JXB Advance Access published online on September 29, 2008
Journal of Experimental Botany, doi:10.1093/jxb/ern240
REVIEW ARTICLE |
Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition
Department of Horticulture, Purdue University, West Lafayette, Indiana 47907-2010, USA
* To whom correspondence should be addressed: E-mail: murphy{at}purdue.edu
Received 2 July 2008; Revised 28 August 2008 Accepted 1 September 2008
 |
Abstract |
|---|
 Top Abstract IntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Auxin concentration gradients, established by polar transport of auxin, are essential for the establishment and maintenance of polar growth and morphological patterning. Three families of cellular transport proteins, PIN-formed (PIN), P-glycoprotein (ABCB/PGP), and AUXIN RESISTANT 1/LIKE AUX1 (AUX1/LAX), can independently and co-ordinately transport auxin in plants. Regulation of these proteins involves intricate and co-ordinated cellular processes, including protein–protein interactions, vesicular trafficking, protein phosphorylation, ubiquitination, and stabilization of the transporter complexes on the plasma membrane.
Key words: AUX/LAX, cellular trafficking, membrane composition, P-glycoprotein, phosphorylation, pin-formed, protein maturation, ubiquitination
|
Introduction |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
The phytohormone indole-3-acetic acid (IAA), or auxin, plays an essential role in embryogenesis (Friml et al., 2003), cell division and elongation (Campanoni and Nick, 2005), vascular tissue differentiation (Mattsson et al., 2003), phyllotactic patterning (Bainbridge et al., 2008), lateral root formation (Dubrovsky et al., 2008), phototropism (Kimura and Kagawa, 2006), gravitropism (Palme et al., 2006), and other physiological processes. Although auxin was the first phytohormone to be discovered (Went, 1927), the molecular mechanisms underlying its transport and perception have only been elucidated in the past decade (Kepinski, 2007; Delker et al., 2008).
IAA is synthesized in the shoot, particularly by leaf primordia and young leaves, and transported to the root through vascular and bundle sheath tissues (Ljung et al., 2005; Bandyopadhyay et al., 2007). The synthesis, transport, and catabolism of IAA is tightly regulated by both transcriptional and post-transcriptional processes that are co-ordinately regulated via the ubiquitination of AUX/IAA repressor proteins by the SCFTIR1/AFB mechanism followed by proteolytic degradation (Quint and Gray, 2006). Additional post-transcriptional mechanisms further regulate auxin transport. This review focuses on the role of post-translational mechanisms that regulate auxin transport processes by modifying, activating, redistributing, or degrading auxin transport proteins or protein complexes.
|
Polar auxin transport |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Auxin is polarly transported from cell to cell in a process that involves chemiosmotically-driven export to and uptake from the apoplast. As IAA is a weak organic acid (pKa=4.75), it exhibits a
5:1 distribution of anionic (IAA–): protonated (IAAH) speciation in the acidic (pH 5.5) apoplast. IAA can thus enter the cell by either lipophilic diffusion of IAAH or by anionic uptake via H+-IAA– symporters. The latter process is required as the diffusive flux of IAAH across the plasma membrane is thought to be an order of magnitude slower than that of carrier-mediated IAA– translocation, and diffusion alone cannot account for auxin fluxes that naturally occur in plants (Kramer and Bennett, 2006). In contrast, the cellular efflux of IAA requires protein mediation, as IAA is almost exclusively anionic in the cytoplasm (pH 7.0) and cannot diffuse across the membrane on its own. The localization and activity of auxin transport complexes are thus crucial in establishing the polarity of auxin transport. The concentration gradient created by directional movement of auxin is fundamental to the establishment of plant axial polarity, organ patterning, and morphological adaptation to the environment (De Smet and Jurgens, 2007). From the first cell division in plant embryogenesis, auxin is preferentially accumulated in the zygotic apical cell where it functions as an important determinant of that cell's proembryonic fate (Friml et al., 2003). Vascular differentiation also coincides with auxin accumulation in preprocambial cells (Mattsson et al., 2003). In the root, acropetal transport (base to apex) of auxin (Blakeslee et al., 2005a) within the stele is responsible for the initiation of lateral root primordia from pericycle cells that can respond to auxin activation (Casimiro et al., 2001; Bhalerao et al., 2002; Wu et al., 2007). In Arabidopsis, the priming of pericycle cells for auxin responsiveness occurs in the basal region of the root meristem and is controlled by a periodic shift in the basipetal (apex to base) redistribution of auxin through the lateral root cap and epidermal cell files, resulting in an alternating pattern of regularly spaced lateral roots (De Smet et al., 2007). In gravitropic root bending, asymmetric changes in the basipetal (root apex to base) transport stream caused by alteration in the gravitational vector leads to differential root elongation and bending in the direction of the gravitational vector (Palme et al., 2006). Similarly, phototropic bending in hypocotyls is thought to result from asymmetric accumulation of auxin in cells distal to the site of illumination resulting in asymmetric growth and bending of the hypocotyl toward light (Kimura and Kagawa, 2006).
|
Classes of auxin transport proteins |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Auxin transport proteins have been identified and, to date, have been grouped in three families: AUXIN RESISTANT 1/LIKE AUX1 (AUX1/LAX) uptake symporters, PIN-FORMED (PIN) efflux carriers, and P-GLYCOPROTEIN (MDR/PGP/ABCB) efflux/conditional transporters.
AUX1/LAX uptake symporters
AUX1 was originally identified in a genetic screen for Arabidopsis mutants that exhibited auxin-resistant root growth (Bennett et al., 1996). The AUX1 gene encodes a transmembrane protein similar to amino acid permeases. AUX1 participates in loading of shoot auxin into the phloem for long-distance transport toward the root tip and in the basipetal transport of auxin out of the lateral root cap at the root apex (Swarup et al., 2002, 2004). The ability of AUX1 to mediate auxin influx has been demonstrated in planta and by expression in heterologous systems. Treatment with the membrane-permeable artificial auxin 1-naphthaleneacetic acid (1-NAA) was shown to rescue the agravitropic phenotype of the aux1 mutant, which is also resistant to the weakly permeate and poorly transported auxin herbicide 2,4-dichlorophenoxyacetic acid (2,4-D) (Marchant et al., 1999). When expressed in Xenopus oocytes, AUX1 was shown to function as a high-affinity auxin uptake carrier protein (Yang et al., 2006; Kerr and Bennett, 2007).
AUX1 is localized to the lower end of the cells in the lateral root cap, epidermal cells below the elongation zone, columella, and protophloem (Kleine-Vehn et al., 2006). The three members of the Like-AUX1 (LAX) family are functional analogues of AUX1, and appear to function in tissue-specific auxin uptake (Swarup et al., 2004). Quadruple aux/lax mutants exhibit aberrant formation of leaf primordia and reduced polar PIN localization consistent with altered auxin flux (Bainbridge et al., 2008). LAX3 functions in the early stages of lateral root formation (de Billy et al., 2001; Swarup et al., 2008).
PIN efflux carriers
The Arabidopsis pin-formed1 (pin1) mutant exhibits defects in vascular patterning, organogenesis, and phyllotaxis (Galweiler et al., 1998; Reinhardt, 2005). PIN proteins belong to the unique auxin efflux facilitator family found in plants and some fungi and are predicted to have 10–12 transmembrane domains (Galweiler et al., 1998; Blakeslee et al., 2007). Among the eight members of the PIN family in Arabidopsis, five have been experimentally shown to function as auxin efflux carrier proteins when expressed in Arabidopsis, tobacco BY-2, human HeLa, and/or yeast cell cultures (Petrasek et al., 2006; Blakeslee et al., 2007). PIN-mediated efflux in these heterologous systems was partially inhibited by the auxin efflux inhibitor 1-naphthylphthalamic acid (NPA), although, in all cases when it was used, NPA strongly inhibited background auxin efflux in cells not expressing recombinant PIN proteins, especially in plant cell systems (Petrasek et al., 2006).
Subcellular localization of PIN proteins maps with the directionality of auxin transport vectors, especially in embryonic development and organogenesis (Benkova et al., 2003; Blilou et al., 2005). In the central vascular cylinder, PIN1 is basally localized in the xylem parenchyma and participates in the transport of auxin along the embryonic axis from the shoot to the root tip. PIN2 exhibits a basal (bottom) and lateral localization in root cortical cells and apical (top) localization in root epidermal cells consistent with its apparent role in redirection and reflux of auxin at the root tip (Chen et al., 1998; Luschnig et al., 1998; Muller et al., 1998). PIN3 exhibits an apolar orientation in root columella cells, but relocalizes in the direction of auxin movement upon gravistimulation (Friml et al., 2002b). PIN3 is also localized to the inner surface of hypocotyl bundle sheath cells where it appears to function in the redirection of auxin back into the vascular cylinder. PIN3 is also found in epidermal cells, and the pin3 mutant shows shorter epidermal cells in light-grown hypocotyls, thought to be caused by a defect in cell elongation (Friml et al., 2002b). As mutational analysis indicates that PIN3 functions in tropic responses, activation of its transport activity near sites of illumination could be expected to accelerate auxin movement out of tissues on the illuminated (non-bending side) of the hypocotyl.
Other PIN proteins exhibit primarily apolar subcellular localizations but still contribute to directional auxin movement. PIN4 exhibits mixed polar and apolar localizations in the provascular quiescent centre and daughter cells and functions in root meristem patterning (Friml et al., 2002a). PIN7 is abundant in epidermal tissues where it exhibits a non-polar localization (Blakeslee et al., 2007), and is also involved in the establishment of the apical–basal axis, particularly in the hypophysis (Friml et al., 2003). Despite their seemingly discrete expression patterns and functions, some redundancy is found among PIN family members as compensatory expression of some PIN genes was observed in pin1 and pin2 mutants, and ectopic expression of these PIN homologues was sufficient to rescue the auxin transport phenotype of the mutants (Vieten et al., 2005). One member of the PIN family, PIN5, is particularly intriguing, as it lacks a variable central domain common to other characterized PIN proteins that, in the case of PIN1 has been shown to mediate protein–protein interactions (Blakeslee et al., 2007). Analysis of PIN5 auxin transport activity (if any) will help determine whether the central variable domain of the PIN proteins plays a functional role in transport or has a primarily regulatory function as has been proposed.
Some evidence suggests that auxin efflux proteins also mediate intercellular auxin movement from mildly alkaline organelles to the neutral cytosol. Anionic auxin accumulation within compartments with a pH >7.0 is predicted by chemiosmotic models, and the essential auxin binding protein ABP1 is relatively abundant in the mildly alkaline endoplasmic reticulum (Timpte, 2001). Further, the toxic effects of the artificial auxin 2,4-dichlorophenoxyacetic acid (2,4-D) are associated with its accumulation in the endoplasmic reticulum (Dharmasiri et al., 2006). As compared to IAA, 2,4-D is poorly transported by efflux carrier proteins, one of the uncharacterized PIN transporters, such as PIN5 or PIN8, and/or one or more uncharacterized ABCB transporter may mediate auxin efflux from the ER.
ABCB efflux transporters
A third class of auxin transporters are phospho-glycoproteins (PGPs) that belong to the ABCB subgroup of the ATP-Binding-Cassette (ABC) transporter superfamily. The best known member of the ABCB subgroup is the human ABCB1 protein which has been extensively studied for its role in increased resistance to chemotherapeutic agents resulting from its overexpression in cancer cells (Luckie et al., 2003). However, the use of the multidrug resistance (MDR) nomenclature for this subgroup of proteins has been discontinued as the majority of family members appear to exhibit a higher degree of transport substrate specificity than mammalian ABCB1 (Verrier et al., 2008). In Arabidopsis thaliana, the 21 members of ABCB subgroup exhibit both distinct and overlapping expression patterns throughout all stages of plant growth and development (Blakeslee et al., 2005b). The best characterized members of Arabidopsis ABCB proteins are the auxin transporters ABCB1, ABCB4, and ABCB19. Multiple reports have catalogued PIN and AUX/LAX gene expression and protein localization (Blakeslee et al., 2005a, b; Tanaka et al., 2006; Zazimalova et al., 2007). By contrast, a current summary of ABCB auxin transporter gene expression and ABCB protein distribution is lacking in the literature. A brief summary of the expression patterns of ABCB auxin transporter genes is provided in Table 1 and a summary of protein localization is shown in Fig. 1.
|
|
The involvement of ABCB proteins in auxin transport was first suggested by Sidler et al., (1998) when expression levels of PGP1/ABCB1 in Arabidopsis were found to regulate hypocotyl elongation in a light-dependent manner (Sidler et al., 1998). ABCB1 was subsequently shown to function co-ordinately with PGP19/MDR1/ABCB19 in mediating polar auxin transport in Arabidopsis (Noh et al., 2001). The sequence of ABCB19 is highly similar to that of ABCB1 (Verrier et al., 2008). Arabidopsis abcb1 and abcb19 mutants exhibit reductions in both growth and root basipetal auxin transport with the most pronounced reductions seen in the double abcb1 abcb19 mutant. Polar auxin transport is reduced
70% in abcb1 abcb19, while pin1 exhibits a 30% reduction (Blakeslee et al., 2007), but abcb mutants show none of the defects in organogenesis that are seen in pin1 (Noh et al., 2001). This suggests that ABCBs primarily regulate long-distance auxin transport and localized loading of auxin into the transport system and do not function in establishing the basal vectorial auxin flows that function in organogenesis (Bandyopadhyay et al., 2007; Blakeslee et al., 2007; Bailly et al., 2008). This interpretation of ABCB auxin transport function was confirmed when loss of function of ABCB1 orthologues were found to underlie the dwarf phenotypes of the agriculturally-important brachytic2/zmabcb1 maize and dwarf3/sbabcb1 sorghum mutants (Multani et al., 2003). Arabidopsis abcb19 also exhibits exaggerated phototropic and gravitropic responses (Noh et al., 2001, 2003; Lin and Wang, 2005; Lewis et al., 2007; Wu et al., 2007). In addition, it has recently been shown that the expression level of ABCB19 is suppressed upon activation of the phytochrome and cryptochrome photoreceptors in response to the red and blue light, respectively (Nagashima et al., 2008). These results point to an ABCB19 function in the repression of the differential growth of the light- and gravity-stimulated hypocotyl (Noh et al., 2003; Nagashima et al., 2008).
A direct role for ABCB1 and ABCB19 in cellular efflux was demonstrated when increased auxin retention was observed in mesophyll protoplasts from Arabidopsis abcb1 and abcb19 mutants (Geisler et al., 2005). Further, as was seen with PIN proteins, heterologous expression of ABCB1 and ABCB19 in HeLa and/or yeast cells resulted in enhanced auxin efflux that was inhibited by NPA (Geisler et al., 2005; Bouchard et al., 2006). However, unlike what was seen with PIN expression, the efflux mediated by the ABCBs in mammalian cells was insensitive to inhibitors of mammalian organic anion transporters, suggesting that ABCB-mediated auxin export did not involve activation of an endogenous transport activity (Geisler et al., 2005; Petrasek et al., 2006).
ABCB4 functions in the movement of auxin away from the root tip and appears to function primarily in the regulated export of auxin out of the elongation zone (Santelia et al., 2005; Terasaka et al., 2005; Cho et al., 2007; Lewis et al., 2007). ABCB4 exhibits structural similarity to the berberine uptake transporter CjMDR1/CjABCB1 from the medicinal plant Coptis japonica (Shitan et al., 2003) and, to a lesser extent, the ABCB14 malate uptake transporter from Arabidopsis guard cells (Lee et al., 2008), but exhibits dissimilarity in putative substrate binding sites (H Yang and A Murphy, unpublished data). Some experimental evidence indicates that ABCB4 functions in auxin uptake. When expressed in mammalian cells, ABCB4 activates a net increase in auxin retention (Terasaka et al., 2005), and heterologous expression of ABCB4 in the yeast IAA-sensitive yap1 mutant led to enhanced growth sensitivity to IAA (Santelia et al., 2005). However, NPA treatment of mammalian cells expressing ABCB4 activated efflux to levels equivalent to that seen in NPA-treated cells expressing Arabidopsis ABCB1 or ABCB19 (Terasaka et al., 2005). Recently, ABCB4 expression has been found to confer auxin efflux activity in root hairs and tobacco suspension cells (Cho et al., 2007). These results suggest that the directionality of ABCB4-mediated transport is regulated by plant-specific modulators (Cho et al., 2007). However, it is also possible that ABCB4 export is directly activated by threshold levels of transport substrates as is the case with human ABCB1 (Kimura et al., 2007). An examination of published results suggests that auxin efflux activated by ABCB4 is more evident in experiments utilizing longer time periods for assays, while activation of uptake is seen with lower concentrations in shorter time periods. As such, ABCB4 might best be referred to as a conditional auxin efflux/uptake transporter. Structural modelling comparisons of ABCB4 with ABCB1, ABCB19, and the ABCB14 malate uptake transporter (H Yang and A Murphy, unpublished results) suggest that unique structure/sequence variations in ABCB4 underlie its conditional activity.
ABCB4 appears to function primarily in the accumulation of auxin in the elongation zone as well as efflux from root trichoblast cells. Mutations in ABCB4 exhibit decreased linear growth (Terasaka et al., 2005), increased initial rates of root bending (Lewis et al., 2007), and altered root hair formation (Santelia et al., 2005; Cho et al., 2007) that are dependent on growth conditions. All of these functions are consistent with ABCB4 expression patterns, ABCB4 protein distribution and subcellular localization, and auxin transport profiles of abcb4 mutants.
|
Regulation of auxin transport proteins by protein–protein interactions |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Activation of ABCB proteins by TWD1/FKBP42
Multiple lines of evidence suggest that there are at least two distinct NPA-binding sites in Arabidopsis membranes. A high affinity site associated with the inhibition of auxin transport at the plasma membrane is associated with an integral membrane protein, and possibly, an associated peripheral protein (Murphy et al., 2002). A second, low affinity NPA binding site is thought to be a membrane anchored or peripheral amidase (Murphy et al., 2002). Other sites of NPA action have been associated with membrane trafficking events, but require such high concentrations of NPA to be visualized that they can be regarded as non-specific (Geldner et al., 2001). NPA affinity chromatography was initially used to isolate the ABCB1, 4, and 19 proteins (Murphy et al., 2002; Geisler et al., 2003; Terasaka et al., 2005). An FKBP immunophilin-like protein, TWD1/FKBP42 was copurified with the ABCBs (Murphy et al., 2002).
Subsequent studies have established that the C-terminal domains of ABCB1 and ABCB19 interact with FKBP42 and that the phenotypes of abcb1 abcb19 resemble those of the twd1 mutant (Geisler et al., 2003). Based on sequence prediction, FKBP42 was proposed to be a glycophosphatidyl inositol (GPI)-anchored protein (Geisler et al., 2003). However, no GPI moiety was detected when TWD1 was biochemically analysed (Murphy et al., 2002; Granzin et al., 2006), and subsequent structural characterizations are inconsistent with the presence of a GPI anchor (Eckhoff et al., 2005). Further, the abundance of FKBP42 is very low compared to ABCB1 and ABCB19 (Bailly et al., 2008), suggesting that FKBP42 functions in activating ABCB membrane complexes, rather than anchoring complex formation. FKBP42 has been proposed to induce conformational changes in ABCB1 and ABCB19 (Geisler et al., 2003; Bouchard et al., 2006; Bailly et al., 2008). ABCB1–FKBP42 interactions have been shown to be sensitive to both NPA and flavonoid inhibitors of auxin transport, which appear to interact with multiple sites of action in the respective proteins (Bailly et al., 2008). Conformational changes are involved in the regulation of mammalian ABCB (Ambudkar et al., 2006), although little is known about the protein interactions that initiate these changes.
Consistent with this proposed function, loss of FKBP42 conferred resistance to the pharmacological agent gravacin, which is an inhibitor of ABCB19 activity (Rojas-Pierce et al., 2007). Gravacin was originally identified as an inhibitor of gravitropic bending in hypocotyls and was subsequently found to interfere with subcellular targeting of vacuolar marker proteins (Surpin et al., 2005). Wild-type Arabidopsis seedlings treated with gravacin resulted in reductions of auxin transport that were similar to those seen in abcb19, while gravacin treatment of abcb19 mutants resulted in nominal further reductions in auxin transport (Rojas-Pierce et al., 2007). A screen for mutants that are resistant to gravacin resulted in the identification of abcb/pgp19-4 which harbours a point mutation in the C-terminal domain of ABCB19 (E1174K) (Rojas-Pierce et al., 2007).
Treatment with gravacin did not alter the gravitropic response of twd1, and microsomes derived from twd1 showed reduced binding to gravacin (Rojas-Pierce et al., 2007; Bailly et al., 2008). However, the immunolocalization of ABCB19 was unchanged in twd1 mutants compared to wild type (Titapiwatanakun et al., 2008), suggesting that FKBP42 is more likely to function in activation, rather than localization of ABCB1/19 to the plasma membrane.
PIN-ABCB interactions
Although both ABCB19 and PIN1 can function as independent auxin efflux transporters, these proteins can interact and co-ordinately transport auxin (Bandyopadhyay et al., 2007; Blakeslee et al., 2007). Co-ordinated, but independent functions for PINs and ABCB1/19 are particularly evident in embryonic development and lateral root formation. However, physical interaction between ABCB19 and PIN1 in post-embryonic growth is suggested by positive results in subcellular colocalization, coimmunoprecipitation, and yeast two-hybrid interaction analyses (Blakeslee et al., 2007). Moreover, functional interactions between ABCB19 and PIN1 are supported by apparently synergistic phenotypes of pin1 abcb19 mutants and enhanced auxin efflux activity, inhibitor sensitivity, and substrate specificity of HeLa cells co-expressing ABCB19 and PIN1. As was the case with FKBP42/TWD1, interactions of ABCB19 with PIN1 are mediated by the C-terminal domain of the protein, and gravacin effectively interferes with the enhanced auxin transport mediated by ABCB19 and PIN1 coexpression (Rojas-Pierce et al., 2007).
Some evidence of interactions between PIN1 and ABCB1 are suggested by co-immunoprecipitation studies and by increases in auxin efflux when the two proteins are co-expressed in heterologous systems (Blakeslee et al., 2007). However, PIN1–ABCB1 interactions appear to be indirect, as no evidence of protein interactions are seen in yeast two-hybrid assays (Blakeslee et al., 2007). By contrast, interactions of PIN2 with ABCB1 may be more robust, as coexpression of PIN2 and ABCB1 in yeast has synergistic effects on auxin transport and pin2 pgp1 pgp19 mutants exhibit severely agravitropic growth phenotypes (Blakeslee et al., 2007).
|
Regulation of auxin transporters by auxin levels and fluxes |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Auxin has been proposed to ‘canalize’ it own transport by reorienting transport components (Sachs, 1981), presumably by altering the subcellular localization of auxin transport proteins or by regulating their transport activity. The direction of auxin flow has been shown to influence polar PIN localization in a cell type-specific manner (Sauer et al., 2006). For instance, in graviresponding root columella cells, PIN3 is disproportionately oriented on the lower side of cells in the path of auxin destined to accumulate in the epidermal cells of the distal elongation zone (Friml et al., 2002b). Similarly, expression of an apically-localized chimeric PIN1 protein under the control of the PIN2 promoter was able to suppress the root agravitropic phenotype of the pin2 mutant, while comparable localization of basally-localized PIN1 protein failed to produce the same result (Wisniewska et al., 2006). To date, most studies have focused on easily visualized changes in PIN protein localization in response to altered auxin fluxes. However, it is unlikely that PIN proteins are only regulated by localized auxin accumulations. Numerous studies have shown that PIN expression and PIN protein abundance are altered by changes in auxin levels or transport (Peer et al., 2004; Vieten et al., 2005). It is likely that protein phosphorylation and turnover of PINs play an important role in auxin-dependent regulation of PIN function as well.
Expression of ABCB1, ABCB4, and ABCB19 is up-regulated by auxin application (Noh et al., 2001; Geisler et al., 2005; Terasaka et al., 2005). The promoter sequence of ABCB1 includes auxin responsive motifs and the time-course of β-glucuronidase (GUS) expression directed by ABCB1 promoter (ABCB1pro:GUS) at the shoot and root apices in response to auxin treatment indicate that ABCB1 expression responds rapidly to auxin treatment (Geisler et al., 2005). By contrast, ABCB4 appears to be a ‘late’ auxin response gene (Terasaka et al., 2005). In general, protein abundances of ABCB1, 4, and 19 appear to reflect gene expression levels (Geisler et al., 2005; Terasaka et al., 2005; Blakeslee et al., 2007; Wu et al., 2007). Overexpression of ABCB4 does not result in the presence of ectopic ABCB4 protein in the shoot (Terasaka et al., 2005). This appears to be a result of regulation of gene expression or RNA stability, as steady-state ABCB4 RNA levels in the shoot were found to be very low in overexpressing lines (Terasaka et al., 2005). A similar disparity is found with expression of ABCB19, as visualized with a MDR1pro:GFP-MDR1 fusion. No signal is seen in root and anther filament epidermal cells where transcriptional reporters, RT-PCR, and microarray expression reports indicate gene expression (Blakeslee et al., 2007; Wu et al., 2007). However, immunolocalizations, epitope-tags, and other protein–reporter fusions indicate that the protein is present in these cells (Blakeslee et al., 2007). Further, ABCB19 appears to be highly stable and protein abundance responds slowly to decreases in gene expression (Titapiwatanakun et al., 2008).
|
Regulation of auxin transporters by cellular trafficking mechanisms |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
The trafficking pathways of the PIN and AUX1 auxin transport proteins have been extensively investigated. Less is known about the trafficking of the ABCBs, primarily due to a strong community bias against the acceptance of these proteins as auxin transporters until recently. In Fig. 2, a summary of the known subcellular trafficking pathways that mediate PIN1, PIN2, AUX1, ABCB1, and ABCB19 to and from the plasma membrane is presented.
|
Trafficking mechanism of PINs
The dynamic trafficking of PIN1 is the one of the best studied trafficking mechanisms in plants. PIN1 trafficking is mediated by ADP-ribosylation factors (ARFs), the GNOM ARF guanine nucleotide exchange factor (ARF-GEF) (Steinmann et al., 1999), and the ARF GTPase activating protein (ARF-GAP) SCARFACE (SFC) (Sieburth et al., 2006). Embryos of gnom mutants exhibit severe polarity defects and altered polar localizations of PIN1 (Steinmann et al., 1999). The Sec7 domain of GNOM has been shown to be a target of the fungal toxin brefeldin A (Geldner et al., 2003), and short-term treatments of brefeldin A (BFA) have been shown to reversibly cause intracellular aggregations of PIN1 in cells at the root apex (Geldner et al., 2001). Mutation of the Sec7 domain of GNOM to a BFA-insensitive form (GNOMM696L) prevents the formation of PIN1 aggregations after BFA treatment (Geldner et al., 2003), indicating that PIN1 trafficking is mediated by GNOM. PIN3 has also been shown to associate with the BFA compartment following BFA treatment (Friml et al., 2002b). PIN1 accumulation after BFA treatment in the sfc mutant resulted in multiple smaller organelles, and implicated a role of the SCARFACE ARF-GAP protein in PIN1 cycling as well (Sieburth et al., 2006). In addition, trafficking of PIN1 also requires an intact actin network, but appears not to require microtubules (Geldner et al., 2001).
The time- and dosage-dependent effects of BFA on PIN trafficking have recently been examined (Kleine-Vehn et al., 2008). Long-term incubation with BFA has been shown to promote transcytosis of PIN1 and PIN2, in which the ARF-GEF-mediated endocytotic vesicles was found to be translocated from one side of the cell to the other.
The subcellular trafficking of PIN2 appears to be regulated by different mechanisms than those mobilizing PIN1. Trafficking of PIN2 is mediated by endosomes containing SORTING NEXIN1 (SNX1), which are distinct from GNOM-mediated endosomes and are sensitive to the phosphatidylinositol-3-OH kinase (PI-3K) inhibitor wortmannin (Jaillais et al., 2006). SNX1 is a subunit of the retromer complex, which functions in recycling transmembrane proteins from endosomal multivesicular bodies (MVBs) to the trans-Golgi network in yeast and mammals (Bonifacino and Rojas, 2006). Another important subunit of the retromer complex is the Vacuolar Protein Sorting 29 (VPS29), which is also localized to MVBs. Arabidopsis mutants lacking VPS29 showed the alterations in the morphology of SNX1-containing endosomes and also altered PIN1 localization (Jaillais et al., 2007), suggesting that the retromer complex functions in the endosomal recycling of PIN1 as well.
The endocytosis of PIN proteins has been shown to be inhibited by auxin itself (Paciorek et al., 2005; Zazimalova et al., 2007). Treatment with high auxin concentrations stabilized PIN proteins (PIN1, 2, 3, and 4) on the plasma membrane. This phenomenon may reflect a need for increased PIN-mediated auxin efflux transport activity in order to prevent accumulation of auxin in the cytoplasm. However, there appears to be a difference between treatment with high concentrations of exogenous auxin and manipulation of auxin transport itself. The application of picomole amounts of auxin at the shoot apex to enhance auxin flux artificially altered the expression of PIN genes, and particularly increased PIN2 expression in the root (Peer et al., 2004). Consistent with this, elevated auxin transport in mutants lacking flavonoids, endogenous auxin transport inhibitors, resulted in increased IAA levels in the root which, in turn, enhanced PIN expression and altered PIN protein localization (Peer et al., 2004).
A number of auxin transport inhibitors have been used as pharmacological agents to probe the subcellular trafficking of PIN proteins. The competitive inhibitor triiodobenzoic acid (TIBA) and the non-competitive inhibitor pyrenoyl benzoic acid (PBA) both disrupt PIN vesicle trafficking processes by interfering with actin stability (Dhonukshe et al., 2008), and TIBA can inhibit restoration of PIN1 to the plasma membrane when included in washout solutions following BFA treatment (Geldner et al., 2001). NPA can function in a similar fashion if used in even higher concentrations (Geldner et al., 2001; Petrasek et al., 2003). However, in all cases, the concentrations of auxin transport inhibitors required for inhibition of cellular trafficking mechanisms are 10–100 times higher than those required to inhibit auxin transport (Petrasek et al., 2003).
Subcellular trafficking of AUX1
The trafficking of AUX1 exhibits both differences and similarities when compared to that of PIN proteins. Although AUX1 exhibits polar localization on the apical plasma membrane in some cells, in others, AUX1 exhibits a non-polar membrane distribution and is also accumulated at the Golgi apparatus and endosomal compartments (Kleine-Vehn et al., 2006). The connections between these plasma membrane and intercellular localizations have been shown to be dependent on actin filaments and the membrane sterols (Kleine-Vehn et al., 2006). Moreover, the apical localization of AUX1 on the plasma membrane of protophloem and epidermal cells requires the presence of AUXIN RESISTANT4 (AXR4), which is found in the endoplasmic reticulum (ER) (Dharmasiri et al., 2006). In contrast to AUX1, the localizations of PIN1 and PIN2 did not appear to be affected by AXR4, thus indicating that the root agravitropic phenotype observed in the axr4 mutant is probably caused by an alteration in the AUX1 function. Although AUX1 trafficking is also BFA-sensitive, it utilizes a GNOM-independent mechanism (Kleine-Vehn et al., 2006; Boutte et al., 2007). However, this is not surprising considering the likelihood of BFA interaction with Sec7-like motifs in multiple proteins.
Subcellular trafficking of ABCBs
ABCB19 is localized on the plasma membrane where it partially overlaps with PIN1 (Blakeslee et al., 2007). However, the trafficking of ABCB19 does not coincide with that of PIN1, PIN2, and AUX1. Compared with the more dynamic processes regulating membrane localization of the AUX1 and PIN-family proteins, ABCB19 is more stably situated on the plasma membrane (Titapiwatanakun et al., 2008). Whereas the dynamic cycling of PIN1 is disrupted by short-term treatments with actin depolymerising agents like latrunculin B (Geldner et al., 2001), the localization of ABCB19 is unaffected by a short-term treatment with latrunculin B. ABCB19 is not recycled by microtubule- or SNX1-dependent processes, as ABCB19 subcellular localization is insensitive to short-term treatments with the microtubule depolymerizing compound oryzalin and is also insensitive to wortmannin (Titapiwatanakun et al., 2008). However, treatment with gravacin does interfere with the trafficking of ABCB19 to the plasma membrane, resulting in aggregation of some ABCB19 protein in an unidentified compartment that does not coincide with the endocytic marker FM4-64 (Rojas-Pierce et al., 2007). Identification of this compartment should help the elucidation of the ABCB19 trafficking pathway.
As the trafficking of ABCB19 to the plasma membrane is not BFA-sensitive, it is not mediated by GNOM-dependent mechanisms (Titapiwatanakun et al., 2008). However, not surpisingly for a P-glycoprotein, ABCB19 appears to be trafficked by GNOM-LIKE1 (GNL1), a BFA-insensitive ARF-GEF in the GNOM family that mediates vesicular ER-Golgi trafficking (Richter et al., 2007; Teh and Moore, 2007). In Arabidopsis, mutations in GNL1 exhibit a reduction in the abundance and plasma membrane localization of ABCB19, but not of PIN1 and PIN2. The gnl1 mutants also exhibited a decrease in NPA-sensitive auxin transport.
On the other hand, ABCB1 does aggregate in intracellular bodies with PIN2 after BFA treatment, suggesting that it is less stable and more readily endocytosed than ABCB19 (Blakeslee et al., 2007; Titapiwatanakun et al., 2008). This is consistent with the synergistic phenotypic effects seen with loss of ABCB1 function in abcb19 mutants and suggests that ABCB1 may be a more dynamic regulator of ABCB19 function. This is even more likely, as ABCB1 exhibits stronger interactions with both FKBP42/TWD1 and the auxin transport inhibitor NPA (Murphy et al., 2002; Geisler et al., 2003; Bouchard et al., 2006; Bailly et al., 2008).
Recently, the involvement of small GTPases, such as the Rab proteins, in the trafficking of human ABCBs has been reported in a HeLa cells study (Fu et al., 2007). The intracellular localization of human ABCB1 became conspicuous when a dominant negative form of Rab5 and GFP-tagged HsABCB1 were co-expressed in HeLa cells (Fu et al., 2007). It will be interesting to investigate further whether the small GTPase family of proteins plays a role in regulating the vesicular trafficking of the ABCBs in plants.
|
Regulation of auxin transporters by protein phosphorylation |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Protein phosphorylation and dephosphorylation are post-translational modifications that are commonly used to regulate activity and/or function of a particular protein. The serine-threonine kinase PINOID has been shown to promote the polar localization of PIN1 and the pinoid mutant exhibits a similar phenotype to that of pin1 (Christensen et al., 2000). The apical and basal membrane localization of PIN1 were also shown to be manipulated by the overexpression and inactivation of PID (Friml et al., 2004). Therefore, PID appears to function as a binary switch that can reverse the direction of auxin movement. The activation of PID, in turn, requires phosphorylation of the protein by a 3-phosphoinositide-dependent protein kinase 1 (PDK1) (Zegzouti et al., 2006). PIN proteins also appear to be regulated by dephosphorylation catalysed by the trimeric serine-threonine protein phosphatase 2A (PP2A) (Michniewicz et al., 2007). A regulatory subunit of PP2A is encoded by the ROOT CURLING IN NPA1 (RCN1) gene. The rcn1 mutant exhibits a decrease in PP2A activity, defects in root and hypocotyl elongation, and altered apical hook formation (Garbers et al., 1996). This suggests that PP2A may play a role in NPA-sensitive root acropetal auxin transport (DeLong et al., 2002).
The linker region between the two repeated nucleotide binding domains of ABCB proteins is a prominent target for phosphorylation in yeast and humans (Ambudkar et al., 1999). In Arabidopsis, phosphoproteomics of plasma membrane proteins revealed three possible sites in ABCB proteins that can be phosphorylated by related protein kinases (Nuhse et al., 2004). One potential candidate is PHOTOTROPIN1 (PHOT1), a plasma membrane serine-threonine protein kinase that functions in multiple blue-light responses (Inoue et al., 2008). The PHOT1 protein exhibits an intracellular localization upon blue-light illumination (Briggs and Christie, 2002; Wan et al., 2008) that is concurrent with the delocalization of PIN1 in vascular tissues of photoresponding hypocotyls (Blakeslee et al., 2004). However, to date there is no evidence of direct interactions between PHOT1 and PIN1. However, ABCB19 may regulate this interaction, as ABCB19 stabilizes PIN1 on the plasma membrane (Titapiwatanakun et al., 2008), and abcb19 mutants exhibit more rapid phototropic responses in hypocotyls (Noh et al., 2003; Lin and Wang, 2005; Nagashima et al., 2008). Another potential target of PHOT1 is PIN3, which is thought to contribute to lateral translocation of auxin (Friml et al., 2002b). PIN3 localization in hypocotyl epidermal cells, whose elongation is differentially regulated in tropic bending, suggests that PHOT1 functions in inactivating localized efflux of auxin mediated by PIN3 in cells below the site of illumination. However, blue light responses mediated by PHOT1 do not appear to regulate membrane localization of ABCB19 or PIN3, as, after the blue-light treatment, no alterations in the subcellular localization of ABCB19 and PIN3 are observed, whether native, epitope-tagged, or YFP/GFP translational fusion proteins are monitored (not shown).
|
Regulation of auxin transporters by ubiquitin-mediated proteolysis |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
The steady-state levels of many proteins that are implicated in auxin transport are actively regulated by ubiquitin-mediated protein degradation. The post-transcriptional stability of PIN proteins has been shown to require the presence of MODULATOR OF PIN (MOP) proteins (Malenica et al., 2007). The Arabidopsis mop2 and mop3 mutants were identified in a genetic screen in the eir1-1 mutant background for mutations that affect auxin responses and/or distribution. In addition to a root agravitropic phenotype, the mop2 and mop3 mutants also exhibited auxin-related phenotypes similar to those seen in pin mutants. Further characterization of these mutants showed a decrease in the abundance of PIN proteins, such as PIN1, PIN2, and PIN3, suggesting that MOP played an essential role in regulating the steady-state level of PIN proteins.
Cumulative evidence suggests that PIN2 is selectively regulated by ubiquitination (Abas et al., 2006). Gravistimulation of roots results in a greater abundance of plasma membrane-localized PIN2 in epidermal cells on the underside of the root. On the upper side of the root, PIN2 was found in an intracellular compartment as well as on the plasma membrane. This internalization of PIN2 appears to be controlled by proteasomic activity, as the internalization and degradation of PIN2 was prevented by pre-treatment with the proteasome inhibitor MG132 (Abas et al., 2006).
Regulation of PIN1 by ubiquitin-mediated turnover is suggested by the presence of a lower molecular weight band (50 kDa) typically observed in immunoblot analyses of PIN1 that is prevented by treatment with inhibitor cocktails containing MG132 (Titapiwatanakun et al., 2008). The presence of PIN1 proteolytic products may also explain differences observed between immunolocalizations of PIN proteins, which all utilize antisera generated against the central ‘soluble’ loop of the proteins, and some PIN-fluorescent protein fusions. Proteolytic turnover may also play a role in the stabilization of PIN1 associated with ABCB19-containing membrane subdomains, as PIN1 is more resistant to degradation in those fractions.
|
Regulation of auxin transporters by flavonoids |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
The effect of NPA can be mimicked by the activity of endogenous flavonoids, which can inhibit polar auxin transport and modify local auxin concentrations (Murphy et al., 2000). In addition, flavonol compounds, such as quercetin and kaempferol, can be displaced by NPA from the microsomal extract of Arabidopsis plants. Endogenous flavonols have also been shown to regulate auxin transport negatively and alter gene expressions and subcellular localization of PIN1, PIN2, and PIN4 (Peer et al., 2004; Peer and Murphy, 2007). To date, no evidence of flavonoid regulation of AUX1 has been reported.
The relationship between flavonoids and ABCB proteins has been demonstrated, as the addition of flavonols inhibits ABCB-mediated auxin transport in heterologous expression systems (Peer and Murphy, 2007). In abcb4 and abcb19 mutants, aggregations of quercetin accumulates in the same region where ABCB4 and ABCB19 would be localized (Terasaka et al., 2005; Titapiwatanakun et al., 2008). ABCB proteins, particularly ABCB4, are likely to be the principal targets of flavonoid regulation of auxin transport at the plasma membrane. Although the flavonoid-deficient transparent testa4 tt4 mutant displayed a slower gravitropic response compared to the wild type, the gravitropic response of abcb4 tt4 double mutant resembled that of abcb4, indicating that abcb4 was epistatic to tt4 (Lewis et al., 2007).
|
Regulation of auxin transporters by membrane composition |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
The mutant lacking STEROL METHYTRANSFERASE1 (SMT1) exhibits aberrant cell polarity, auxin distribution, and embryo development (Willemsen et al., 2003). SMT1 is required for the first step of sterol biosynthesis and for the correct membrane localization of PIN1 and PIN3, but not for localization of AUX1. The loss-of-function cpi1-1 mutant, which is deficient in the cyclopropylsterol isomerase1 that catalyses a step following SMT1 in the sterol biosynthesis pathway, was also recently shown to exhibit defects in PIN2 polarity (Men et al., 2008). In normal cytokinetic epidermal cells, PIN2 is detected in both apical and basal membranes, whereas, in the post-cytokinetic epidermal cells, PIN2 is localized only at the apical membrane. However, in the cpi1-1 mutant, where PIN2 endocytosis is altered, the subcellular localization of PIN2 following cytokinesis is associated with the cell-plate-like structure. Sterols internalized from the plasma membrane colocalize with the PIN2 recycling endosome and are both BFA-sensitive and actin-dependent, suggesting a link between endocytic sterol trafficking and PIN polarity (Grebe et al., 2003). However, not all phenoytpes resulting from altered sterol trafficking are derived from altered auxin transport. A mutation in a gene encoding an Arabidopsis sterol carrier protein-2 was recently shown to regulate normal seed and seedling metabolism (Zheng et al., 2008).
A defect in myo-inositol-1-phosphate synthase (MIPS) results in an altered embryogenesis, venation patterning, and root growth. MIPS plays a crucial role in inositol biosynthesis. Thus, it has been suggested that the phosphoinositide levels of the plasma membrane can directly impact polar auxin transport. Mutants lacking MIPS showed a slower rate of endocytosis and a higher degree of wortmannin sensitivity in PIN2-positive endosomes, thereby providing evidence for a contribution of MIPS to the regulation of vesicular trafficking in plants.
Specialized microdomains that are characteristically enriched in sterol lipids and remain soluble in high concentrations of detergents have been reported (Mongrand et al., 2004; Borner et al., 2005). These microdomains have also been shown to function in the association of membrane proteins and in endocytosis (Morel et al., 2006). Sterols and sphingolipids constitute a principal factor in the formation of plasma membrane microdomains (Heese-Peck et al., 2002; Jaillais and Gaude, 2008). Although the evidence that supports the existence of plasma membrane microdomains in plants is relatively limited, the lipid composition of the detergent-resistant membrane (DRM) fraction from Arabidopsis membranes is enriched in sterols, as well as glucosylceramide. A link between sterol composition and the endocytotic pathway has also been reported (Sharma et al., 2002). More recently, functional sphingolipid synthesis and trafficking has been shown to be required for normal plant development and growth (Chen et al., 2008), suggesting that sphingolipid content may also be an important factor in regulating membrane domains.
DRM fractions derived from plant cell cultures were shown to contain ABCB and PIN proteins (Mongrand et al., 2004; Borner et al., 2005; Morel et al., 2006). Interestingly, the localization of PIN1 in DRMs requires intact ABCB19, as PIN1 was undetectable in DRM fractions derived from abcb19 seedlings and mature plants (Fig. 3; Titapiwatanakun et al., 2008). The abcb19 mutant also exhibits an altered rate of endocytosis compared to the wild type. As the DRM-associated proteins in mammals are thought to be sorted and internalized via a caveolin-dependent pathway (Sharma et al., 2002), the presence of ABCB19 in DRMs suggests that it may not only stabilize membrane microdomains, but also, indirectly, regulate endocytotic processes. Consistent with this interpretation, some BFA-induced aggregates containing PIN1 remain intact in abcb19 after BFA is washed out, suggesting that ABCB19 also has an important function in reconstitution of the endosomes to the plasma membrane (Titapiwatanakun et al., 2008).
|
The importance of sterols in defining the proper membrane environment may explain the difficulty encountered in attempting biochemically to demonstrate PIN1 auxin efflux activity by heterologous expression in multiple host organisms (Petrasek et al., 2006; Blakeslee et al., 2007). However, Schizosaccharomyces pombe was recently found to be suitable for the expression of PIN1 as a fully active transporter (Titapiwatanakun et al., 2008). This appears to be due to the presence of plant-like sterol-enriched microdomains in S. pombe (Wachtler et al., 2003), not found in Saccharomyces cerevisiae or Xenopus oocytes.
|
Conclusion |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Regulation of auxin transport mechanisms is an important aspect of plant hormone biology, as impairment of auxin transport activity results in severe aberrations in plant growth and development. Plants regulate the activity and localization of these auxin transport proteins and protein complexes through a repertoire of cellular processes, many of which have now been identified. The use of Arabidopsis mutants, transgenic markers, and inducible expression constructs as well as concentration-dependent pharmalogical agents that interfere with specific proteins or enzymes have proven instrumental in deciphering these regulatory processes. While much attention has focused on their cellular trafficking pathways, the post-translational modifications of the auxin transport proteins, particularly by phosphorylation, ubiquitination, and maturation processes, are likely to be an important factor in regulating polar auxin transport and clearly need to be explored further. The role of ubiqutination and dynamic changes in the plasma membrane environment that affect the activity, localization and interaction of the auxin transport proteins deserve particular attention. The precise nature of the structural and biochemical properties that govern the interaction between auxin transport proteins and their membrane environment will require the development of new molecular genetic tools and pharmacological inhibitors to be fully elucidated.
|
Acknowledgements |
|---|
We thank Dr Wendy Ann Peer for a careful reading of the manuscript. This work is supported by the US Department of Energy to ASM.
|
References |
|---|
|
TopAbstractIntroductionPolar auxin transportClasses of auxin transport...Regulation of auxin transport...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...Regulation of auxin transporters...ConclusionReferences |
|---|
Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nature Cell Biology (2006) 8:249–256.[CrossRef][Web of Science][Medline]
Ambudkar SV, Dey S, Hrycyna CA, Ramachandra M, Pastan I, Gottesman MM. Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annual Review of Pharmacology and Toxicology (1999) 39:361–398.[CrossRef][Web of Science][Medline]
Ambudkar SV, Kim IW, Sauna ZE. The power of the pump: mechanisms of action of P-glycoprotein (ABCB1). European Journal of Pharmaceutical Sciences (2006) 27:392–400.[CrossRef][Web of Science][Medline]
Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M. Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. Journal of Biological Chemistry (2008) 283:21817–21826.
Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M, Mandel T, Kuhlemeier C. Auxin influx carriers stabilize phyllotactic patterning. Genes and Development (2008) 22:810–823.
Bandyopadhyay A, Blakeslee JJ, Lee OR, et al. Interactions of PIN and PGP auxin transport mechanisms. Biochemical Society Transactions (2007) 35:137–141.[CrossRef][Web of Science][Medline]
Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell (2003) 115:591–602.[CrossRef][Web of Science][Medline]
Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science (1996) 273:948–950.[Abstract]
Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G. Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. The Plant Journal (2002) 29:325–332.[CrossRef][Web of Science][Medline]
Blakeslee JJ, Bandyopadhyay A, Lee OR, et al. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. The Plant Cell (2007) 19:131–147.
Blakeslee JJ, Bandyopadhyay A, Peer WA, Makam SN, Murphy AS. Relocalization of the PIN1 auxin efflux facilitator plays a role in phototropic responses. Plant Physiology (2004) 134:28–31.
Blakeslee JJ, Peer WA, Murphy AS. Auxin transport. Current Opinion in Plant Biology (2005a) 8:494–500.[CrossRef][Web of Science][Medline]
Blakeslee JJ, Peer WA, Murphy AS. MDR/PGP Auxin transport proteins and endocytic cycling. Plant Cell Monographs: Plant Endocytosis (2005b) 159–176.
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature (2005) 433:39–44.[CrossRef][Web of Science][Medline]
Bonifacino JS, Rojas R. Retrograde transport from endosomes to the trans-Golgi network. Nature Reviews Molecular and Cellular Biology (2006) 7:568–579.[CrossRef]
Borner GH, Sherrier DJ, Weimar T, Michaelson LV, Hawkins ND, Macaskill A, Napier JA, Beale MH, Lilley KS, Dupree P. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiology (2005) 137:104–116.
Bouchard R, Bailly A, Blakeslee JJ, et al. Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. Journal of Biological Chemistry (2006) 281:30603–30612.
Boutte Y, Ikeda Y, Grebe M. Mechanisms of auxin-dependent cell and tissue polarity. Current Opinion in Plant Biology (2007) 10:616–623.[CrossRef][Web of Science][Medline]
Briggs WR, Christie JM. Phototropins 1 and 2: versatile plant blue-light receptors. Trends in Plant Science (2002) 7:204–210.[CrossRef][Web of Science][Medline]
Campanoni P, Nick P. Auxin-dependent cell division and cell elongation. 1-Naphthaleneacetic acid and 2,4-dichlorophenoxyacetic acid activate different pathways. Plant Physiology (2005) 137:939–948.
Casimiro I, Marchant A, Bhalerao RP, et al. Auxin transport promotes Arabidopsis lateral root initiation. The Plant Cell (2001) 13:843–852.
Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH. The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proceedings of the National Academy of Sciences, USA (1998) 95:15112–15117.
Chen M, Markham JE, Dietrich CR, Jaworski JG, Cahoon EB. Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell (2008) 20:1862–78.
Cho M, Lee SH, Cho HT. P-glycoprotein4 displays auxin efflux transporter-like action in Arabidopsis root hair cells and tobacco cells. The Plant Cell (2007) 19:3930–3943.
Christensen SK, Dagenais N, Chory J, Weigel D. Regulation of auxin response by the protein kinase PINOID. Cell (2000) 100:469–478.[CrossRef][Web of Science][Medline]
de Billy F, Grosjean C, May S, Bennett M, Cullimore JV. Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. Molecular Plant–Microbe Interactions (2001) 14:267–277.[CrossRef]
De Smet I, Jurgens G. Patterning the axis in plants: auxin in control. Current Opinion in Genetic Development (2007) 17:337–343.[CrossRef]
De Smet I, Tetsumura T, De Rybel B, et al. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development (2007) 134:681–690.
Delker C, Raschke A, Quint M. Auxin dynamics: the dazzling complexity of a small molecule's message. Planta (2008) 227:929–941.[CrossRef][Web of Science][Medline]
DeLong A, Mockaitis K, Christensen S. Protein phosphorylation in the delivery of and response to auxin signals. Plant Molecular Biology (2002) 49:285–303.[CrossRef][Web of Science][Medline]
Dharmasiri S, Swarup R, Mockaitis K, et al. AXR4 is required for localization of the auxin influx facilitator AUX1. Science (2006) 312:1218–1220.
Dhonukshe P, Grigoriev I, Fischer R, et al. Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proceedings of the National Academy of Sciences, USA (2008) 105:4489–4494.
Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proceedings of the National Academy of Sciences, USA (2008) 105:8790–8794.
Eckhoff A, Granzin J, Kamphausen T, Buldt G, Schulz B, Weiergraber OH. Crystallization and preliminary X-ray analysis of immunophilin-like FKBP42 from Arabidopsis thaliana. Acta Crystallogrophy Section F Structural Biology and Crystallization Communications (2005) 61:363–365.[CrossRef]
Friml J, Benkova E, Blilou I, et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell (2002a) 108:661–673.[CrossRef][Web of Science][Medline]
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature (2003) 426:147–153.[CrossRef][Web of Science][Medline]
Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature (2002b) 415:806–809.[Web of Science][Medline]
Friml J, Yang X, Michniewicz M, et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science (2004) 306:862–865.
Fu D, van Dam EM, Brymora A, Duggin IG, Robinson PJ, Roufogalis BD. The small GTPases Rab5 and RalA regulate intracellular traffic of P-glycoprotein. Biochimica et Biophysica Acta (2007) 1773:1062–1072.[Medline]
Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov A, Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science (1998) 282:2226–2230.
Garbers C, DeLong A, Deruere J, Bernasconi P, Soll D. A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO Journal (1996) 15:2115–2124.[Web of Science][Medline]
Geisler M, Kolukisaoglu HU, Bouchard R, et al. TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Molecular Biology of the Cell (2003) 14:4238–4249.
Geisler M, Blakeslee JJ, Bouchard R, et al. Cellular efflux of auxin catalysed by the Arabidopsis MDR/PGP transporter AtPGP1. The Plant Journal (2005) 44:179–194.[CrossRef][Web of Science][Medline]
Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature (2001) 413:425–428.[CrossRef][Web of Science][Medline]
Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell (2003) 112:219–230.[CrossRef][Web of Science][Medline]
Granzin J, Eckhoff A, Weiergraber OH. Crystal structure of a multi-domain immunophilin from Arabidopsis thaliana: a paradigm for regulation of plant ABC transporters. Journal of Molecular Biology (2006) 364:799–809.[CrossRef][Web of Science][Medline]
Grebe M, Xu J, Mobius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B. Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Current Biology (2003) 13:1378–1387.[CrossRef][Web of Science][Medline]
Heese-Peck A, Pichler H, Zanolari B, Watanabe R, Daum G, Riezman H. Multiple functions of sterols in yeast endocytosis. Molecular Biology of the Cell (2002) 13:2664–2680.
Inoue S, Kinoshita T, Matsumoto M, Nakayama KI, Doi M, Shimazaki K. Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proceedings of the National Academy of Sciences, USA (2008) 105:5626–5631.
Jaillais Y, Fobis-Loisy I, Miege C, Rollin C, Gaude T. AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature (2006) 443:106–109.[CrossRef][Web of Science][Medline]
Jaillais Y, Gaude T. Plant cell polarity: sterols enter into action after cytokinesis. Developmental Cell (2008) 14:318–320.[CrossRef][Web of Science][Medline]
Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miege C, Gaude T. The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell (2007) 130:1057–1070.[CrossRef][Web of Science][Medline]
Kepinski S. The anatomy of auxin perception. Bioessays (2007) 29:953–956.[CrossRef][Web of Science][Medline]
Kerr ID, Bennett MJ. New insight into the biochemical mechanisms regulating auxin transport in plants. Biochemistry Journal (2007) 401:613–622.[CrossRef][Web of Science][Medline]
Kimura M, Kagawa T. Phototropin and light-signaling in phototropism. Current Opinion in Plant Biology (2006) 9:503–508.[CrossRef][Web of Science][Medline]
Kimura Y, Morita SY, Matsuo M, Ueda K. Mechanism of multidrug recognition by MDR1/ABCB1. Cancer Science (2007) 98:1303–1310.[CrossRef][Medline]
Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wisniewska J, Paciorek T, Benkova E, Friml J. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Current Biology (2008) 18:526–531.[CrossRef][Web of Science][Medline]
Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J. Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. The Plant Cell (2006) 18:3171–3181.
Kramer EM, Bennett MJ. Auxin transport: a field in flux. Trends in Plant Science (2006) 11:382–386.[CrossRef][Web of Science][Medline]
Lee M, Choi Y, Burla B, Kim Y-Y, Jeon B, Maeshima M, Yoo J-Y, Martinoia E, Lee Y. The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nature Cell Biology (2008) doi:10.1038/ncb1782.
Lewis DR, Miller ND, Splitt BL, Wu G, Spalding EP. Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. The Plant Cell (2007) 19:1838–1850.
Lin R, Wang H. Two homologous ATP-binding cassette transporter proteins, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. Plant Physiology (2005) 138:949–964.
Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G. Sites and regulation of auxin biosynthesis in Arabidopsis roots. The Plant Cell (2005) 17:1090–1104.
Luckie DB, Wilterding JH, Krha M, Krouse ME. CFTR and MDR: ABC transporters with homologous structure but divergent function. Current Genomics (2003) 4:225–235.[CrossRef]
Luschnig C, Gaxiola RA, Grisafi P, Fink GR. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes and Development (1998) 12:2175–2187.
Malenica N, Abas L, Benjamins R, Kitakura S, Sigmund HF, Jun KS, Hauser MT, Friml J, Luschnig C. MODULATOR OF PIN genes control steady-state levels of Arabidopsis PIN proteins. The Plant Journal (2007) 51:537–550.[CrossRef][Web of Science][Medline]
Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO Journal (1999) 18:2066–2073.[CrossRef][Web of Science][Medline]
Mattsson J, Ckurshumova W, Berleth T. Auxin signaling in Arabidopsis leaf vascular development. Plant Physiology (2003) 131:1327–1339.
Men S, Boutte Y, Ikeda Y, Li X, Palme K, Stierhof YD, Hartmann MA, Moritz T, Grebe M. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nature Cell Biology (2008) 10:237–244.[CrossRef][Web of Science][Medline]
Michniewicz M, Zago MK, Abas L, et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell (2007) 130:1044–1056.[CrossRef][Web of Science][Medline]
Mongrand S, Morel J, Laroche J, Claverol S, Carde JP, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ. Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. Journal of Biological Chemistry (2004) 279:36277–36286.
Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule JJ, Blein JP, Simon-Plas F. Proteomics of plant detergent-resistant membranes. Molecular Cell Proteomics (2006) 5:1396–1411.[CrossRef]
Muller A, Guan C, Galweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO Journal (1998) 17:6903–6911.[CrossRef][Web of Science][Medline]
Multani DS, Briggs SP, Chamberlin MA, Blakeslee JJ, Murphy AS, Johal GS. Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science (2003) 302:81–84.
Murphy A, Peer WA, Taiz L. Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta (2000) 211:315–324.[CrossRef][Web of Science][Medline]
Murphy AS, Hoogner KR, Peer WA, Taiz L. Identification, purification, and molecular cloning of N-1-naphthylphthalmic acid-binding plasma membrane-associated aminopeptidases from Arabidopsis. Plant Physiology (2002) 128:935–950.
Nagashima A, Suzuki G, Uehara Y, et al. Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. The Plant Journal (2008) 53:516–529.[CrossRef][Web of Science][Medline]
Noh B, Bandyopadhyay A, Peer WA, Spalding EP, Murphy AS. Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1. Nature (2003) 423:999–1002.[CrossRef][Web of Science][Medline]
Noh B, Murphy AS, Spalding EP. Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. The Plant Cell (2001) 13:2441–2454.
Nuhse TS, Stensballe A, Jensen ON, Peck SC. Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. The Plant Cell (2004) 16:2394–2405.
Paciorek T, Zazimalova E, Ruthardt N, et al. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature (2005) 435:1251–1256.[CrossRef][Web of Science][Medline]
Palme K, Dovzhenko A, Ditengou FA. Auxin transport and gravitational research: perspectives. Protoplasma (2006) 229:175–181.[CrossRef][Web of Science][Medline]
Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS. Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. The Plant Cell (2004) 16:1898–1911.
Peer WA, Murphy AS. Flavonoids and auxin transport: modulators or regulators? Trends in Plant Science (2007) 12:556–563.[CrossRef][Web of Science][Medline]
Petrasek J, Cerna A, Schwarzerova K, Elckner M, Morris DA, Zazimalova E. Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiology (2003) 131:254–263.
Petrasek J, Mravec J, Bouchard R, et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science (2006) 312:914–918.
Quint M, Gray WM. Auxin signaling. Current Opinion in Plant Biology (2006) 9:448–453.[CrossRef][Web of Science][Medline]
Reinhardt D. Phyllotaxis: a new chapter in an old tale about beauty and magic numbers. Current Opinion in Plant Biology (2005) 8:487–493.[CrossRef][Web of Science][Medline]
Richter S, Geldner N, Schrader J, Wolters H, Stierhof YD, Rios G, Koncz C, Robinson DG, Jurgens G. Functional diversification of closely related ARF-GEFs in protein secretion and recycling. Nature (2007) 448:488–492.[CrossRef][Web of Science][Medline]
Rojas-Pierce M, Titapiwatanakun B, Sohn EJ, et al. Arabidopsis P-glycoprotein19 participates in the inhibition of gravitropism by gravacin. Chemistry and Biology (2007) 14:1366–1376.[CrossRef][Web of Science][Medline]
Sachs T. The control of the patterned differentiation of vascular tissues. Advances in Botanical Research Incorporating Advances in Plant Pathology (1981) 9:151–262.[Web of Science]
Santelia D, Vincenzetti V, Azzarello E, Bovet L, Fukao Y, Duchtig P, Mancuso S, Martinoia E, Geisler M. MDR-like ABC transporter AtPGP4 is involved in auxin-mediated lateral root and root hair development. FEBS Letters (2005) 579:5399–5406.[CrossRef][Web of Science][Medline]
Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova E. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes and Development (2006) 20:2902–2911.
Sharma P, Sabharanjak S, Mayor S. Endocytosis of lipid rafts: an identity crisis. Seminars in Cell Development Biology (2002) 13:205–214.[CrossRef]
Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K. Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proceedings of the National Academy of Sciences, USA (2003) 100:751–756.
Sidler M, Hassa P, Hasan S, Ringli C, Dudler R. Involvement of an ABC transporter in a developmental pathway regulating hypocotyl cell elongation in the light. The Plant Cell (1998) 10:1623–1636.
Sieburth LE, Muday GK, King EJ, Benton G, Kim S, Metcalf KE, Meyers L, Seamen E, Van Norman JM. SCARFACE encodes an ARF-GAP that is required for normal auxin efflux and vein patterning in Arabidopsis. The Plant Cell (2006) 18:1396–1411.
Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G. Co-ordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science (1999) 286:316–318.
Surpin M, Rojas-Pierce M, Carter C, Hicks GR, Vasquez J, Raikhel NV. The power of chemical genomics to study the link between endomembrane system components and the gravitropic response. Proceedings of the National Academy of Sciences, USA (2005) 102:4902–4907.
Swarup K, Benkova E, Swarup R, et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nature Cell Biology (2008) 10:946–954.[CrossRef][Web of Science][Medline]
Swarup R, Parry G, Graham N, Allen T, Bennett M. Auxin cross-talk: integration of signalling pathways to control plant development. Plant Molecular Biology (2002) 49:411–426.[Web of Science][Medline]
Swarup R, Kargul J, Marchant A, et al. Structure–function analysis of the presumptive Arabidopsis auxin permease AUX1. The Plant Cell (2004) 16:3069–3083.
Tanaka H, Dhonukshe P, Brewer PB, Friml J. Spatiotemporal asymmetric auxin distribution: a means to co-ordinate plant development. Cellular and Molecular Life Sciences (2006) 63:2738–2754.[CrossRef][Web of Science][Medline]
Teh OK, Moore I. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature (2007) 448:493–496.[CrossRef][Web of Science][Medline]
Terasaka K, Blakeslee JJ, Titapiwatanakun B, et al. PGP4, an ATP binding cassette P-glycoprotein, catalyses auxin transport in Arabidopsis thaliana roots. The Plant Cell (2005) 17:2922–2939.
Timpte C. Auxin binding protein: curiouser and curiouser. Trends in Plant Science (2001) 6:586–590.[CrossRef][Web of Science][Medline]
Titapiwatanakun B, Blakeslee J, Bandyopadhyay A, et al. ABCB19/PGP19 stabilizes PIN1 on membrane microdomains in Arabidopsis. The Plant Journal (2008) (in press).
Verrier PJ, Bird D, Burla B, et al. Plant ABC proteins: a unified nomenclature and updated inventory. Trends in Plant Science (2008) 13:151–159.[CrossRef][Web of Science][Medline]
Vieten A, Vanneste S, Wisniewska J, Benkova E, Benjamins R, Beeckman T, Luschnig C, Friml J. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development (2005) 132:4521–4531.
Wachtler V, Rajagopalan S, Balasubramanian MK. Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe. Journal of Cell Science (2003) 116:867–874.
Wan YL, Eisinger W, Ehrhardt D, Kubitscheck U, Baluska F, Briggs W. The subcellular localization and blue-light-induced movement of phototropin 1-GFP in etiolated seedlings of Arabidopsis thaliana. Molecular Plant (2008) 1:103–117.
Went FW. On growth-accelerating substances in the coleoptile of Avena sativa. Proceedings of the Koninklijke Akademie Van Wetenschappen Te Amsterdam (1927) 30:10–19.[Web of Science]
Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B. Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. The Plant Cell (2003) 15:612–625.
Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J. Polar PIN localization directs auxin flow in plants. Science (2006) 312:883.
Wu G, Lewis DR, Spalding EP. Mutations in Arabidopsis multidrug resistance-like ABC transporters separate the roles of acropetal and basipetal auxin transport in lateral root development. The Plant Cell (2007) 19:1826–1837.
Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E. High-affinity auxin transport by the AUX1 influx carrier protein. Current Biology (2006) 16:1123–1127.[CrossRef][Web of Science][Medline]
Zazimalova E, Krecek P, Skupa P, Hoyerova K, Petrasek J. Polar transport of the plant hormone auxin: the role of PIN-FORMED (PIN) proteins. Cellular and Molecular Life Sciences (2007) 64:1621–1637.[CrossRef][Medline]
Zegzouti H, Anthony RG, Jahchan N, Bogre L, Christensen SK. Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proceedings of the National Academy of Sciences, USA (2006) 103:6404–6409.
Zheng BS, Ronnberg E, Viltanen L, Salminen TA, Lundgren K, Mortiz T, Edqvist J. Arabidopsis sterol carrier protein-2 is required for normal development of seeds and seedlings. Journal of Experimental Botany (2008) doi:10.1093/jxb/ern201.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  P. Nick, M.-J. Han, and G. An Auxin Stimulates Its Own Transport by Shaping Actin Filaments Plant Physiology, September 1, 2009; 151(1): 155 - 167. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||