Flux-Based Transport Enhancement as a Plausible Unifying Mechanism for Auxin Transport in Meristem Development

Plants continuously generate new organs through the activity of populations of stem cells called meristems. The shoot apical meristem initiates leaves, flowers, and lateral meristems in highly ordered, spiralled, or whorled patterns via a process called phyllotaxis. It is commonly accepted that the active transport of the plant hormone auxin plays a major role in this process. Current hypotheses propose that cellular hormone transporters of the PIN family would create local auxin maxima at precise positions, which in turn would lead to organ initiation. To explain how auxin transporters could create hormone fluxes to distinct regions within the plant, different concepts have been proposed. A major hypothesis, canalization, proposes that the auxin transporters act by amplifying and stabilizing existing fluxes, which could be initiated, for example, by local diffusion. This convincingly explains the organised auxin fluxes during vein formation, but for the shoot apical meristem a second hypothesis was proposed, where the hormone would be systematically transported towards the areas with the highest concentrations. This implies the coexistence of two radically different mechanisms for PIN allocation in the membrane, one based on flux sensing and the other on local concentration sensing. Because these patterning processes require the interaction of hundreds of cells, it is impossible to estimate on a purely intuitive basis if a particular scenario is plausible or not. Therefore, computational modelling provides a powerful means to test this type of complex hypothesis. Here, using a dedicated computer simulation tool, we show that a flux-based polarization hypothesis is able to explain auxin transport at the shoot meristem as well, thus providing a unifying concept for the control of auxin distribution in the plant. Further experiments are now required to distinguish between flux-based polarization and other hypotheses.Author Summary: Plants continuously generate new organs through the activity of populations of stem cells called meristems. The shoot apical meristem (SAM) initiates leaves, flowers, and lateral organs in highly ordered, spiraled, or whorled arrangements via a process called phyllotaxis. Auxin, a plant hormone, plays an essential role in this process. It is actively transported from cell to cell by specific membrane-associated transporters. In the SAM, this coordinated transport creates organized auxin fluxes resulting in hormone accumulation at precise positions, where organ formation is triggered. One key question in this process is to understand how auxin transport is coordinated. To address this issue, we have investigated a specific hypothesis, the canalization hypothesis, whereby every cell senses and attempts to stabilize existing hormone fluxes. Because such a patterning process would require the interaction of hundreds of cells, it is impossible to estimate on a purely intuitive basis whether it would be able to generate the observed organ positions. We, therefore, developed a computational approach to test this hypothesis and showed that a flux-based mechanism is indeed able to generate phyllotactic patterns and is consistent with biological data describing meristem development.