Limits...
Putting theory to the test: which regulatory mechanisms can drive realistic growth of a root?

De Vos D, Vissenberg K, Broeckhove J, Beemster GT - PLoS Comput. Biol. (2014)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Molecular Plant Physiology and Biotechnology, Department of Biology, University of Antwerp, Antwerp, Belgium.

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.

Show MeSH

Related in: MedlinePlus

Cytokinin-auxin cross-talk in root development.Simulation output of Model 12 (Table S1). (A) Schematic view of regulatory interactions between model variables (in italics) and PIN exporters. Dotted lines illustrate potential cross-talk with gibberellin (GA) signalling (auxin stimulating GA and GA inhibiting cytokinin signalling) not included in the model. GA is represented in the model as an independent signal that undergoes growth-dilution, thereby determining the exit from elongation [19]. (B) Simulation output at 30 h with blue colouring relative to the SHY2 concentration. A domain with strong SHY2 expression is present. (C–E) Colouring of the cell grid is according to the auxin concentration in arbitrary units (‘AU’). Notice a transition from a (basal) linear gradient to a (apical) 2D gradient dominated by polar transport. This is caused by the PIN inhibition at the SHY2 expression domain. The extent of the division zone (DZ) is indicated. (D) Simulation of this model with a 4-fold stronger auxin source shows that the DZ is expanded. (E) Simulation of this model with a 4-fold stronger cytokinin source shows that the DZ has shrunk considerably. This corresponds to observations from Beemster and Baskin [34] on treatment of Arabidopsis root with auxin and cytokinin analogues.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4214622&req=5

pcbi-1003910-g009: Cytokinin-auxin cross-talk in root development.Simulation output of Model 12 (Table S1). (A) Schematic view of regulatory interactions between model variables (in italics) and PIN exporters. Dotted lines illustrate potential cross-talk with gibberellin (GA) signalling (auxin stimulating GA and GA inhibiting cytokinin signalling) not included in the model. GA is represented in the model as an independent signal that undergoes growth-dilution, thereby determining the exit from elongation [19]. (B) Simulation output at 30 h with blue colouring relative to the SHY2 concentration. A domain with strong SHY2 expression is present. (C–E) Colouring of the cell grid is according to the auxin concentration in arbitrary units (‘AU’). Notice a transition from a (basal) linear gradient to a (apical) 2D gradient dominated by polar transport. This is caused by the PIN inhibition at the SHY2 expression domain. The extent of the division zone (DZ) is indicated. (D) Simulation of this model with a 4-fold stronger auxin source shows that the DZ is expanded. (E) Simulation of this model with a 4-fold stronger cytokinin source shows that the DZ has shrunk considerably. This corresponds to observations from Beemster and Baskin [34] on treatment of Arabidopsis root with auxin and cytokinin analogues.

Mentions: A consequence of the symplastic growth of the root is that at a given distance from the tip all cells have the same relative expansion rate [32]. As stated by Ivanov [33], any observed difference in cell lengths between tissues must therefore reflect differences in cell proliferation (see also [26]). Inversely, any form of growth regulation that results in different elongation rates for cells at the same distance from the tip would disrupt symplastic growth (Figure 1A). For instance, suppose all cells at the same (vertical) position in a downward growing root have the same absolute (areal) expansion rate, irrespective of their size (Model 1, Tables 1 and S1). With inner cell files narrower than outer cell files (similar to the real root) this fixed size increment results in consistently larger relative elongation rates for the inner tissue layers leading to tissue distortion and unbalanced distribution of mechanical stresses (Figure 1B and C). Note that the same situation would occur when adjacent files contain cells of similar width, but different lengths growing at the same absolute rates. Hence, non-uniform relative strain rates at some position along the principal growth axis eventually lead to malformations.


Putting theory to the test: which regulatory mechanisms can drive realistic growth of a root?

De Vos D, Vissenberg K, Broeckhove J, Beemster GT - PLoS Comput. Biol. (2014)

Cytokinin-auxin cross-talk in root development.Simulation output of Model 12 (Table S1). (A) Schematic view of regulatory interactions between model variables (in italics) and PIN exporters. Dotted lines illustrate potential cross-talk with gibberellin (GA) signalling (auxin stimulating GA and GA inhibiting cytokinin signalling) not included in the model. GA is represented in the model as an independent signal that undergoes growth-dilution, thereby determining the exit from elongation [19]. (B) Simulation output at 30 h with blue colouring relative to the SHY2 concentration. A domain with strong SHY2 expression is present. (C–E) Colouring of the cell grid is according to the auxin concentration in arbitrary units (‘AU’). Notice a transition from a (basal) linear gradient to a (apical) 2D gradient dominated by polar transport. This is caused by the PIN inhibition at the SHY2 expression domain. The extent of the division zone (DZ) is indicated. (D) Simulation of this model with a 4-fold stronger auxin source shows that the DZ is expanded. (E) Simulation of this model with a 4-fold stronger cytokinin source shows that the DZ has shrunk considerably. This corresponds to observations from Beemster and Baskin [34] on treatment of Arabidopsis root with auxin and cytokinin analogues.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4214622&req=5

pcbi-1003910-g009: Cytokinin-auxin cross-talk in root development.Simulation output of Model 12 (Table S1). (A) Schematic view of regulatory interactions between model variables (in italics) and PIN exporters. Dotted lines illustrate potential cross-talk with gibberellin (GA) signalling (auxin stimulating GA and GA inhibiting cytokinin signalling) not included in the model. GA is represented in the model as an independent signal that undergoes growth-dilution, thereby determining the exit from elongation [19]. (B) Simulation output at 30 h with blue colouring relative to the SHY2 concentration. A domain with strong SHY2 expression is present. (C–E) Colouring of the cell grid is according to the auxin concentration in arbitrary units (‘AU’). Notice a transition from a (basal) linear gradient to a (apical) 2D gradient dominated by polar transport. This is caused by the PIN inhibition at the SHY2 expression domain. The extent of the division zone (DZ) is indicated. (D) Simulation of this model with a 4-fold stronger auxin source shows that the DZ is expanded. (E) Simulation of this model with a 4-fold stronger cytokinin source shows that the DZ has shrunk considerably. This corresponds to observations from Beemster and Baskin [34] on treatment of Arabidopsis root with auxin and cytokinin analogues.
Mentions: A consequence of the symplastic growth of the root is that at a given distance from the tip all cells have the same relative expansion rate [32]. As stated by Ivanov [33], any observed difference in cell lengths between tissues must therefore reflect differences in cell proliferation (see also [26]). Inversely, any form of growth regulation that results in different elongation rates for cells at the same distance from the tip would disrupt symplastic growth (Figure 1A). For instance, suppose all cells at the same (vertical) position in a downward growing root have the same absolute (areal) expansion rate, irrespective of their size (Model 1, Tables 1 and S1). With inner cell files narrower than outer cell files (similar to the real root) this fixed size increment results in consistently larger relative elongation rates for the inner tissue layers leading to tissue distortion and unbalanced distribution of mechanical stresses (Figure 1B and C). Note that the same situation would occur when adjacent files contain cells of similar width, but different lengths growing at the same absolute rates. Hence, non-uniform relative strain rates at some position along the principal growth axis eventually lead to malformations.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Molecular Plant Physiology and Biotechnology, Department of Biology, University of Antwerp, Antwerp, Belgium.

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.

Show MeSH
Related in: MedlinePlus