Polar Auxin Transport

Abstract

Auxins, a group of plant signalling compounds, ensure proper growth and development of the plant in relation to both external and internal stimuli. Within a plant, auxin is distributed asymmetrically, thus creating local auxin maxima and minima. Such asymmetric auxin distribution underlies many developmental and stress adaptation processes and facilitates their spatial and temporal coordination. The appropriate local auxin level is achieved by regulation of biosynthesis, metabolism and through active, cell‐to‐cell transport relying on auxin carriers that are embedded in the plasma membrane. Owing to the physical–chemical properties of the auxin molecule, the asymmetric (polar) localisation of auxin efflux carriers, analogous in neighbouring cells, determines the direction of intercellular auxin flow (polar auxin transport). With respect to the important function of polar auxin transport for plant development, the polar auxin transport machinery is subject to a tight control at multiple regulatory levels.

Key Concepts

  • Auxin flow through polar auxin transport pathways relies on concerted action of passive diffusion and auxin transporters.
  • Complex machinery consisting of both auxin carriers and regulatory networks modulates polar auxin transport.
  • Polar auxin transport machinery, together with auxin biosynthesis and its further metabolism, contributes to establishment and control of auxin homeostasis and therefore to the availability of auxin for signalling pathways.
  • Detailed quantitative data are needed for further understanding of polar auxin transport regulation.
  • Mathematical modelling based on detailed quantitative data represents a promising tool to understand contribution of individual processes to resulting polar auxin flow.

Keywords: plant hormones; auxin maxima and minima; auxin transporters; PIN proteins; ABCB proteins; AUX1/LAX proteins; Arabidopsis thaliana

Figure 1. Auxin and its transport. (a) Chemical structure of the most abundant native auxin indole‐3‐acetic acid (IAA). (b) Auxin flow through plant. Postembryonic plant growth and development is regulated by auxin distribution (symbolised by arrows) to create auxin minima and maxima. In the shoot, reverse, and in the root, inverse fountain‐like auxin flow (Benková et al., ) maintains proper plant growth and allows adaptation to environmental changes. Main processes regulated by auxin are emphasised. Adapted from Prusinkiewicz and Runions 2012 © John Wiley and Sons Ltd. (c) Cell‐to‐cell auxin transport. The short‐distance, cell‐to‐cell auxin transport is achieved by the defined, often polar, localisation of individual transporters and underlies the formation of auxin minima and maxima, which are important for proper plant growth and adaptation to environmental stimuli. IAA (auxin) can enter the cell either in a protonated form (IAAH) via passive transport or as an anion through the influx carriers from the family AUX1/LAX and some members of the ABCB family. Inside the cell, IAAH dissociates because of the higher pH within the cytoplasm. IAA anion (IAA) cannot pass the membrane by passive diffusion; therefore, it must be exported by active transport through plasma membrane‐localised efflux carriers belonging to either PIN of ABCB families. Thus, the auxin efflux carriers represent bottlenecks in auxin movement through cells and it is their polar localisation (if analogous in neighbouring cells) that determines the direction of the auxin flow.
Figure 2. Auxin transporters and auxin flow during embryogenesis and root gravitropic response. Auxin regulates many aspects of plant development and adaptation to environmental stimuli. In this figure, we describe the involvement of polar auxin transport at early steps of plant development (embryogenesis) and during the response of the root to gravitropic stimulus. Adapted from Petrášek and Friml . (a) Auxin distribution during embryogenesis. Arrows indicate auxin flow mediated by a particular transporter; dotted lines indicate the cell‐type‐specific localisation of particular auxin transporters with no obvious polarity. PIN7, localised at the apical sides of the suspensor cells (s), transports auxin towards the apical cell (a) that forms the proembryo; therefore, PIN1, which is localised at all inner cell sides, distributes auxin homogenously. ABCB1 and ABCB19 cooperate during this initial stage and are localised apolarly in all cells or only in the uppermost suspensor cell, respectively. The crucial moment in the setting of the basal end of the apical–basal embryonic axis occurs during the early globular stage, when PIN1 starts to be localised basally in the proembryonal cells, and PIN7 is simultaneously shifted from the apical to the basal plasma membrane of suspensor cells. These PIN polarity rearrangements reverse the auxin flow downwards and, with the aid of PIN4, lead to auxin accumulation in the forming hypophysis (h). At this stage, ABCB19 helps to maintain the auxin distribution in the outer layers of the embryo. In triangular‐ and heart‐stage embryos, bilateral symmetry is established through auxin maxima at the incipient cotyledon (c) primordia. These auxin maxima are generated by PIN1 activity in the epidermis; in the inner cells of cotyledon primordia, however, PIN1 mediates basipetal auxin transport towards the root pole. SAM, future shoot apical meristem. (b) Positive root gravitropism. In starch‐containing, gravity‐sensing columella cells, PIN3 is relocalised from a symmetric distribution (left) towards the newly established bottom side after gravistimulation (right). The auxin that is redirected to the lower side of the root tip is further transported to the elongation zone by epidermal PIN2/AUX1mediated flow, where it inhibits the cell growth and causes the downward bending of the root. ABCB4 and ABCB19 are considered to regulate gravitropic response, as their mutants show enhanced root gravitropic bending. Coloured arrows indicate auxin flow mediated by a particular transporter; dotted lines indicate the cell‐type‐specific localisation of particular auxin transporters with no obvious polarity and black arrows indicate the gravity vector (left) and the direction of bending (right). Adapted from Petrášek and Friml 2009 © Company of Biologists Ltd.
Figure 3. Mutant versions of crucial auxin transporters. Often, single mutants of auxin transporters do not show a dramatic phenotype, owing to the high redundancy within the protein families [described in Vieten et al., ]. The figure shows the most obvious phenotypes of selected auxin transporter mutants. (a) Phenotype of full‐grown wild type plant. (b) The auxin efflux carrier PIN‐FORMED 1 (PIN1) is expressed almost everywhere in the plant, but pin1 mutants are characterised typically by an inflorescence meristem that does not initiate any flowers, resulting in the formation of a naked inflorescence stem (Gälweiler et al., ). (c) The abcb19 (ARABIDOPSIS THALIANA ATPBINDING CASSETTE B19) mutant shows phenotype consisting of several features connected to auxin action but the most obvious one is reduced stem height (partial dwarfism; Noh et al., ). (d) Phenotype of wild‐type Arabidopsis seedling. (e) Loss of function of an auxin influx transporter, aux1 (AUXIN RESISTANT 1 (AUX1); Bennett et al., ), as well as of the efflux transporter pin2 (f) (EIR1/PIN‐FORMED 2 (PIN2)/AGR1; Luschnig et al., ; Müller et al., ), results in agravitropic roots, as auxin is not only regulating proper plant growth but also adaptation to environmental changes, such as gravity stimulus. (g) Proper auxin distribution is crucial for organ development; therefore, the triple mutant of the auxin influx carrier aux1 lax1/2 results in misshaped seedlings (Robert et al., ). (h) Loss of the closely related AGCVIII protein kinases pid wag1 wag2, which orchestrate the proper localisation of distinct auxin carriers, results in arrested development (Dhonukshe et al.,).
Figure 4. Predicted auxin transporters topology. (a) Auxin transporters of the AUX1/LAX family represented by the auxin influx carrier AtAUX1, auxin transporters of the PIN family represented by the auxin efflux carrier AtPIN1 with long cytosolic loop, (b) the endoplasmic reticulum (ER)‐localised auxin carrier AtPIN5 with short cytosolic loop (b) and (c) auxin transporters of the ABCB family represented by the auxin efflux carrier AtABCB19. Adapted from Petrášek et al. 2011 © Springer. (d) AtNRT1.1 primarily functions as a dual‐affinity transporter, which can change its affinity for nitrate in response to substrate availability. The figure shows a cylinder representation of the AtNRT1.1 dimer with highlighted Thr101. The two monomers are coloured in pale green and light blue, according to Sun and Zheng .
Figure 5. Cellular processes involved in auxin transport regulation. This figure shows a schematic overview of cellular distribution of main auxin carriers and processes that are involved in control of their abundance, localisation and activity. Cellular uptake of auxin is mediated by proteins from the auxin influx carrier family AUX1/LAX and by selected ABCB transporters. Cellular auxin efflux requires the action of certain ABCB transporters, and PINs (PIN1, 2, 3, 4, 7) at the plasma membrane (PM). Localisation of PINs (PIN5, 6, 8) at the endoplasmic reticulum (ER) membrane, together with some proteins from the PILS family, leads to compartmentalisation of auxin between cytoplasm and lumen of the ER, thus modifying overall auxin metabolic conversion. Auxin homeostasis is sensed by nuclear TIR1/AFB‐Aux/IAA coreceptor complexes. Intracellular trafficking of the auxin transporters regulates their abundance at the PM, comprising both recycling back to the PM (GNOM‐dependent, over early endosomes, EE) and the targeting to the lytic vacuole for degradation (over sorting endosomes (SE) and the trans‐Golgi network (TGN)). Although all auxin transporters undergo intracellular trafficking, PIN2 was most studied so far. Endocytic sorting and further targeting of PIN proteins into the lytic vacuole depends on putative retromer subunit SNX1, which functions as a gating factor, promoting protein recycling to the PM and thereby antagonising vacuolar sorting. CLASP‐mediated tethering of SNX1 to microtubules links PIN sorting to cytoskeleton components. Posttranslational modifications regulate the abundance, polarity and activity of auxin transporters: ubiquitylation targets PINs towards the lytic vacuole, phosphorylation regulates either their polarity (by PID/WAG) towards apical PM or their activity (by D6PK). U, ubiquitin; P, phosphate and MT, microtubules. Adapted from Retzer et al. 2014 © Springer.
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Further Reading

Bennett T, Hines G and Leyser O (2014) Canalization: what the flux? Trends in Genetics 30: 41–48.

Bishopp A and Bennett MJ (2014) Hormone crosstalk: directing the flow. Current Biology 24: R366R368.

Taiz L, Zeiger E, Moller IM and Murphy A (eds) (2015) Plant Physiology and Development. Sunderland, MA: Sinauer Associates.

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Jozef, Lacek, Katarzyna, Retzer, Christian, Luschnig, and Eva, Zažímalová(Apr 2017) Polar Auxin Transport. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020116.pub2]