Save your TIRs - more to auxin than meets the eye

Abstract

Auxin has long been known as an important regulator of plant growth and development. Classical studies in auxin biology have uncovered a 'canonical' transcriptional auxin-signalling pathway involving the TRANSPORT INHIBITOR RESPONSE1/AUXIN SIGNALING F-BOX (TIR1/AFB) receptors. TIR1/AFB perception of auxin triggers the degradation of repressors and the derepression of auxin-responsive genes. Nevertheless, the canonical pathway cannot account for all aspects of auxin biology, such as physiological responses that are too rapid for transcriptional regulation. This Tansley insight will explore several 'non-canonical' pathways that have been described in recent years mediating fast auxin responses. We focus on the interplay between a nontranscriptional branch of TIR1/AFB signalling and a TRANSMEMBRANE KINASE1 (TMK1)-mediated pathway in root acid growth. Other developmental aspects involving the TMKs and their association with the controversial AUXIN-BINDING PROTEIN 1 (ABP1) will be discussed. Finally, we provide an updated overview of the ETTIN (ETT)-mediated pathway in contexts outside of gynoecium development.

Keywords: acid growth; auxin; gene expression control; nontranscriptional auxin effects; signal transduction.

Fig. 1

Auxin signalling pathways in plants. (a) The ‘canonical’ pathway involves the perception of auxin by the TIR1/AFB‐SCF complex which facilitates the degradation of AUX/IAA repressors by the 26 S proteasome, freeing the Class A ARFs to mediate gene expression (Dharmasiri et al., ; Kepinski & Leyser, 2005). In acid growth, the TIR1/AFB‐mediated pathway induces the expression of SMALL AUXIN UP RNA19 (SAUR19) which inhibits the PP2C‐D protein phosphatases, allowing H⁺ efflux through H⁺ ATPases and cell wall acidification (Spartz et al., ; Ren et al., 2018). The cytosolic AFB1 has also been shown to mediate apoplast alkalinisation but the mechanism is yet to be elucidated (Prigge et al., ; Li et al., ; Serre et al., 2021). Apoplast acidification is also induced by the phosphorylation of H⁺ ATPases by the TMKs (Li et al., ; Lin et al., 2021). ABP1 is secreted from the endoplasmic reticulum (ER) to the plasma membrane (PM) to function as the auxin receptor in complex with the TMKs (Friml et al., 2022). The TMK‐ABP1 complex activate ROPs and promotes the internalisation of MAKR2, an antagonist of ROP signalling (Xu et al., ; Marques‐Bueno et al., 2021). Other TMK‐ABP1 activated pathways include the MAPK pathway through the MKK4/5‐MPK3/6 module and abscisic acid signalling through ABA INSENSITIVE 1 and 2 (ABI1/2) (Huang et al., ; Yang et al., 2021). (b) Auxin perception also promotes DA1‐dependent cleavage of the TMK C‐terminus domain, which enters the nucleus and phosphorylates IAA32/34 to prevent their degradation (Cao et al., ; Gu et al., 2022). IAA32/34 then promotes growth repression on the concave side of the apical hook through their antagonism of ARF activity. (c) ETT interacts with TPL and other transcription factors (TFs) through its ES domain in an auxin‐sensitive manner (Simonini et al., , ; Kuhn et al., 2020). Direct binding of auxin to ETT disrupts these protein–protein interactions and possibly promotes interactions with partners associated with the activation of gene expression. Auxin is shown as Indole‐3‐Acetic Acid.