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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.

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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Mitotic activity in the root and its simulation. a. The scheme of root tip structure in Arabidopsis. The cells of different types marked by different colors (for details, see figure 1). b. Qualitative profile of mitotic activity in cells along the central root axis. Two maxima of mitotic activity are distinguished along the central root axis according to Dolan et al. (1993) [1] and Beemster and Baskin (2000) [27]. c. The model solution: auxin (red squares) and substance Y (blue circles) distributions regulate the rates of cell divisions in the root (gray columns). The dynamical characteristics (cell coordinates on the axis, auxin concentration, and division rates) in the model solutions reproduce root patterning, where the cells of different types are specifying around the distal auxin maximum. d. The plot of auxin-regulated Y degradation rate used in the model (Eq. (8)). (E) The plot of Y-regulated rates of cell division (first coefficient in Eq. (10)). QC is the quiescent center and RCI is the root cap initial.
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Figure 3: Mitotic activity in the root and its simulation. a. The scheme of root tip structure in Arabidopsis. The cells of different types marked by different colors (for details, see figure 1). b. Qualitative profile of mitotic activity in cells along the central root axis. Two maxima of mitotic activity are distinguished along the central root axis according to Dolan et al. (1993) [1] and Beemster and Baskin (2000) [27]. c. The model solution: auxin (red squares) and substance Y (blue circles) distributions regulate the rates of cell divisions in the root (gray columns). The dynamical characteristics (cell coordinates on the axis, auxin concentration, and division rates) in the model solutions reproduce root patterning, where the cells of different types are specifying around the distal auxin maximum. d. The plot of auxin-regulated Y degradation rate used in the model (Eq. (8)). (E) The plot of Y-regulated rates of cell division (first coefficient in Eq. (10)). QC is the quiescent center and RCI is the root cap initial.

Mentions: The profile of cell mitotic activity along the meristematic zone of the root is bell-shaped with the maximum located at a distance of 10-16 cells from the QC [27]. Taking into account also the dividing root cap initials [1], the profile of mitotic activity in the whole root acquires two maxima of the division rate along the central root axis (Figure 3A, B).


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)

Mitotic activity in the root and its simulation. a. The scheme of root tip structure in Arabidopsis. The cells of different types marked by different colors (for details, see figure 1). b. Qualitative profile of mitotic activity in cells along the central root axis. Two maxima of mitotic activity are distinguished along the central root axis according to Dolan et al. (1993) [1] and Beemster and Baskin (2000) [27]. c. The model solution: auxin (red squares) and substance Y (blue circles) distributions regulate the rates of cell divisions in the root (gray columns). The dynamical characteristics (cell coordinates on the axis, auxin concentration, and division rates) in the model solutions reproduce root patterning, where the cells of different types are specifying around the distal auxin maximum. d. The plot of auxin-regulated Y degradation rate used in the model (Eq. (8)). (E) The plot of Y-regulated rates of cell division (first coefficient in Eq. (10)). QC is the quiescent center and RCI is the root cap initial.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2921385&req=5

Figure 3: Mitotic activity in the root and its simulation. a. The scheme of root tip structure in Arabidopsis. The cells of different types marked by different colors (for details, see figure 1). b. Qualitative profile of mitotic activity in cells along the central root axis. Two maxima of mitotic activity are distinguished along the central root axis according to Dolan et al. (1993) [1] and Beemster and Baskin (2000) [27]. c. The model solution: auxin (red squares) and substance Y (blue circles) distributions regulate the rates of cell divisions in the root (gray columns). The dynamical characteristics (cell coordinates on the axis, auxin concentration, and division rates) in the model solutions reproduce root patterning, where the cells of different types are specifying around the distal auxin maximum. d. The plot of auxin-regulated Y degradation rate used in the model (Eq. (8)). (E) The plot of Y-regulated rates of cell division (first coefficient in Eq. (10)). QC is the quiescent center and RCI is the root cap initial.
Mentions: The profile of cell mitotic activity along the meristematic zone of the root is bell-shaped with the maximum located at a distance of 10-16 cells from the QC [27]. Taking into account also the dividing root cap initials [1], the profile of mitotic activity in the whole root acquires two maxima of the division rate along the central root axis (Figure 3A, B).

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.

Show MeSH