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A plausible mechanism for auxin patterning along the developing root.

Mironova VV, Omelyanchuk NA, Yosiphon G, Fadeev SI, Kolchanov NA, Mjolsness E, Likhoshvai VA - BMC Syst Biol (2010)

Bottom Line: In addition, the proximal maxima are formed under the reflected flow mechanism in response to periods of increasing auxin flow from the growing shoot.These events may predetermine lateral root initiation in a rhyzotactic pattern.Another outcome of the reflected flow mechanism - the predominance of lateral or adventitious roots in different plant species - may be based on the different efficiencies with which auxin inhibits its own transport in different species, thereby distinguishing two main types of plant root architecture: taproot vs. fibrous.

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Affiliation: Institute of Cytology and Genetics, SB RAS, Lavrentyeva 10, Novosibirsk, Russia.

ABSTRACT

Background: In plant roots, auxin is critical for patterning and morphogenesis. It regulates cell elongation and division, the development and maintenance of root apical meristems, and other processes. In Arabidopsis, auxin distribution along the central root axis has several maxima: in the root tip, in the basal meristem and at the shoot/root junction. The distal maximum in the root tip maintains the stem cell niche. Proximal maxima may trigger lateral or adventitious root initiation.

Results: We propose a reflected flow mechanism for the formation of the auxin maximum in the root apical meristem. The mechanism is based on auxin's known activation and inhibition of expressed PIN family auxin carriers at low and high auxin levels, respectively. Simulations showed that these regulatory interactions are sufficient for self-organization of the auxin distribution pattern along the central root axis under varying conditions. The mathematical model was extended with rules for discontinuous cell dynamics so that cell divisions were also governed by auxin, and by another morphogen Division Factor which combines the actions of cytokinin and ethylene on cell division in the root. The positional information specified by the gradients of these two morphogens is able to explain root patterning along the central root axis.

Conclusion: We present here a plausible mechanism for auxin patterning along the developing root, that may provide for self-organization of the distal auxin maximum when the reverse fountain has not yet been formed or has been disrupted. In addition, the proximal maxima are formed under the reflected flow mechanism in response to periods of increasing auxin flow from the growing shoot. These events may predetermine lateral root initiation in a rhyzotactic pattern. Another outcome of the reflected flow mechanism - the predominance of lateral or adventitious roots in different plant species - may be based on the different efficiencies with which auxin inhibits its own transport in different species, thereby distinguishing two main types of plant root architecture: taproot vs. fibrous.

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The auxin distribution pattern reproduced by the model. a. Expression of DR5::GUS detects the auxin pattern in the root tip (adapted from Sabatini et al., 1999; [3]). b. The surface plot of DR5 activity in the root tip scanned from figure 2a by ImageJ program. The x axis corresponds to the central axis of the root; the root width extends along the y axis; and the z axis shows DR5 activity. c. The model solution (black line) agrees well with semi-quantitative data of auxin distribution along the central root axis, obtained from the surface plot at figure 2b (red line). d. The auxin distribution pattern in the stationary solution of the 2D minimal model. Blue arrowhead denotes the QC position.
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Figure 4: The auxin distribution pattern reproduced by the model. a. Expression of DR5::GUS detects the auxin pattern in the root tip (adapted from Sabatini et al., 1999; [3]). b. The surface plot of DR5 activity in the root tip scanned from figure 2a by ImageJ program. The x axis corresponds to the central axis of the root; the root width extends along the y axis; and the z axis shows DR5 activity. c. The model solution (black line) agrees well with semi-quantitative data of auxin distribution along the central root axis, obtained from the surface plot at figure 2b (red line). d. The auxin distribution pattern in the stationary solution of the 2D minimal model. Blue arrowhead denotes the QC position.

Mentions: A characteristic feature of auxin distribution patterns in the root is the presence of concentration maximum in the root cap initial cells (Figure 4A, B; [3]). We have hypothesized that auxin regulation of its own transport with positive and negative feedbacks (Figure 1B) is a sufficient condition for formation of this characteristic auxin distribution pattern in a functionally uniform cell array. To verify this hypothesis, we constructed 1D and 2D minimal mathematical models that take into account auxin and PIN1 concentrations dynamics (see the Methods section). The 1D minimal model (7) describes the auxin distribution (from a source in the shoot) over a linear array of non-dividing cells located along the central root axis (Figure 1A). The same processes take place in each cell of the model except for the cells at both ends of the root due to necessary boundary conditions. For the 1D minimal model with number of cell N = 50, we estimated several sets of parameter values that gave steady-state solutions with auxin distribution matching the experimentally observed pattern reported by Sabatini et al. (1999) ([3]; Figure 4B-C; [Additional files 1: Text S3; 3; 4: I]). Two of them, the "basic" [Additional file 4: II] and the "robust" [Additional file 4: III] are used in the present work for the model analysis.


A plausible mechanism for auxin patterning along the developing root.

Mironova VV, Omelyanchuk NA, Yosiphon G, Fadeev SI, Kolchanov NA, Mjolsness E, Likhoshvai VA - BMC Syst Biol (2010)

The auxin distribution pattern reproduced by the model. a. Expression of DR5::GUS detects the auxin pattern in the root tip (adapted from Sabatini et al., 1999; [3]). b. The surface plot of DR5 activity in the root tip scanned from figure 2a by ImageJ program. The x axis corresponds to the central axis of the root; the root width extends along the y axis; and the z axis shows DR5 activity. c. The model solution (black line) agrees well with semi-quantitative data of auxin distribution along the central root axis, obtained from the surface plot at figure 2b (red line). d. The auxin distribution pattern in the stationary solution of the 2D minimal model. Blue arrowhead denotes the QC position.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 4: The auxin distribution pattern reproduced by the model. a. Expression of DR5::GUS detects the auxin pattern in the root tip (adapted from Sabatini et al., 1999; [3]). b. The surface plot of DR5 activity in the root tip scanned from figure 2a by ImageJ program. The x axis corresponds to the central axis of the root; the root width extends along the y axis; and the z axis shows DR5 activity. c. The model solution (black line) agrees well with semi-quantitative data of auxin distribution along the central root axis, obtained from the surface plot at figure 2b (red line). d. The auxin distribution pattern in the stationary solution of the 2D minimal model. Blue arrowhead denotes the QC position.
Mentions: A characteristic feature of auxin distribution patterns in the root is the presence of concentration maximum in the root cap initial cells (Figure 4A, B; [3]). We have hypothesized that auxin regulation of its own transport with positive and negative feedbacks (Figure 1B) is a sufficient condition for formation of this characteristic auxin distribution pattern in a functionally uniform cell array. To verify this hypothesis, we constructed 1D and 2D minimal mathematical models that take into account auxin and PIN1 concentrations dynamics (see the Methods section). The 1D minimal model (7) describes the auxin distribution (from a source in the shoot) over a linear array of non-dividing cells located along the central root axis (Figure 1A). The same processes take place in each cell of the model except for the cells at both ends of the root due to necessary boundary conditions. For the 1D minimal model with number of cell N = 50, we estimated several sets of parameter values that gave steady-state solutions with auxin distribution matching the experimentally observed pattern reported by Sabatini et al. (1999) ([3]; Figure 4B-C; [Additional files 1: Text S3; 3; 4: I]). Two of them, the "basic" [Additional file 4: II] and the "robust" [Additional file 4: III] are used in the present work for the model analysis.

Bottom Line: In addition, the proximal maxima are formed under the reflected flow mechanism in response to periods of increasing auxin flow from the growing shoot.These events may predetermine lateral root initiation in a rhyzotactic pattern.Another outcome of the reflected flow mechanism - the predominance of lateral or adventitious roots in different plant species - may be based on the different efficiencies with which auxin inhibits its own transport in different species, thereby distinguishing two main types of plant root architecture: taproot vs. fibrous.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Cytology and Genetics, SB RAS, Lavrentyeva 10, Novosibirsk, Russia.

ABSTRACT

Background: In plant roots, auxin is critical for patterning and morphogenesis. It regulates cell elongation and division, the development and maintenance of root apical meristems, and other processes. In Arabidopsis, auxin distribution along the central root axis has several maxima: in the root tip, in the basal meristem and at the shoot/root junction. The distal maximum in the root tip maintains the stem cell niche. Proximal maxima may trigger lateral or adventitious root initiation.

Results: We propose a reflected flow mechanism for the formation of the auxin maximum in the root apical meristem. The mechanism is based on auxin's known activation and inhibition of expressed PIN family auxin carriers at low and high auxin levels, respectively. Simulations showed that these regulatory interactions are sufficient for self-organization of the auxin distribution pattern along the central root axis under varying conditions. The mathematical model was extended with rules for discontinuous cell dynamics so that cell divisions were also governed by auxin, and by another morphogen Division Factor which combines the actions of cytokinin and ethylene on cell division in the root. The positional information specified by the gradients of these two morphogens is able to explain root patterning along the central root axis.

Conclusion: We present here a plausible mechanism for auxin patterning along the developing root, that may provide for self-organization of the distal auxin maximum when the reverse fountain has not yet been formed or has been disrupted. In addition, the proximal maxima are formed under the reflected flow mechanism in response to periods of increasing auxin flow from the growing shoot. These events may predetermine lateral root initiation in a rhyzotactic pattern. Another outcome of the reflected flow mechanism - the predominance of lateral or adventitious roots in different plant species - may be based on the different efficiencies with which auxin inhibits its own transport in different species, thereby distinguishing two main types of plant root architecture: taproot vs. fibrous.

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