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Maintenance of Asymmetric Cellular Localization of an Auxin Transport Protein Through Interaction with the Actin Cytoskeleton

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Maintenance of Asymmetric Cellular Localization of an Auxin Transport Protein Through Interaction with the Actin Cytoskeleton J Plant Growth Regul (2000) 19:385–396 DOI: 10.1007/s003440000041 © 2000 Springer-Verlag Maintenance of Asymmetric Cellular Localization of an Auxin Transport Protein through Interaction with the Actin Cytoskeleton Gloria K. Muday* Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27109-7325, USA ABSTRACT In shoots, polar auxin transport is basipetal (that is, addition, the idea that this localization of the efflux from the shoot apex toward the base) and is driven carrier may control both the polarity of auxin move- by the basal localization of the auxin efflux carrier ment and more globally regulate developmental po- complex. The focus of this article is to summarize the larity is explored. Finally, evidence indicating that experiments that have examined how the asymmet- the gravity vector controls auxin transport polarity is ric distribution of this protein complex is controlled summarized and possible mechanisms for the envi- and the significance of this polar distribution. Ex- ronmentally induced changes in auxin transport po- perimental evidence suggests that asymmetries in larity are discussed. the auxin efflux carrier may be established through localized secretion of Golgi vesicles, whereas an at- tachment of a subunit of the efflux carrier to the Key words: Auxin transport; Actin cytoskeleton; actin cytoskeleton may maintain this localization. In Polarity; F-actin; Gravity; Embryo development INTRODUCTION maintaining the localization after initial sorting is complete (Drubin and Nelson 1996; Nelson and The mechanism by which cells and tissues develop Grindstaff 1997). Protein sorting through directed and maintain polarity is a growing area of study. In vesicle targeting is critical for establishment of asym- mammalian systems, a number of proteins have metry (Nelson and Grindstaff 1997), whereas at- been examined to understand how asymmetric cel- tachment to the actin cytoskeleton, either directly or lular localization is established and maintained. In through large protein complexes, maintains the asymmetric cells, such as epithelial or nerve cells, asymmetric localization (Colledge and Froehner there are mechanisms both for initially sorting pro- 1998; Froehner 1993). teins into different membrane domains and for In plant cells, one of the best-understood ex- Online publication 2 May 2001 amples of a protein with asymmetric cellular local- *Corresponding author; e-mail: [email protected] ization is the auxin efflux carrier, which controls 385 386 G. K. Muday plex interacts with the actin cytoskeleton to fix this protein in one domain of the plasma membrane. In addition, the idea is explored that this localization of the efflux carrier may control both the polarity of auxin movement and globally regulate developmen- tal polarity. Finally, experimental results are sum- marized that suggest that environmental stimuli can change the polarity of auxin transport, and the pos- sible roles of the cytoskeleton in mediating these alterations in auxin transport direction are dis- cussed. BIOCHEMICAL CHARACTERIZATION OF THE AUXIN EFFLUX CARRIER Figure 1. Schematic model of the chemiosmotic hypoth- A biochemical dissection of the auxin efflux carrier esis for polar auxin transport. Protonated IAA in the cell has increased our understanding of the regulation of wall space can enter the cell either by diffusion or by an this protein complex and how its localization to the uptake carrier. Once in the more basic cytoplasm, the IAA basal plasma membrane controls the polarity of dissociates and can exit only by the auxin efflux carrier. auxin movement. The efflux carrier complex ap- The names of the protein that may constitute auxin trans- pears to be composed of at least two polypeptides. porters are in parentheses. Reprinted from Muday (2000) One polypeptide is an integral membrane trans- with kind permission from Kluwer Academic Publishers. porter presumably encoded by one of the members of the PIN gene family (Palme and Ga¨lweiler 1999). A second polypeptide (the NPA-binding protein) polar auxin transport. Auxins, of which indole-3- binds synthetic inhibitors of auxin efflux, including acetic acid (IAA) is the predominant naturally oc- naphthylphthalamic acid, and may act as a regula- curring hormone, move through plants by a unique tory polypeptide (Dixon and others 1996; Muday polar transport mechanism (reviewed in Goldsmith 2000). The existence of a third, rapidly turned over 1977; Lomax and others 1995). This polar move- protein that connects these two subunits has also ment of auxin in the shoot is a cell-to-cell move- been suggested (Morris and Robinson 1998; Morris ment from the shoot apex toward the base. Polar and others 1991). auxin transport results in an auxin gradient down Several members of the PIN gene family in Ara- the length of the plant, with the highest auxin con- bidopsis have been identified (Ga¨lweiler and others centrations found in the regions of greatest elonga- 1998; Mu¨ ller and others 1998), indicating that there tion (Ortuno and others 1990). There are two pro- are multiple auxin efflux carriers with distinct ex- tein complexes that control auxin movement into pression patterns (Palme and Ga¨lweiler 1999). Four and out of cells (Lomax and others 1995). These groups published the isolation of the PIN2 gene, protein complexes, the auxin uptake carrier, and the within several months, but using different names. auxin efflux carrier, respectively, are shown in Fig- PIN2 is equivalent to EIR1, AGR1, and WAV6 (Chen ure 1. IAA can move into cells both passively, be- and others 1998; Luschnig and others 1998; Mu¨ ller cause it is hydrophobic when protonated, and and others 1998; Utsuno and others 1998). Plants through an uptake carrier. The amount and direc- with mutations in either PIN1 or PIN2 have pheno- tion of polar auxin transport are thought to be con- types consistent with tissue-specific alterations in trolled by the auxin efflux carrier. Basal localization auxin transport (Ga¨lweiler and others 1998; Mu¨ ller of an auxin efflux carrier in cells of the plant stem and others 1998; Okada and others 1991) and have has also been proposed to determine the polarity of alterations in auxin transport in the affected tissues IAA transport (Ga¨lweiler and others, 1998; Jacobs (Chen and others 1998; Okada and others 1991; and Gilbert 1983; Rubery and Sheldrake 1974). Rashotte and others 2000). PIN genes encode pro- This review focuses on the asymmetric localiza- teins with 10 membrane-spanning domains and tion of the auxin efflux carrier. Evidence will be have similarities to other membrane transport pro- summarized that indicates that the auxin efflux car- teins (Chen and others 1999). The protein products rier complex may be directed to one membrane of these genes show an asymmetric localization in through vesicle targeting and that this protein com- the plasma membrane that is consistent with con- Polar Auxin Transport and the Cytoskeleton 387 trolling the polarity of auxin movement (Ga¨lweiler binding activity (Bernasconi and others 1996; Dixon and others 1998; Mu¨ ller and others 1998). It has and others 1996), whereas disruption of membranes been suggested, therefore, that the PIN genes en- by detergent, followed by protease treatment, results code one polypeptide of the auxin efflux carrier. in a total loss of NPA-binding activity (Bernasconi Until the recent identification of the PIN proteins, and others 1996). Furthermore, plasma membrane most studies of the auxin efflux carrier focused on vesicles have been subjected to several different the NPA-binding protein. The activity of this protein treatments that should convert them to an inside- can be followed using a binding assay with [3H]- out orientation (Bernasconi and others 1996; Dixon NPA. NPA binds with high affinity to a single class of and others 1996; Hertel and others 1983), although NPA-binding proteins associated with the zucchini the effectiveness of these treatments was only veri- plasma membrane (Muday and others 1993). There- fied by analysis of marker enzymes in one case fore, this assay has allowed extensive biochemical (Dixon and others 1996). In two of these reports, characterization of the NPA-binding protein. In ad- inside-out vesicles had twofold to fourfold increases dition, an [3H]-azido NPA derivative has been syn- in NPA-binding activity and fourfold to fivefold in- thesized (Voet and others 1987) and has been used creases in protease sensitivity of NPA-binding activ- to identify a 23-kDa protein that binds both NPA ity compared with right-side-out vesicles (Dixon and and IAA (Zettl and others 1992). others 1996; Hertel and others 1983). Therefore, the Several lines of evidence suggest that the protein NPA-binding site appears to be localized to the cy- that binds inhibitors of auxin efflux, including NPA, toplasmic face of the membrane and poised for in- is distinct from the PIN gene products. Treatments teraction with the cytoskeleton. with inhibitors of protein translation or protein pro- cessing in the Golgi apparatus prevent the NPA- mediated reductions in auxin transport without al- EVIDENCE FOR NPA-BINDING PROTEIN tering the amount of NPA-binding activity (Morris INTERACTION WITH ACTIN and Robinson 1998; Morris and others 1991; Wilkinson and Morris 1994). These results suggest One of the hallmarks of proteins that interact with that the NPA-binding and auxin-efflux activities are the cytoskeleton is their retention in the pellet after on separate proteins and support the idea that a ultracentrifugation
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