Abstract

The intercellular transport of auxin is driven by PIN-formed (PIN) auxin efflux carriers. PINs are localized at the plasma membrane (PM) and on constitutively recycling endomembrane vesicles. Therefore, PINs can mediate auxin transport either by direct translocation across the PM or by pumping auxin into secretory vesicles (SVs), leading to its secretory release upon fusion with the PM. Which of these two mechanisms dominates is a matter of debate. Here, we addressed the issue with a mathematical modeling approach. We demonstrate that the efficiency of secretory transport depends on SV size, half-life of PINs on the PM, pH, exocytosis frequency and PIN density. 3D structured illumination microscopy (SIM) was used to determine PIN density on the PM. Combining this data with published values of the other parameters, we show that the transport activity of PINs in SVs would have to be at least 1000× greater than on the PM in order to produce a comparable macroscopic auxin transport. If both transport mechanisms operated simultaneously and PINs were equally active on SVs and PM, the contribution of secretion to the total auxin flux would be negligible. In conclusion, while secretory vesicle-mediated transport of auxin is an intriguing and theoretically possible model, it is unlikely to be a major mechanism of auxin transport in planta.

Highlights

  • The plant hormone auxin is subject to intercellular polar auxin transport (PAT) mediated by diffusion and the action of efflux and influx carriers

  • Three hypotheses have been suggested [7] to explain the requirement of PIN recycling: (1) recycling enables rapid relocation of PINs and thereby the rapid redirection of auxin transport; (2) PINs serve as IAA transceptors and their recycling is important for the process of signal transduction; and (3) the PIN-containing secretory vesicles (SVs) are filled with auxin, which is released into the apoplast upon fusion of the SV with the plasma membrane (PM)

  • PAT is characterized by the sustained velocity of auxin over long distances

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Summary

Introduction

The plant hormone auxin (indole-3-acetic acid; IAA) is subject to intercellular polar auxin transport (PAT) mediated by diffusion and the action of efflux and influx carriers. Three hypotheses have been suggested [7] to explain the requirement of PIN recycling: (1) recycling enables rapid relocation of PINs and thereby the rapid redirection of auxin transport; (2) PINs serve as IAA transceptors (transporters and receptors at the same time) and their recycling is important for the process of signal transduction; and (3) the PIN-containing secretory vesicles (SVs) are filled with auxin, which is released into the apoplast upon fusion of the SV with the PM. This process is analogous to neurotransmitter release in animals, and is important for the transport of auxin as suggested by previous reports [7,8] (Figure 1)

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