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

Abstract

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.

The build-up of osmotic stress responses within the growing root apex using kinematics and RNA-sequencing

“…The importance of apical meristem activity in determining growth rate has been highlighted (Beemster and Baskin, 1998), and its sensitivity to water deficit has been shown in maize and poplar roots (Fraser et al , 1990; Sacks et al , 1997; Bizet et al , 2015 b ). The balance between proliferation and elongation processes, as well as their underlying molecular control, is a current research focus (Tardieu et al , 2011; Baskin, 2013; De Vos et al , 2014). A gene expression map at high spatial resolution has led to better knowledge of the transcriptional circuits linked to root development in Arabidopsis thaliana (Birnbaum et al , 2003; Brady et al , 2007; Iyer-Pascuzzi et al , 2009).…”

Mechanical Behavior of Cells within a Cell-Based Model of Wheat Leaf Growth

“…For example, in the model of Vos et al (2014), vertices are constrained to move only parallel to the longitudinal axis of the root. This allows for the anisotropic elastic-plastic properties of the cell-wall material to be taken into account.…”

“…Vos et al (2014) also considered such a growth function (for the cell target volume) as one of the options in the vertex-based simulation of Arabidopsis root growth. At the same time, in a number of studies (Barlow, 1969; van der Weele et al, 2003) based on experimental data on cell length profiles along the growth axis of the Arabidopsis root, the authors suggested a smooth non-linear growth function for the cell length.…”

“…Our assumption of the stationary location of the two zones with respect to the leaf base is based on the model of switching between two zones due to morphogenetic mechanisms. For instance, such a model was used in the work of Vos et al (2014) in the simulation of Arabidopsis thaliana root growth. Similar molecular mechanisms were used for justifying the stable location of the growth zone size in the shoot apical meristem of A. thaliana in our earlier work (Nikolaev et al, 2011).…”

Modelling Plant Hormone Gradients

“…how hormonal crosstalk influences the size of the root meristem (de Vos et al, 2014); and how this crosstalk can lead to the emergence of gene expression patterns (Liu et al 2010;Moore et al 2015a).…”