An Emerging Model of Auxin Transport Regulation

Abstract

The hormone auxin plays a critical role in the regulation of plant growth and development. Auxin is transported from cell to cell with strict directionality by uptake and efflux carrier proteins (reviewed by Muday and DeLong, 2001). The polarity of auxin transport is believed to be controlled by the localization of auxin transport proteins, with both putative efflux carriers and influx carriers having asymmetric distributions (Gälweiler et al., 1998; Muller et al., 1998; Swarup et al., 2001). This article highlights recent advances in identification of proteins that participate in auxin efflux and the mechanisms by which these proteins control the polar movement of auxin. Several proteins have been implicated in the control of auxin efflux from cells. The best characterized are the PIN proteins, which are encoded by a large gene family in Arabidopsis (reviewed by Palme and Gälweiler, 1999). Other proteins that bind indoleacetic acid (IAA) efflux inhibitors, including a multidrug resistance–like protein, also may function in auxin transport, as discussed below. Defects in the genes encoding PIN proteins were identified first in mutants with shoot (pin1) and root (agr1/eir1/pin2/wav6) phenotypes consistent with reduced IAA transport (Chen et al., 1998; Gälweiler et al., 1998; Luschnig et al., 1998; Muller et al., 1998; Utsuno et al., 1998). Functional assays in yeast expressing AGR1 or EIR1 suggest carrier activity (Chen et al., 1998; Luschnig et al., 1998), although the ability of PIN proteins to mediate IAA transport has not been demonstrated directly. The most exciting aspect of these proteins is that they show asymmetric cellular localization consistent with a role in controlling the polar efflux of IAA from cells (Gälweiler et al., 1998; Muller et al., 1998). A very recent report presents evidence that both asymmetric localization and dynamic redistribution of PIN3 protein are involved in the lateral redistribution of auxin in response to tropic stimuli (Friml et al., 2002). Model of Experiments That Have Examined the Mechanisms of the Control of PIN1 Protein Localization. (A) Vesicle-dependent transport of the PIN1 protein to the basal membrane appears to be along actin tracks. A high-affinity NPA binding protein has been found to interact with actin and may act as a bridge between these transport vesicles and the actin tracks and/or may serve to localize PIN1-containing IAA efflux complexes to the basal membrane. (B) Treatment with cytochalasin leads to a random PIN1 protein distribution and reduces polar auxin transport. (C) Treatment with BFA leads to a loss of PIN1 protein on the membrane and an accumulation of PIN1 protein at two undefined internal membrane structures. The effect is reversible upon removal of the BFA. (D) Treatment with either cytochalasin or the IAA efflux inhibitor TIBA during the removal of BFA prevents the restoration of asymmetric PIN1 distribution. Treatment with either cytochalasin or TIBA before BFA treatment prevents the BFA-induced PIN1 internalization, and treatment with TIBA alone has no effect on PIN1 localization (data not shown). (This figure was modified from Muday and DeLong [2001]). The localization of PIN1 also appears to depend on the actin cytoskeleton. Both PIN1 asymmetric localization and polar auxin transport are reduced in response to treatment with cytochalasin, a drug that fragments the actin cytoskeleton (Butler et al., 1998; Geldner et al., 2001). Cytochalasin treatment also prevents both the internalization of PIN1 in response to BFA treatment and the restoration of PIN1 localization upon the removal of BFA (Geldner et al., 2001). The role of the actin cytoskeleton in this process may be to provide tracks for vesicle movement and/or to fix the efflux carriers in an asymmetric distribution after delivery to the membrane surface (reviewed by Muday and DeLong, 2001). The involvement of the actin cytoskeleton in this process is consistent with results that indicate that a protein that binds auxin transport inhibitors, such as naphthylphthalamic acid (NPA), interacts with the actin cytoskeleton (Butler et al., 1998; Hu et al., 2000), and this NPA binding protein may provide a bridge between efflux carriers and the actin network used to transport and/or localize these complexes (Figures 1A and 1B). This rapid vesicle cycling of auxin efflux carriers may deliver these proteins to the appropriate membrane and could allow the redistribution of carriers to a new membrane when auxin transport polarity is changed by environmental stimuli such as light or gravity (reviewed by Muday, 2001; Friml et al., 2002). Two recent reports have suggested that high concentrations of artificial IAA efflux inhibitors may reduce transport by perturbing the movement of vesicles containing auxin efflux carriers to and from the membrane surface. Geldner et al. (2001)have shown that the IAA efflux inhibitor triiodobenzoic acid (TIBA) can prevent both the internalization of PIN1 in