An auxin homeostat allows plant cells to establish and control defined transmembrane auxin gradients

Summary Extracellular auxin maxima and minima are important to control plant developmental programs. Auxin gradients are provided by the concerted action of proteins from the three major plasma membrane auxin transporter classes AUX1/LAX, PIN and ABCB transporters. But neither genetic nor biochemical nor modelling approaches have been able to reliably assign the individual roles and interplay of these transporter types. Based on the thermodynamic properties of the transporters, we show here by mathematical modeling and computational simulations that the concerted action of different auxin transporter types allow the adjustment of specific transmembrane auxin gradients. The dynamic flexibility of the “auxin homeostats” comes at the cost of an energy-consuming “auxin cycling” across the membrane. An unexpected finding was that functional ABCB-PIN coupling appears to allow an optimization of the trade-off between the speed of auxin gradient adjustment on the one hand and ATP consumption and disturbance of general anion homeostasis on the other. In conclusion, our analyses provide fundamental insights into the thermodynamic constraints and flexibility of transmembrane auxin transport in plants. Plain language summary The phytohormone auxin controls essentially plant development. Plant cells produce auxin and export it to establish patterns by local auxin minima and maxima. Although several transporter proteins are known to contribute to this process, the mechanism by which a defined auxin gradient can be produced is not clear. This study now uses mathematical modeling based on the thermodynamic features of the auxin transporters to illustrate in computational simulations the fundamental characteristics of an “auxin homeostat”. The concerted interplay of different auxin transporters allows plant cells to establish defined transmembrane auxin gradients that are the indispensable basis for polarized auxin maxima and minima and auxin fluxes within tissues.