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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.

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Experimental cell length distribution.Cell length distribution along the principal growth axis (distance from the QC/quiescent centre) determined for a typical 7-day-old Arabidopsis seedling root. Experimental set-up and growth conditions were in accordance with Beemster and Baskin [5]. The data points represent epidermal cell lengths. The ‘polyloc method’ was used for curve fitting (full line, cf.Methods).
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pcbi-1003910-g002: Experimental cell length distribution.Cell length distribution along the principal growth axis (distance from the QC/quiescent centre) determined for a typical 7-day-old Arabidopsis seedling root. Experimental set-up and growth conditions were in accordance with Beemster and Baskin [5]. The data points represent epidermal cell lengths. The ‘polyloc method’ was used for curve fitting (full line, cf.Methods).

Mentions: Since only averaged data or progress curves have been reported of cell length distributions along the primary root axis of Arabidopsis, we have generated a new curve (Figure 2) based on plants cultured in the same growth conditions as in [5].


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)

Experimental cell length distribution.Cell length distribution along the principal growth axis (distance from the QC/quiescent centre) determined for a typical 7-day-old Arabidopsis seedling root. Experimental set-up and growth conditions were in accordance with Beemster and Baskin [5]. The data points represent epidermal cell lengths. The ‘polyloc method’ was used for curve fitting (full line, cf.Methods).
© Copyright Policy
Related In: Results  -  Collection

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

pcbi-1003910-g002: Experimental cell length distribution.Cell length distribution along the principal growth axis (distance from the QC/quiescent centre) determined for a typical 7-day-old Arabidopsis seedling root. Experimental set-up and growth conditions were in accordance with Beemster and Baskin [5]. The data points represent epidermal cell lengths. The ‘polyloc method’ was used for curve fitting (full line, cf.Methods).
Mentions: Since only averaged data or progress curves have been reported of cell length distributions along the primary root axis of Arabidopsis, we have generated a new curve (Figure 2) based on plants cultured in the same growth conditions as in [5].

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