No Time for Transcription-Rapid Auxin Responses in Plants

Abstract

Auxin regulates the transcription of auxin-responsive genes by the TIR1/AFBs-Aux/IAA-ARF signaling pathway, and in this way facilitates plant growth and development. However, rapid, nontranscriptional responses to auxin that cannot be explained by this pathway have been reported. In this review, we focus on several examples of rapid auxin responses: (1) the triggering of changes in plasma membrane potential in various plant species and tissues, (2) inhibition of root growth, which also correlates with membrane potential changes, cytosolic Ca²⁺ spikes, and a rise of apoplastic pH, (3) the influence on endomembrane trafficking of PIN proteins and other membrane cargoes, and (4) activation of ROPs (Rho of plants) and their downstream effectors such as the cytoskeleton or vesicle trafficking. In most cases, the signaling pathway triggering the response is poorly understood. A role for the TIR1/AFBs in rapid root growth regulation is emerging, as well as the involvement of transmembrane kinases (TMKs) in the activation of ROPs. We discuss similarities and differences among these rapid responses and focus on their physiological significance, which remains an enigma in most cases.

Figure 1.

Possible scenarios that could explain the underlying mechanisms of auxin-induced cell depolarization. (A) Proton influx driven by auxin/proton symport. Import of auxin into the cell participates in the accumulation of 2H⁺/1IAA^– by AUX1/LAX and/or 1H⁺ by diffusion (dissociation of IAAH at cytoplasmic pH 7). Such accumulation of cytoplasmic-positive charges could increase membrane potential. This could stimulate the proton pump activity, which in turn would fuel auxin import by AUX1/LAX. (B) Inhibition of the proton pump by an intracellular auxin receptor. Similar to A, auxin influx participates in the accumulation of protons in the cytoplasm. In this model, this process is enhanced by the inhibition of the proton pump by active signaling event(s) from auxin receptor(s). (C) Regulation of the activities of ion channels/carriers by intracellular auxin receptor(s). Inhibition of cations efflux or activation of influx and reciprocally for anions could influence membrane potential by accumulation of positive charges in the cytoplasm. The actual mechanism of depolarization is likely to be a combination of these scenarios.

Figure 2.

Schematic model of nontranscriptional auxin signaling at the cellular level. (A) Auxin entering the cell by influx or diffusion activates the TIR1/AFB receptors in the nucleus or possibly in the cytoplasm. Further, these receptors activate Ca²⁺ and H⁺ fluxes at the plasma membrane (PM) via an unknown signaling branch and lead to root growth inhibition. (B) Auxin activates ROPs (Rho of plants) by unknown mechanism(s), possibly via the TMK1 receptor. Lipid composition and organization of the membrane play a key role (magenta triangles). Activation by cytoplasmic auxin has not been excluded (C). Activated ROPs trigger downstream events including changes in PIN endomembrane trafficking, cytoskeletal reorganization, and activation of the TOR (target of rapamycin) pathway.