Auxin: regulation, action, and interaction

Abstract

Background: The phytohormone auxin is critical for plant growth and orchestrates many developmental processes.

Scope: This review considers the complex array of mechanisms plants use to control auxin levels, the movement of auxin through the plant, the emerging view of auxin-signalling mechanisms, and several interactions between auxin and other phytohormones. Though many natural and synthetic compounds exhibit auxin-like activity in bioassays, indole-3-acetic acid (IAA) is recognized as the key auxin in most plants. IAA is synthesized both from tryptophan (Trp) using Trp-dependent pathways and from an indolic Trp precursor via Trp-independent pathways; none of these pathways is fully elucidated. Plants can also obtain IAA by beta-oxidation of indole-3-butyric acid (IBA), a second endogenous auxin, or by hydrolysing IAA conjugates, in which IAA is linked to amino acids, sugars or peptides. To permanently inactivate IAA, plants can employ conjugation and direct oxidation. Consistent with its definition as a hormone, IAA can be transported the length of the plant from the shoot to the root; this transport is necessary for normal development, and more localized transport is needed for tropic responses. Auxin signalling is mediated, at least in large part, by an SCFTIR1 E3 ubiquitin ligase complex that accelerates Aux/IAA repressor degradation in response to IAA, thereby altering gene expression. Two classes of auxin-induced genes encode negatively acting products (the Aux/IAA transcriptional repressors and GH3 family of IAA conjugating enzymes), suggesting that timely termination of the auxin signal is crucial. Auxin interaction with other hormone signals adds further challenges to understanding auxin response.

Conclusions: Nearly six decades after the structural elucidation of IAA, many aspects of auxin metabolism, transport and signalling are well established; however, more than a few fundamental questions and innumerable details remain unresolved.

Fig. 1.

Auxins promote lateral root formation and inhibit root elongation. Arabidopsis thaliana Col-0 ecotype plants were grown on unsupplemented medium (Haughn and Somerville, 1986) for 6 d, then transferred to unsupplemented medium (A) or medium supplemented with 10 nm IAA (B), 100 nM 2,4-D (C), 100 nM NAA (D) or 10 μM IBA (E) and grown for 6 additional days. (F) Plants were grown on various concentrations of natural and synthetic auxins for 8 d. Points represent means ± standard error, n ≥ 8. All plants were grown at 22 °C under yellow light.

Fig. 2.

Potential pathways of IAA biosynthesis in arabidopsis. De novo IAA biosynthetic pathways initiate from Trp or Trp precursors. Compounds quantified in arabidopsis are in blue, enzymes for which the arabidopsis genes are identified are in red, and arabidopsis mutants are in lower-case italics. Suggested conversions for which genes are not identified are indicated with question marks. Trp biosynthesis and the P450-catalysed conversion of Trp to IAOx are chloroplastic, whereas many Trp-dependent IAA biosynthetic enzymes are apparently cytoplasmic. See Table 1 for references.

Fig. 3.

Potential pathways of IAA metabolism. Compounds quantified in arabidopsis are in blue, enzymes for which the arabidopsis genes are cloned are in red, and arabidopsis mutants are in lower-case italics. Suggested conversions for which plant genes are not identified are indicated with question marks. A family of amidohydrolases that apparently resides in the ER lumen can release IAA from IAA conjugates. ILR1 has specificity for IAA–Leu (Bartel and Fink, 1995), whereas IAR3 prefers IAA–Ala (Davies et al., 1999). Maize (Zm) iaglu and arabidopsis UGT84B1 esterify IAA to glucose (Szerszen et al., 1994; Jackson et al., 2001); the enzymes that form and hydrolyse IAA–peptides have not been identified. IBA is likely to be converted to IAA–CoA in a peroxisomal process that parallels fatty acid β-oxidation to acetyl-CoA (Bartel et al., 2001). IAA can be inactivated by oxidation (oxIAA) or by formation of non-hydrolysable conjugates (IAA–Asp and IAA–Glu). IAA–amino acid conjugates can be formed by members of the GH3/JAR1 family (Staswick et al., 2002, 2005). OxIAA can be conjugated to hexose, and IAA–Asp can be further oxidized (Östin et al., 1998). IAMT1 can methylate IAA (Zubieta et al., 2003), but whether this activates or inactivates IAA is not known. IBA and hydrolysable IAA conjugates are presumably derived from IAA; biosynthesis of these compounds may contribute to IAA inactivation. Formation and hydrolysis of IBA conjugates may also contribute to IAA homeostasis; the wheat (Ta) enzyme TaIAR3 hydrolyses IBA–Ala (Campanella et al., 2004).

Fig. 4.

The SCF^TIR1 relieves Aux/IAA repression of activating ARFs. (A) An activating ARF protein (green) binds an AuxRE promoter element via an N-terminal DNA binding domain (DBD). Under low-auxin conditions, an Aux/IAA repressor (red) binds the activating ARF via heterodimerization between Aux/IAA and ARF domains III and IV. (B) Auxin promotes Aux/IAA domain II-TIR1 association, bringing the Aux/IAA protein to the SCF^TIR1 complex (purple) for ubiquitination (Ub) and subsequent destruction by the 26S proteasome. The activating ARF, with a Gln-rich (Q) middle domain, is then freed to promote auxin-induced gene expression.