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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.

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AUX1 Affects Lateral Root Initiation(A–D) AUX1-YFP accumulates uniformly in the pericycle cells on the outside of the curve prior to lateral root initiation. (A) 230 min before, (B) 90 min before, (C) 10 min after, and (D) 520 min after the first asymmetric cell division. Insets from (A) and (C) show AUX1 levels in a single founder cell. Left shows a blowup of (A); right, a blowup of (C). White asterisks indicate the pericycle cell files.(E) Simulation showing the effect of a 4-fold increased influx in the two most apical pericycle cells of the outer bend, resulting in a local maximum, shown by comparing the transversal profile through an AUX1-expressing cell row (red) with cell rows proximal (green) and distal (yellow) to the bend. Default bias caused solely by curvature is shown in blue.(F–I and K–N) Simulation in which the whole tissue is endowed with the same sigmoidal auxin-dependent AUX1 response; (F–I) show the increase in magnitude of the AUX1 response after bending that eventually becomes focused to the outer pericycle cells, using a logarithmic color map from black (no AUX1 expression) to white (high AUX1 expression), as indicated in color bar; (K–N) show the resulting corresponding auxin concentration profiles, presenting a localization and amplification of the maximum. Heatmap for auxin concentrations indicated below; 30 min (F and K), 1 h (G and L), 1.5 h (H and M), and 2 h (I and N) after root bend.(J) 1-NOA inhibits lateral root formation, with wild-type plants being more sensitive than aux1 mutants. Density of emerged lateral roots was determined 4 d after roots were transferred to fresh media, for that region of the root that grew after transfer. Error bars represent the standard error of the mean (SEM).
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pbio-0060307-g004: AUX1 Affects Lateral Root Initiation(A–D) AUX1-YFP accumulates uniformly in the pericycle cells on the outside of the curve prior to lateral root initiation. (A) 230 min before, (B) 90 min before, (C) 10 min after, and (D) 520 min after the first asymmetric cell division. Insets from (A) and (C) show AUX1 levels in a single founder cell. Left shows a blowup of (A); right, a blowup of (C). White asterisks indicate the pericycle cell files.(E) Simulation showing the effect of a 4-fold increased influx in the two most apical pericycle cells of the outer bend, resulting in a local maximum, shown by comparing the transversal profile through an AUX1-expressing cell row (red) with cell rows proximal (green) and distal (yellow) to the bend. Default bias caused solely by curvature is shown in blue.(F–I and K–N) Simulation in which the whole tissue is endowed with the same sigmoidal auxin-dependent AUX1 response; (F–I) show the increase in magnitude of the AUX1 response after bending that eventually becomes focused to the outer pericycle cells, using a logarithmic color map from black (no AUX1 expression) to white (high AUX1 expression), as indicated in color bar; (K–N) show the resulting corresponding auxin concentration profiles, presenting a localization and amplification of the maximum. Heatmap for auxin concentrations indicated below; 30 min (F and K), 1 h (G and L), 1.5 h (H and M), and 2 h (I and N) after root bend.(J) 1-NOA inhibits lateral root formation, with wild-type plants being more sensitive than aux1 mutants. Density of emerged lateral roots was determined 4 d after roots were transferred to fresh media, for that region of the root that grew after transfer. Error bars represent the standard error of the mean (SEM).

Mentions: Seedlings with loss-of-function mutations in AUX1 have decreased numbers of lateral roots [10] (Figure 5A), resulting from reduced rates of lateral root initiation [12]. To investigate how changes in AUX1 might be associated with lateral root formation, AUX1:YFP plants were gravistimulated for 4 h and then subjected to dynamic imaging. AUX1:YFP levels accumulated asymmetrically in the region of the bend, with levels on the outside of the curve being clearly higher than those on the inside (Figure 4A–4D; Video S2). Fluorescence intensity within the pericycle increased steadily before and after the first asymmetric cell divisions. Notably, the distribution of AUX1:YFP was relatively uniform within a single pericycle cell membrane (Figure 4C). The first cell divisions took place 2–3.5 h after imaging began, thus the increase in AUX1 along the vasculature occurs no later than the increase in auxin response in the founder cells, and likely before it (Figure 4A–4D).


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)

AUX1 Affects Lateral Root Initiation(A–D) AUX1-YFP accumulates uniformly in the pericycle cells on the outside of the curve prior to lateral root initiation. (A) 230 min before, (B) 90 min before, (C) 10 min after, and (D) 520 min after the first asymmetric cell division. Insets from (A) and (C) show AUX1 levels in a single founder cell. Left shows a blowup of (A); right, a blowup of (C). White asterisks indicate the pericycle cell files.(E) Simulation showing the effect of a 4-fold increased influx in the two most apical pericycle cells of the outer bend, resulting in a local maximum, shown by comparing the transversal profile through an AUX1-expressing cell row (red) with cell rows proximal (green) and distal (yellow) to the bend. Default bias caused solely by curvature is shown in blue.(F–I and K–N) Simulation in which the whole tissue is endowed with the same sigmoidal auxin-dependent AUX1 response; (F–I) show the increase in magnitude of the AUX1 response after bending that eventually becomes focused to the outer pericycle cells, using a logarithmic color map from black (no AUX1 expression) to white (high AUX1 expression), as indicated in color bar; (K–N) show the resulting corresponding auxin concentration profiles, presenting a localization and amplification of the maximum. Heatmap for auxin concentrations indicated below; 30 min (F and K), 1 h (G and L), 1.5 h (H and M), and 2 h (I and N) after root bend.(J) 1-NOA inhibits lateral root formation, with wild-type plants being more sensitive than aux1 mutants. Density of emerged lateral roots was determined 4 d after roots were transferred to fresh media, for that region of the root that grew after transfer. Error bars represent the standard error of the mean (SEM).
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Related In: Results  -  Collection

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

pbio-0060307-g004: AUX1 Affects Lateral Root Initiation(A–D) AUX1-YFP accumulates uniformly in the pericycle cells on the outside of the curve prior to lateral root initiation. (A) 230 min before, (B) 90 min before, (C) 10 min after, and (D) 520 min after the first asymmetric cell division. Insets from (A) and (C) show AUX1 levels in a single founder cell. Left shows a blowup of (A); right, a blowup of (C). White asterisks indicate the pericycle cell files.(E) Simulation showing the effect of a 4-fold increased influx in the two most apical pericycle cells of the outer bend, resulting in a local maximum, shown by comparing the transversal profile through an AUX1-expressing cell row (red) with cell rows proximal (green) and distal (yellow) to the bend. Default bias caused solely by curvature is shown in blue.(F–I and K–N) Simulation in which the whole tissue is endowed with the same sigmoidal auxin-dependent AUX1 response; (F–I) show the increase in magnitude of the AUX1 response after bending that eventually becomes focused to the outer pericycle cells, using a logarithmic color map from black (no AUX1 expression) to white (high AUX1 expression), as indicated in color bar; (K–N) show the resulting corresponding auxin concentration profiles, presenting a localization and amplification of the maximum. Heatmap for auxin concentrations indicated below; 30 min (F and K), 1 h (G and L), 1.5 h (H and M), and 2 h (I and N) after root bend.(J) 1-NOA inhibits lateral root formation, with wild-type plants being more sensitive than aux1 mutants. Density of emerged lateral roots was determined 4 d after roots were transferred to fresh media, for that region of the root that grew after transfer. Error bars represent the standard error of the mean (SEM).
Mentions: Seedlings with loss-of-function mutations in AUX1 have decreased numbers of lateral roots [10] (Figure 5A), resulting from reduced rates of lateral root initiation [12]. To investigate how changes in AUX1 might be associated with lateral root formation, AUX1:YFP plants were gravistimulated for 4 h and then subjected to dynamic imaging. AUX1:YFP levels accumulated asymmetrically in the region of the bend, with levels on the outside of the curve being clearly higher than those on the inside (Figure 4A–4D; Video S2). Fluorescence intensity within the pericycle increased steadily before and after the first asymmetric cell divisions. Notably, the distribution of AUX1:YFP was relatively uniform within a single pericycle cell membrane (Figure 4C). The first cell divisions took place 2–3.5 h after imaging began, thus the increase in AUX1 along the vasculature occurs no later than the increase in auxin response in the founder cells, and likely before it (Figure 4A–4D).

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