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Annual Report: CIRAD 2008

A unified auxin transport mechanism explains the formation of new plant organs

In plants, the formation of new organs in apical meristems is controlled by an auxin transport mechanism. Auxin is transported between cells by membrane proteins, which are located in a polar way within each cell, thus enabling the plant to accumulate auxin at specific sites. This accumulation process triggers organogenesis. However, what mechanism controls the polarization of these proteins? A research team used an integrated modelling strategy to demonstrate that a unified flux-enhancement-based mechanism could generate both vascularization and organ initiation patterns.

Auxin transport in a virtual meristem: comparison between simulations and experimental data Top: top view of the observed distribution of membrane transporters (PIN1 proteins) in Arabidopsis thaliana apical meristem cells. This image was obtained by immunolabelling PIN1 proteins and viewing them under a confocal microscope. Bottom left: digital version of the top image where the transporters (red) were manually positioned around each digitized cell wall. Bottom right: simulation of the distribution of transporters in cells based on the flux-enhanced polarization hypothesis. The two transporter motifs (real and simulated) are complex and, as can be noted, quantitatively very similar. The site of auxin accumulation (green) predicted by the model is located far from the previously formed organs (light blue dots).

Plants grow via their stem tips in small cellular areas called meristems. These areas contain undifferentiated cells that divide throughout the plant’s life and give rise to different organs, including leaves, sepals, petals, sexual organs, etc. In most plants, these organs show remarkable organization patterns, ie spirals or combinations of several spirals. Such arrangements, called phyllotaxis, have been studied by scientists for decades. These studies have shown that it is possible to explain most phyllotactic motifs by a simple geometric law. This is based on the hypothesis that recently formed organs hamper the formation of new organs in their immediate vicinity. It is as if these new organs emit an ”inhibitory field” around them to hinder the development of new organs in their immediate vicinity. The explanatory capacity of this model was successfully tested for many motifs, and the scientific community now considers it to be the ”standard model” of phyllotaxis. Scientists are now seeking to determine the physical or biochemical origin of these inhibitory fields. This research is focused on molecular and cellular biology and on microscopic imaging techniques. Over the last decade, several multidisciplinary teams of biologists and modelling specialists have been investigating the fundamental features of this mechanism.

Two hypotheses to explain polarization regulation

The findings of these studies revealed that the formation of new organs in apical meristem regions is regulated, on the cellular scale, by an auxin transport mechanism. Auxin is transported between cells by the coordinated action of membrane transporters of the PIN family located in the polar regions of each cell. These proteins create transport pathways that enable the plant to accumulate auxin around shoot tips. This accumulation triggers organogenesis.

Two main hypotheses have been put forward concerning the PIN protein polarization regulation mechanism. One, which is based on the notion of enhancing auxin fluxes, can explain the formation of a vascular network to transport nutrients to organs, like the formation of veins in leaves. The other is based on local increases in auxin concentrations, and can explain the positioning of organs on the meristem surface.

A mechanism that unifies auxin transport

A joint team of researchers from CIRAD, INRIA and INRA, in collaboration with the Ecole normale supérieure de Lyon, using a system biology approach integrating imaging, molecular biology and modelling, has just demonstrated that an approach based only on the flux enhancement hypothesis is actually enough to give estimates of both organ initiation and vascularization phenomena. The team has managed, for the first time, to accurately reproduce complex PIN protein motifs observed in the meristem.

These findings were based on a comparison of the distribution of membrane transporters in apical meristem cells of Arabidopsis thaliana, as detected by monitoring immunolabelled proteins under a confocal microscope and simulating the distribution with a model based on the flux-enhanced polarization hypothesis. The two real and simulated motifs are complex but quantitatively very similar.
This approach to assessing the unification of auxin transport in plant tissues will be the focus of experiments carried out to check the validity of these different hypotheses

Contact

Christophe Godin
INRIA-CIRAD-INRA joint project team, Plant Development and Genetic Improvement (UMR DAP)
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Partner

  • Ecole normale supérieure de Lyon (France)

For further information

  • Barbier de Reuille P., Bohn-Courseau I., Ljung K., Morin H., Carraro N., Godin C., Traas J., 2006. Computer simulations reveal novel properties of the cell-cell signaling network at the shoot apex in Arabidopsis. PNAS, 103 : 1627-1632.
  • Stoma S., Lucas M., Chopard J., Scheadel M., Traas J., Godin C., 2008. Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLoS Computational Biology, 4, doi : 10.1371/image. pcbi.v04.i10.