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

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 (PM) auxin transporter classes AUX1/LAX, PIN and ATP-BINDING CASSETTE subfamily B (ABCB) transporters. But neither genetic nor biochemical nor modeling 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 allows the adjustment of specific transmembrane auxin gradients. The dynamic flexibility of the 'auxin homeostat' comes at the cost of an energy-consuming 'auxin cycling' across the membrane. An unexpected finding was that potential functional ABCB-PIN synchronization appears to allow an optimization of the trade-off between the speed of PM 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.