Editors' ChoicePlant biology

Shaping Up with Auxin

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Science Signaling  12 Oct 2010:
Vol. 3, Issue 143, pp. ec314
DOI: 10.1126/scisignal.3143ec314

Two receptors have been identified for the plant hormone auxin. One, the TIR1 signaling system, mediates auxin’s transcriptional responses. The other is AUXIN BINDING PROTEIN 1 (ABP1), the function of which has been elusive because it is encoded by an essential gene. ABP1 exists in two pools; the majority is localized to the endoplasmic reticulum (ER), and a smaller pool is secreted and interacts with cell surface proteins to associate with the plasma membrane. Two groups, Xu et al. and Robert et al., report that ABP1 mediates the rapid effects of auxin in Arabidopsis leaf epidermal cells and root epidermal cells (see commentary by Pietra and Grebe).

In plant leaves, the pavement cells form an interdigitated pattern resembling a jigsaw puzzle. This pattern involves the guanosine triphosphatases ROP2 (or ROP4), which organizes the actin cytoskeleton in the lobe of the extending cell, and ROP6, which organizes the microtubule cytoskeleton in the indentating adjacent cell. Xu et al. found that the addition of a synthetic auxin (NAA) promoted interdigitation, whereas mutants with compromised auxin production had reduced interdigitation and resembled plants with reduced function of both of the functionally redundant guanosine triphosphatases ROP2 and ROP4. NAA rapidly, within 30 seconds, increased the amount of active ROP2 or ROP6 and promoted the redistribution of their downstream effectors, RIC4 and RIC1. These NAA-mediated responses required ABP1 and were compromised in plants with a weak allele, abp1-5, that fails to bind auxin effectively or in plants in which ABP1 was knocked down. In vivo auxin signaling involves the polarized transport of auxin, which is mediated by the auxin transporter PIN1. PIN1 was preferentially localized to the lobe tips, and this distribution was disrupted in plants with reduced ABP1, which exhibited increased internalized PIN1. Thus, auxin acting through ABP1 promotes PIN1 accumulation at the lobe tips and stimulates ROP2 and ROP6 signaling in adjacent cells to promote the appropriate cytoskeletal reorganizations necessary for interdigitation.

In plant roots, the polarized distribution of PIN1 creates a gradient of auxin activity, which is necessary for root elongation and initiation. Robert et al. found that, in root, auxin rapidly inhibited the internalization of green fluorescent protein (GFP)–tagged PIN1 that occurred in response to brefeldin A (BFA) and that this process was rapid and did not involve TIR1 or transcription or translation. Knockdown of ABP1 resulted in reduced PIN1 internalization, and roots exhibited a general reduction in endocytosis, based on monitoring the trafficking of an endocytic tracer. Introduction of a gain-of-function mutant of ABP1, lacking the ER retention signal and thus causing increased abundance of ABP1 at the cell surface, produced auxin-related phenotypes and increased PIN1 internalization in response to BFA. The increased PIN1 internalization in the ABP1 gain-of-function roots was blocked by the addition of a synthetic auxin, suggesting that auxin inhibits ABP1’s activity in promoting internalization. Natural or synthetic auxins inhibited transferrin internalization in protoplasts transfected with the human transferrin receptor and, in root cells, decreased the association of a GFP-tagged clathrin light chain with the plasma membrane, indicating that auxin inhibited clathrin-mediated endocytosis. In transfected cells, inhibitors of clathrin function blocked ABP1-mediated PIN1 internalization and, in plants in which ABP1 activity was reduced, less clathrin was associated with the plasma membrane. Thus, the evidence suggests that auxin acts through ABP1 at the cell surface to stabilize PIN1 at the plasma membrane by inhibiting clathrin-mediated endocytosis.

Together these two studies reveal functions for the auxin receptor ABP1 and provide mechanisms by which the rapid effects of auxin are mediated to regulate polarity and morphogenesis.

T. Xu, M. Wen, S. Nagawa, Y. Fu, J.-G. Chen, M.-J. Wu, C. Perrot-Rechenmann, J. Friml, A. M. Jones, Z. Yang, Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143, 99–110 (2010). [PubMed]

S. Robert, J. Kleine-Vehn, E. Barbez, M. Sauer, T. Paciorek, P. Baster, S. Vanneste, J. Zhang, S. Simon, M. Čovanová, K. Hayashi, P. Dhonukshe, Z. Yang, S. Y. Bednarek, A. M. Jones, C. Luschnig, F. Aniento, E. Zažímalová, J. Friml, ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143, 111–121 (2010). [PubMed]

S. Pietra, M. Grebe, Auxin paves the way for planar morphogenesis. Cell 143, 29–31 (2010). [PubMed]

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