Limits...
Root system architecture from coupling cell shape to auxin transport.

Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Marée AF, Scheres B - PLoS Biol. (2008)

Bottom Line: The auxin import facilitator, AUX1, is up-regulated by auxin, resulting in additional local auxin import, thus creating a new auxin maximum that triggers organ formation.Longitudinal spacing of lateral roots is modulated by PIN proteins that promote auxin efflux, and pin2,3,7 triple mutants show impaired lateral inhibition.Thus, lateral root patterning combines a trigger, such as cell size difference due to bending, with a self-organizing system that mediates alterations in auxin transport.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Oberlin College, Oberlin, Ohio, USA.

ABSTRACT
Lateral organ position along roots and shoots largely determines plant architecture, and depends on auxin distribution patterns. Determination of the underlying patterning mechanisms has hitherto been complicated because they operate during growth and division. Here, we show by experiments and computational modeling that curvature of the Arabidopsis root influences cell sizes, which, together with tissue properties that determine auxin transport, induces higher auxin levels in the pericycle cells on the outside of the curve. The abundance and position of the auxin transporters restricts this response to the zone competent for lateral root formation. The auxin import facilitator, AUX1, is up-regulated by auxin, resulting in additional local auxin import, thus creating a new auxin maximum that triggers organ formation. Longitudinal spacing of lateral roots is modulated by PIN proteins that promote auxin efflux, and pin2,3,7 triple mutants show impaired lateral inhibition. Thus, lateral root patterning combines a trigger, such as cell size difference due to bending, with a self-organizing system that mediates alterations in auxin transport.

Show MeSH

Related in: MedlinePlus

Root and Model Layout(A) Image of a live root, with meristem (MZ), elongation (EZ), and differentiation (DZ) zones indicated.(B–E) PIN expression domains of (B1–B3) PIN1:GFP, (C1–C3) PIN2:GFP, (D1–D3) PIN3:GFP, and (E1–E3) PIN7:GFP. For B1, C1, D1, and E1, the GFP is shown in green and the propidium iodide (PI) stain in red. In B2, C2, D2, and E2 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP is shown in red and PI channel in blue. In B3, C3, D3, and E3 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP channel is shown in white. Laser and microscope settings were constant for each marker line. Scale bars represent 100 μm in overviews and 50 μm in enlargements.(F) The in silico root describes the epidermis ([ep]; blue), cortex ([c]; green), endodermis ([en]; yellow), pericycle ([p]; orange), and vasculature ([v]; red). QC (grey) and columella cells (cyan) are only in the distal MZ. Scale bars represent 100 μm. Model cell types are endowed with specific PIN topologies and strengths, which vary by zone. Differences between zones are indicated by changes in color tone. Red indicates strong PIN expression, blue weak. Typical cell lengths vary between zones, as indicated. Cell widths vary between tissue types and are kept constant through the zones. Parameter values are given in Protocol S1: Tables S1–S3 and Text S1.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2602721&req=5

pbio-0060307-g002: Root and Model Layout(A) Image of a live root, with meristem (MZ), elongation (EZ), and differentiation (DZ) zones indicated.(B–E) PIN expression domains of (B1–B3) PIN1:GFP, (C1–C3) PIN2:GFP, (D1–D3) PIN3:GFP, and (E1–E3) PIN7:GFP. For B1, C1, D1, and E1, the GFP is shown in green and the propidium iodide (PI) stain in red. In B2, C2, D2, and E2 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP is shown in red and PI channel in blue. In B3, C3, D3, and E3 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP channel is shown in white. Laser and microscope settings were constant for each marker line. Scale bars represent 100 μm in overviews and 50 μm in enlargements.(F) The in silico root describes the epidermis ([ep]; blue), cortex ([c]; green), endodermis ([en]; yellow), pericycle ([p]; orange), and vasculature ([v]; red). QC (grey) and columella cells (cyan) are only in the distal MZ. Scale bars represent 100 μm. Model cell types are endowed with specific PIN topologies and strengths, which vary by zone. Differences between zones are indicated by changes in color tone. Red indicates strong PIN expression, blue weak. Typical cell lengths vary between zones, as indicated. Cell widths vary between tissue types and are kept constant through the zones. Parameter values are given in Protocol S1: Tables S1–S3 and Text S1.

Mentions: To understand how root curvature affects lateral root initiation, we developed a model that describes the dynamics of auxin transport through the root. In the model, we consider that auxin can only diffuse freely within cells and in the cell wall, whereas passage of auxin over cell membranes is determined by permeability properties. The efflux and influx permeability values are enhanced by the presence of PIN and AUX1 expression, respectively. The model captures the following basic biophysical characteristics of the system: (1) the overall cell geometries and tissue types; (2) typical lineage- and zone-dependent PIN distributions and expression levels; (3) cell-shape changes due to a mechanical alteration of curvature of the whole organ; and (4) auxin transport itself (see Protocol S1: Tables S1–S3 and Text S1 for a detailed discussion). Given the discrete nature of cells, and the manner in which free diffusion of auxin is interrupted by membranes, auxin dynamics may be strongly influenced by cell shape. The in silico root layout is therefore constructed using typical cell lengths and widths within the MZ, EZ, and DZ. In live roots, cells in the MZ are smaller, but transiently increase length when in the EZ, until reaching a maximally elongated state in the DZ. This is modeled by selecting different characteristic cell lengths for each of the three zones. Differences in width between the external cell files, and the thinner nature of the vascular cells, are also included (Figure 2F and Protocol S1: Text S1 for details). Such models are necessary because simple, intuitive predictions of auxin flow based only on the location of auxin transporters neglect important factors that determine flux patterns within the context of the whole tissue, including the impact of cell size and shape and the fact that the amount of flux through the transport facilitators is determined by the substrate concentrations [19–22].


Root system architecture from coupling cell shape to auxin transport.

Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Marée AF, Scheres B - PLoS Biol. (2008)

Root and Model Layout(A) Image of a live root, with meristem (MZ), elongation (EZ), and differentiation (DZ) zones indicated.(B–E) PIN expression domains of (B1–B3) PIN1:GFP, (C1–C3) PIN2:GFP, (D1–D3) PIN3:GFP, and (E1–E3) PIN7:GFP. For B1, C1, D1, and E1, the GFP is shown in green and the propidium iodide (PI) stain in red. In B2, C2, D2, and E2 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP is shown in red and PI channel in blue. In B3, C3, D3, and E3 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP channel is shown in white. Laser and microscope settings were constant for each marker line. Scale bars represent 100 μm in overviews and 50 μm in enlargements.(F) The in silico root describes the epidermis ([ep]; blue), cortex ([c]; green), endodermis ([en]; yellow), pericycle ([p]; orange), and vasculature ([v]; red). QC (grey) and columella cells (cyan) are only in the distal MZ. Scale bars represent 100 μm. Model cell types are endowed with specific PIN topologies and strengths, which vary by zone. Differences between zones are indicated by changes in color tone. Red indicates strong PIN expression, blue weak. Typical cell lengths vary between zones, as indicated. Cell widths vary between tissue types and are kept constant through the zones. Parameter values are given in Protocol S1: Tables S1–S3 and Text S1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2602721&req=5

pbio-0060307-g002: Root and Model Layout(A) Image of a live root, with meristem (MZ), elongation (EZ), and differentiation (DZ) zones indicated.(B–E) PIN expression domains of (B1–B3) PIN1:GFP, (C1–C3) PIN2:GFP, (D1–D3) PIN3:GFP, and (E1–E3) PIN7:GFP. For B1, C1, D1, and E1, the GFP is shown in green and the propidium iodide (PI) stain in red. In B2, C2, D2, and E2 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP is shown in red and PI channel in blue. In B3, C3, D3, and E3 (enlargements of the insets of the DZ, EZ, and MZ in overviews B1, C1, D1, and E1, respectively), the GFP channel is shown in white. Laser and microscope settings were constant for each marker line. Scale bars represent 100 μm in overviews and 50 μm in enlargements.(F) The in silico root describes the epidermis ([ep]; blue), cortex ([c]; green), endodermis ([en]; yellow), pericycle ([p]; orange), and vasculature ([v]; red). QC (grey) and columella cells (cyan) are only in the distal MZ. Scale bars represent 100 μm. Model cell types are endowed with specific PIN topologies and strengths, which vary by zone. Differences between zones are indicated by changes in color tone. Red indicates strong PIN expression, blue weak. Typical cell lengths vary between zones, as indicated. Cell widths vary between tissue types and are kept constant through the zones. Parameter values are given in Protocol S1: Tables S1–S3 and Text S1.
Mentions: To understand how root curvature affects lateral root initiation, we developed a model that describes the dynamics of auxin transport through the root. In the model, we consider that auxin can only diffuse freely within cells and in the cell wall, whereas passage of auxin over cell membranes is determined by permeability properties. The efflux and influx permeability values are enhanced by the presence of PIN and AUX1 expression, respectively. The model captures the following basic biophysical characteristics of the system: (1) the overall cell geometries and tissue types; (2) typical lineage- and zone-dependent PIN distributions and expression levels; (3) cell-shape changes due to a mechanical alteration of curvature of the whole organ; and (4) auxin transport itself (see Protocol S1: Tables S1–S3 and Text S1 for a detailed discussion). Given the discrete nature of cells, and the manner in which free diffusion of auxin is interrupted by membranes, auxin dynamics may be strongly influenced by cell shape. The in silico root layout is therefore constructed using typical cell lengths and widths within the MZ, EZ, and DZ. In live roots, cells in the MZ are smaller, but transiently increase length when in the EZ, until reaching a maximally elongated state in the DZ. This is modeled by selecting different characteristic cell lengths for each of the three zones. Differences in width between the external cell files, and the thinner nature of the vascular cells, are also included (Figure 2F and Protocol S1: Text S1 for details). Such models are necessary because simple, intuitive predictions of auxin flow based only on the location of auxin transporters neglect important factors that determine flux patterns within the context of the whole tissue, including the impact of cell size and shape and the fact that the amount of flux through the transport facilitators is determined by the substrate concentrations [19–22].

Bottom Line: The auxin import facilitator, AUX1, is up-regulated by auxin, resulting in additional local auxin import, thus creating a new auxin maximum that triggers organ formation.Longitudinal spacing of lateral roots is modulated by PIN proteins that promote auxin efflux, and pin2,3,7 triple mutants show impaired lateral inhibition.Thus, lateral root patterning combines a trigger, such as cell size difference due to bending, with a self-organizing system that mediates alterations in auxin transport.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Oberlin College, Oberlin, Ohio, USA.

ABSTRACT
Lateral organ position along roots and shoots largely determines plant architecture, and depends on auxin distribution patterns. Determination of the underlying patterning mechanisms has hitherto been complicated because they operate during growth and division. Here, we show by experiments and computational modeling that curvature of the Arabidopsis root influences cell sizes, which, together with tissue properties that determine auxin transport, induces higher auxin levels in the pericycle cells on the outside of the curve. The abundance and position of the auxin transporters restricts this response to the zone competent for lateral root formation. The auxin import facilitator, AUX1, is up-regulated by auxin, resulting in additional local auxin import, thus creating a new auxin maximum that triggers organ formation. Longitudinal spacing of lateral roots is modulated by PIN proteins that promote auxin efflux, and pin2,3,7 triple mutants show impaired lateral inhibition. Thus, lateral root patterning combines a trigger, such as cell size difference due to bending, with a self-organizing system that mediates alterations in auxin transport.

Show MeSH
Related in: MedlinePlus