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The phytohormone auxin is polarly transported in plants by PIN-FORMED (PIN) transporters and controls virtually all growth and developmental processes. Canonical PINs possess a long, largely disordered cytosolic loop. Auxin transport by canonical PINs is activated by loop phosphorylation by certain kinases. The structure of the PIN transmembrane domains was recently determined, their transport properties remained poorly characterized, and the role of the loop in the transport process was unclear. Here, we determined the quantitative kinetic parameters of auxin transport mediated by Arabidopsis PINs to mathematically model auxin distribution in roots and to test these predictions in vivo. Using chimeras between transmembrane and loop domains of different PINs, we demonstrate a strong correlation between transport parameters and physiological output, indicating that the loop domain is not only required to activate PIN-mediated auxin transport, but it has an additional role in the transport process by a currently unknown mechanism. [Display omitted] • PIN-FORMED auxin exporters have different transport properties • The intrinsically disordered loop contributes to the transport process • Properties of the loop domains are interchangeable between PINs • Slow auxin transport in the PIN2 domain is required for gravitropic root growth Polar auxin transport regulates plant growth responses, and Janacek et al. establish that PIN-FORMED auxin exporters have transport properties unique to every individual PIN. These properties depend on the interplay of transmembrane and loop domains to precisely fine-tune auxin flow to mediate growth responses. [ABSTRACT FROM AUTHOR]