Auxin perception--structural insights

Abstract

The identity of the auxin receptor(s) and the mechanism of auxin perception has been a subject of intense interest since the discovery of auxin almost a century ago. The development of genetic approaches to the study of plant hormone signaling led to the discovery that auxin acts by promoting degradation of transcriptional repressors called Aux/IAA proteins. This process requires a ubiquitin protein ligase (E3) called SCF(TIR1) and related SCF complexes. Surprisingly, auxin works by directly binding to TIR1, the F-box protein subunit of this SCF. Structural studies demonstrate that auxin acts like a "molecular glue," to stabilize the interaction between TIR1 and the Aux/IAA substrate. These exciting results solve an old problem in plant biology and reveal new mechanisms for E3 regulation and hormone perception.

Figure 1.

Model for auxin signaling. TIR1 is an F-box protein that binds auxin directly and targets auxin/indole acetic acid proteins (Aux/IAAs) for degradation. (A) At low auxin levels, ARF-dependent transcription of auxin response genes is repressed by the Aux/IAAs and the corepressor TPL. These proteins interact through the xxLXLXLxx (EAR motif) of Aux/IAAs and the carboxy-terminal to lissencephaly homology (CTLH) domain of TPL (B) Higher auxin levels result in the formation of the TIR1-Aux/IAA complex leading to Aux/IAA ubiquitination and subsequent degradation. Adapted from Santner et al. 2009.

Figure 2.

Regulation of ASK1-TIR1-Aux/IAA auxin receptor complexes. Auxin acts like “molecular glue” to stabilize the interaction between TIR1 (gray) and domain II of the Aux/IAA (orange). Gain-of-function mutations in domain II of several Aux/IAAs result in reduced binding to TIR1 and stabilization of the Aux/IAA. A variety of loss-of-function mutations in TIR1/AFB proteins have been characterized (T-DNA insertions (arrows) and point mutations (asterisks)) that result in an auxin-resistant phenotype. Indole-3-acetic acid (IAA) is the major natural auxin but other auxinic compounds, including α-Naphthalene acetic acid (1-NAA), 2,4-Dichlorophenoxyacetic acid (2,4-D) and 4-Amino-3,5,6-trichloropicolinic acid (picloram) promote auxin specific responses in the root or shoot of the plant. These compounds and other natural auxins may bind to the promiscuous auxin binding pocket of TIR1 with different affinities.

Figure 3.

(A) Overall view of the TIR1 surface pocket. (B) A slab view of the TIR1–auxin–IAA7 peptide complex, showing that IAA7 peptide covers the auxin binding site from the top. The molecular surface of TIR1 is shown in grey mesh. Adapted from (Tan et al. 2007).

Figure 4.

InsP6 binds with a few key residues that form the binding site of auxin. The auxin molecule (IAA) is shown as a green stick model, together with its electron density map. The TIR1 residues surrounding auxin and right underneath the auxin-binding site are shown as a yellow stick model. A central water molecule as part of the pocket floor is shown as a red sphere. The hydrogen-bond and salt-bridge network connecting auxin and InsP6 are indicated by orange dashed lines. Adapted from (Tan et al. 2007).