SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development

Abstract

Auxin regulates a vast array of growth and developmental processes throughout the life cycle of plants. Auxin responses are highly context dependent and can involve changes in cell division, cell expansion, and cell fate. The complexity of the auxin response is illustrated by the recent finding that the auxin-responsive gene set differs significantly between different cell types in the root. Auxin regulation of transcription involves a core pathway consisting of the TIR1/AFB F-box proteins, the Aux/IAA transcriptional repressors, and the ARF transcription factors. Auxin is perceived by a transient coreceptor complex consisting of a TIR1/AFB protein and an Aux/IAA protein. Auxin binding to the coreceptor results in degradation of the Aux/IAAs and derepression of ARF-based transcription. Although the basic outlines of this pathway are now well established, it remains unclear how specificity of the pathway is conferred. However, recent results, focusing on the ways that these three families of proteins interact, are starting to provide important clues.

Figure 1.

SCF^TIR1/AFB-Based Auxin Perception and Response. (A) Domain structure of the Aux/IAA and ARF proteins. EAR is the ETHYLENE RESPONSE FACTOR-associated amphiphilic repression motif that interacts with the TPL corepressor. The dII domain facilitates interaction with the TIR1/AFB protein in response to auxin. The PB1 domain has both positive and negative electrostatic interfaces for directional protein interaction. DBD is the B3 DNA binding domain, and MR is the middle region that determines the activity of the ARF. (B) Activating ARFs can form dimers through their DBDs and bind inverted repeat AuxREs (Boer et al., 2014). At low auxin levels, the Aux/IAA proteins form multimers with ARFs and recruit TPL to the chromatin. Note that most AuxREs are not found as inverted repeats in plant genomes, indicating that ARFs bind to DNA in configurations other than shown here. (C) High levels of auxin promote ubiquitination and degradation of Aux/IAAs through SCF^TIR1/AFB and the proteasome. ARFs are free to activate transcription of target genes. The site of Aux/IAA ubiquitination is arbitrary. The actual sites are unknown. Auxin is represented by the red oval.

Figure 2.

Structure of TIR1-ASK1 in a Complex with IAA and the Degron Peptide from IAA7. TIR1-ASK1 structure as described by Tan et al. (2007). ASK1 (green) interacts with TIR1 (red) through the F-box domain. IAA (blue) is present in the auxin binding pocket and acts to stabilize the interaction between TIR1 and the degron peptide (pale cyan). A single InsP6 molecule (pale orange) is bound to TIR1 beneath the auxin binding pocket.

Figure 3.

Different TIR1/AFB-AUX/1AA-ARF Modules May Regulate Different Developmental Processes. Six TIR1/AFB can interact with the 23 different Aux/IAAs containing the dII to form numerous coreceptor complexes. Each of the Aux/IAA may interact with up to 19 ARFs containing Domains III/IV to regulate distinct sets of target genes that control different physiological processes in the plant.

Figure 4.

Regulation of the TIR1/AFB Pathway. ARF-mediated regulation of the Aux/IAA genes constitutes a robust negative feedback loop. Other pathways may regulate transcription of auxin response genes in both a positive and negative manner. For example, the cytokinin responsive transcription factor ARR1 promotes transcription of IAA3 in the root, resulting in downregulation of the ARF target PIN1. This results in a change in auxin distribution that affects cell differentiation (Dello Ioio et al., 2008). In addition, other pathways may act directly on the ARFs. For example, the BIN2 kinase regulates the interaction between ARF7 and Aux/IAA by directly phosphorylating the ARF (Cho et al., 2014).