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Polar Targeting and Endocytic Recycling in Auxin-Dependent ANRV356-CB24-18 ARI 3 September 2008 16:57 ANNUAL Polar Targeting and REVIEWS Further Click here for quick links to Annual Reviews content online, Endocytic Recycling including: • Other articles in this volume • Top cited articles in Auxin-Dependent • Top downloaded articles • Our comprehensive search Plant Development Jurgen¨ Kleine-Vehn and Jirˇı´ Friml Department of Plant Systems Biology, VIB, and Department of Molecular Genetics, Ghent University, 9052 Ghent, Belgium; email: [email protected] Annu. Rev. Cell Dev. Biol. 2008. 24:447–73 Key Words The Annual Review of Cell and Developmental trafficking, endocytosis, polar auxin transport, PIN proteins Biology is online at cellbio.annualreviews.org This article’s doi: Abstract 10.1146/annurev.cellbio.24.110707.175254 Plant development is characterized by a profound phenotypic plastic- Copyright c 2008 by Annual Reviews. ⃝ ity that often involves redefining of the developmental fate and polar- All rights reserved ity of cells within differentiated tissues. The plant hormone auxin and 1081-0706/08/1110-0447$20.00 its directional intercellular transport play a major role in these pro- Plant Hormones 2010.1:447-473. Downloaded from www.annualreviews.org Access provided by Cambridge University on 05/01/17. For personal use only. cesses because they provide positional information and link cell polar- ity with tissue patterning. This plant-specific mechanism of transport- dependent auxin gradients depends on subcellular dynamics of auxin transport components, in particular on endocytic recycling and polar targeting. Recent insights into these cellular processes in plants have revealed important parallels to yeast and animal systems, including clathrin-dependent endocytosis, retromer function, and transcytosis, but have also emphasized unique features of plant cells such as diversity of polar targeting pathways; integration of environmental signals into subcellular trafficking; and the link between endocytosis, cell polarity, and cell fate specification. We review these advances and focus on the translation of the subcellular dynamics to the regulation of whole-plant development. 447 ANRV356-CB24-18 ARI 3 September 2008 16:57 behavioral responses, such as the fight-or-flight Contents response, to overcome environmental stress. In contrast, during their evolution plants DEVELOPMENTAL emphasized increased physiological tolerance INTRODUCTION . 448 and phenotypic plasticity. These different POLAR TARGETING . 449 life strategies are also adequately reflected in Passengers and Destinations: Polar the various ways in which animals and plants Cargos and Polar Domains . 450 establish their body architecture. Whereas Tickets to Go or to Stay: during embryogenesis animals are already Polar Targeting Signals. 452 defining their adult shape to a large extent, Staying at the Station: Retention in plants this early developmental phase just at the Polar Domains. 453 sketches a basic body plan, and the final How to Get There: Polar shape of a plant will be largely defined by an Targeting Pathways . 453 elaborate postembryonic development (Weigel ENDOCYTIC RECYCLING &Jurgens¨ 2002). To achieve this develop- IN PLANT CELLS . 454 mental plasticity, plants maintain permanent The Back and Forth: Constitutive populations of stem cells (meristems) at the Endocytic Recycling of Plasma growing root and shoot apices and are able Membrane Proteins . 454 to redefine the developmental programs as Getting Away: Endocytosis well as the polarity of already specified tissues. in Plant Cells . 455 Thus, plants can sustain and regulate their Getting Back: Recycling in growth rate, can postembryonically form new Plant Cells. 457 organs, and possess a high capacity for tissue Going to the Other Side: regeneration (Steeves & Sussex 1989, Weigel Transcytosis Linking Endocytic &Jurgens¨ 2002). Different animal species also Recycling and Polar Targeting. 459 retain these capabilities to some extent; how- Separating the Daughters: Endocytic ever, plants are far superior in utilizing these Recycling in Cytokinetic Cells . 461 mechanisms for individually shaping their body EXEMPLIFIED CASES: POLAR according to the demands of the environment. TARGETING AND The plant signaling molecule auxin determines ENDOCYTIC RECYCLING many aspects of this flexible plant development. IN PLANT DEVELOPMENT . 462 Auxin acts as a prominent signal, providing, by Induced Endocytosis in Plants . 462 its local accumulation in selected cells, a spatial Integrating Developmental and temporal reference for changes in the and Environmental Signals Plant Hormones 2010.1:447-473. Downloaded from www.annualreviews.org Access provided by Cambridge University on 05/01/17. For personal use only. developmental program (Reinhardt et al. 2000, through Polarity Modulations . 463 Friml 2003, Leyser 2006, Esmon et al. 2006, Canalization Hypothesis and the Tanaka et al. 2006, Dubrovsky et al. 2008). Effect of Auxin on Its Auxin is distributed through tissues by a di- Own Efflux . 465 rectional cell-to-cell transport system, termed polar auxin transport, that depends on specific auxin carrier proteins (Figure 1) (Benjamins et al. 2005, Blakeslee et al. 2005, Kramer & DEVELOPMENTAL Bennett 2006, Vieten et al. 2007). Auxin efflux INTRODUCTION Polar auxin carriers of the PIN-FORMED (PIN) family transport: the Animals and plants evolved basic biologi- (Galweiler¨ et al. 1998, Luschnig et al. 1998, directional transport cal differences that characterize their survival Chen et al. 1998, Utsono et al. 1998, Petra´sekˇ of the plant hormone strategies. Animals developed elaborate sensory et al. 2006) show a polar subcellular localiza- auxin from cell to cell and locomotory capacities that enable complex tion that correlates with and determines the 448 Kleine-Vehn Friml · ANRV356-CB24-18 ARI 3 September 2008 16:57 output related to auxin-mediated signaling. PIN At the level of polar auxin transport, many developmental and environmental signals are Recycling: Efux carrier integrated. By rearranging the subcellular – + membranes and other IAAH IAA + H localization of PIN auxin efflux carriers, such molecules recycle from signals influence auxin-dependent patterning intracellular endocytic and contribute substantially to the adaptive compartments back to and flexible nature of plant development. the plasma membrane Our aim is to review recent advances on Tight junctions: subcellular trafficking and polar targeting in anchored protein complexes forming a plants and to highlight links with physiol- physical barrier – + IAAH IAA + H ogy and development. A special focus is given between polar to auxin-dependent regulation of development domains; limit lateral diffusion and are auxin transport because this area is intimately linked to en- Direction of polar Cytoplasm docytic recycling and polar targeting. Most of involved in polarity pH = 7.0 establishment and these concepts were formulated on the basis of maintenance in animal studies in the model plant Arabidopsis thaliana; epithelial cells nonetheless, they seem to apply to a large extent to higher plants in general. Cell wall pH = 5.5 AUX1/LAX POLAR TARGETING Infux carrier The establishment and maintenance of cell polarity are central themes of developmental Figure 1 and cell biology because individual cell polar- The chemiosmotic hypothesis: far ahead of its time! ities, transmitted by cell divisions, are trans- Rubery & Sheldrake postulated in the mid-1970s the so-called chemiosmotic hypothesis for directional lated into tissue and organ polarity and, ulti- intercellular auxin movement (Rubery & Sheldrake mately, shape. In addition, cell polarity plays a 1974 and, independently, Raven 1975). Accordingly, key role in directional signaling and intercellu- the auxin indole acetic acid (IAAH) is largely pro- lar communication. tonated at the lower pH of the cell wall and can pass At the level of individual cells, polarity is through the plasma membrane into the cell. In the higher-pH cytosol, part of the IAAH is deprotonated, typically reflected by the asymmetric distribu- and the resulting charged IAA− is largely membrane tion of intracellular components that can form impermeable and requires transporter activity to functionally and/or morphologically distinct Plant Hormones 2010.1:447-473. Downloaded from www.annualreviews.org exit the cell. The localization of the PIN-FORMED Access provided by Cambridge University on 05/01/17. For personal use only. domains (Bonifacino & Lippincott-Schwartz (PIN) auxin efflux carrier at the plasma membrane 2003). Mechanisms for generating or maintain- determines the auxin exit site from an individual cell. Coordinated polar localization of PINs in a given ing cell polarity have been extensively studied tissue hence determines the direction of cell-to-cell in different model organisms, such as worms, auxin transport. AUX1/LAX1 denotes auxin influx flies, mammals, and yeasts (e.g., Knoblich 2000, carriers AUXIN RESISTANT1/LIKE AUX1. Irazoqui & Lew 2004, Margolis & Borg 2005, Nance 2005). Animal epithelial cells are a fa- direction of auxin flow through tissues (Friml vorite model system because their plasma mem- et al. 2004, Wisniewska´ et al. 2006). In plants, brane harbors two distinct domains that are polarities of tissue and of individual cells are separated by tight junctions: an apical domain closely connected by the flow of auxin (Sauer facing the lumen and a basolateral domain et al. 2006), and the cell biological processes (Mostov et al. 2003, Janssens & Chavrier 2004). depending on vesicle trafficking and
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