was found that steady developmental zones and smooth transitions in cell lengths are not feasible. By introducing spatial cues into growth regulation, those inadequacies could be avoided and experimental data could be faithfully reproduced. Nevertheless, a root growth model based on previous polar auxin-transport mechanisms violates the proposed ULSR due to the presence of lateral gradients. Models with layer-specific regulation or layer-driven growth offer potential solutions. Alternatively, a model representing the known cross-talk between auxin, as the cell proliferation promoting factor, and cytokinin, as the cell differentiation promoting factor, predicts the effect of hormone-perturbations on meristem size. By down-regulating PIN-mediated transport through the transcription factor SHY2, cytokinin effectively flattens the lateral auxin gradient, at the basal boundary of the division zone, (thereby imposing the ULSR) to signal the exit of proliferation and start of elongation. This model exploration underlines the value of generating virtual root growth kinematics to dissect and understand the mechanisms controlling this biological system.Author Summary: The growth of a plant root is driven by cell division and cell expansion occurring in spatially distinct developmental zones. Although these zones are in principle stable, depending on the conditions, their size and properties can be modulated. This has been meticulously described by kinematic studies, which have led to the proposal of mechanisms underpinning those observations. At the same time, much knowledge of the identities and interactions of molecules involved in these mechanisms has accumulated, in particular from the model species Arabidopsis thaliana. Here we attempt to resolve the longstanding question whether observed growth patterns can be explained by autonomous decision-making at the level of individual cells or if the aid of some external signal is required. We then ask, building on the accumulated molecular information, which minimal models can provide for stable growth while keeping sufficient flexibility to regulate growth. Therefore, we constructed computational models for different growth mechanisms operating in a virtual two-dimensional Arabidopsis root and compared their behaviour with biological experiments. The simulations provide strong indications that spatial signals are required for realistic and flexible root growth, likely orchestrated by the plant hormones auxin and cytokinin.