Protein degradation in auxin response

Abstract

The signaling molecule auxin sits at the nexus of plant biology where it coordinates essentially all growth and developmental processes. Auxin molecules are transported throughout plant tissues and are capable of evoking highly specific physiological responses by inducing various molecular pathways. In many of these pathways, proteolysis plays a crucial role for correct physiological responses. This review provides a chronology of the discovery and characterization of the auxin receptor, which is a fascinating example of separate research trajectories ultimately converging on the discovery of a core auxin signaling hub that relies on degradation of a family of transcriptional inhibitor proteins-the Aux/IAAs. Beyond describing the "classical" proteolysis-driven auxin response system, we explore more recent examples of the interconnection of proteolytic systems, which target a range of other auxin signaling proteins, and auxin response. By highlighting these emerging concepts, we provide potential future directions to further investigate the role of protein degradation within the framework of auxin response.

Figure 1.

Phenotypes of auxin-insensitive mutants. A) Schematic illustration of auxin-controlled plant developmental processes, which were used as read-outs in various genetic screens. B–G) Examples of mutants identified in genetic screens. The illustrations are based on (B) Estelle and Somerville (1987), (C) Wilson et al. (1990), (D) Leyser et al. (1996), (E) Ruegger et al. (1997), (F) Tian and Reed (1999), and (G) Hobbie et al. (2000).

Figure 2.

Overview of the UPS, domain architecture of auxin response proteins, and the canonical nuclear auxin pathway. A) Schematic overview of the enzymatic cascade leading to ubiquitylation of a substrate protein, resulting in its recognition and subsequent degradation by the 26S proteasome. Ub, ubiquitin. B) General domain composition of canonical TIR1/AFB, ARF, and Aux/IAA proteins. This figure is not an alignment, and the protein and domain sizes are not to scale. AC, Adenylate Cyclase; DBD, DNA-binding domain; LRR, leucine-rich repeat; MR, middle region; PB1, Phox-Bem1. C–E) Model of auxin signaling through auxin-induced and SCF^TIR1/AFB-mediated degradation of the Aux/IAA repressors. When auxin levels are low (C), ARFs are repressed by Aux/IAAs; however, upon removal of the Aux/IAA repressors by auxin-triggered degradation (D), ARF proteins are able to induce transcription of auxin-responsive genes, which includes Aux/IAA encoding genes. E) Detailed overview of the composition of the SCF^TIR1/AFB complex and hypothesized (dashed lines) as well as known (solid lines) regulatory mechanisms that tune SCF^TIR1/AFB activity.

Figure 3.

Regulation of ARF activity and accumulation via proteolysis and PTRE1-mediated tuning of proteasomal functioning. Factors influencing degradation are color coded as indicated in the legend. Abbreviations preceding protein names indicate that these proteins are from the following plant species: At, Arabidopsis thaliana; Md, Malus domesticus; Mp, Marchantia polymorpha; Pp, Physcomitrium patens; Zm, Zea mays.