Auxin transport is sufficient to generate a maximum and gradient guiding root growth

Abstract

The plant growth regulator auxin controls cell identity, cell division and cell expansion. Auxin efflux facilitators (PINs) are associated with auxin maxima in distal regions of both shoots and roots. Here we model diffusion and PIN-facilitated auxin transport in and across cells within a structured root layout. In our model, the stable accumulation of auxin in a distal maximum emerges from the auxin flux pattern. We have experimentally tested model predictions of robustness and self-organization. Our model explains pattern formation and morphogenesis at timescales from seconds to weeks, and can be understood by conceptualizing the root as an ‘auxin capacitor’. A robust auxin gradient associated with the maximum, in combination with separable roles of auxin in cell division and cell expansion, is able to explain the formation, maintenance and growth of sharply bounded meristematic and elongation zones. Directional permeability and diffusion can fully account for stable auxin maxima and gradients that can instruct morphogenesis.

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Figure 1: Mesoscopic model for polar auxin transport.
Figure 2: Auxin maximum in simulations (a–k) and experiments (l–p).
Figure 3: An autonomous auxin capacitor in cut-root simulations (a, b) and experiments (c, d).
Figure 4: Repositioning of the maximum owing to ablation and in the pin triple mutant, in simulations (a–e, upper panels, and f–h) and experiments (a–e, lower panels).
Figure 5: Root growth and zonation in simulations (a–n, q–t) and experiments (o, p).

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Acknowledgements

A.F.M.M. and B.S. are supported by the Netherlands Organization for Scientific Research (NWO). We thank I. Blilou for experiments performed in the early phase of this study and discussions. We acknowledge T. Berleth and K. Ljung for helpful comments.

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Correspondence to Ben Scheres.

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Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-10 with Legends, Supplementary Tables 1-4, Legends to the Supplementary Movies 1-8 and Supplementary Methods with additional references. (PDF 10134 kb)

Supplementary Movie 1

The file contains Supplementary Movie 1 which shows establishment of the auxin maximum in a root receiving shoot-derived auxin influx (simulation of Fig. 2b). Relative auxin concentrations according to the colour bar of Fig. 2d. Scale bar 1 00µm. (MPG 6516 kb)

Supplementary Movie 2

The file contains Supplementary Movie 2 which shows establishment of the auxin maximum solely through ubiquitous auxin production (simulation of Figs. 2g,h). Absolute auxin concentrations according to colour bar indicated in movie. (MPG 3898 kb)

Supplementary Movie 3

The file contains Supplementary Movie 3 which shows establishment of the auxin maximum within a root immersed in auxin, and receiving no additional auxin influx contribution (simulation of Figs. 2i-k). Relative auxin concentration according to the colour bar of Fig. 2d. (MPG 6456 kb)

Supplementary Movie 4

The file contains Supplementary Movie 4 which shows dynamical changes in auxin concentration profile before and after root cut (simulation of Figs. 3a-b). Relative log auxin concentration according to the colour bar of Fig. 3. Moment of root cut is indicated by the change in colour of the clock. (MPG 3374 kb)

Supplementary Movie 5

The file contains Supplementary Movie 5 which shows reestablishment of the auxin maximum after ‘QC’ ablation (simulation of Figs. 4a1-c1). Relative auxin concentrations according to the colour bar of Fig. 2d. (MPG 2598 kb)

Supplementary Movie 6

The file contains Supplementary Movie 6 which shows root growth of an ‘intact’ root over a period of 8 days (simulation of Figs. 5d-k). Relative auxin concentrations according to the colour bar of Fig. 2d. (MPG 8790 kb)

Supplementary Movie 7

The file contains Supplementary Movie 7 which shows 2 days of growth of an ‘intact’ root, followed by a further 6 days of growth while lacking shoot influx, i.e. root cut (simulations of Figs. 5l-t). Colours given by relative log scale through colour bar of Fig. 3 (left) and relative scale through colour bar of Fig. 2d (middle and right). Moment of root cut is indicated by the change in colour of the clock. (MPG 8560 kb)

Supplementary Movie 8

The file contains Supplementary Movie 8 which shows establishment of the auxin maximum solely through localised (one cell) auxin production (simulations of Supplementary Figure 5). Relative auxin concentration according to the colour bar of Fig. 2d. (MPG 7916 kb)

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Grieneisen, V., Xu, J., Marée, A. et al. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449, 1008–1013 (2007). https://doi.org/10.1038/nature06215

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