Auxin Metabolism in Plants

Abstract

The major natural auxin in plants, indole-3-acetic acid (IAA), orchestrates a plethora of developmental responses that largely depend on the formation of auxin concentration gradients within plant tissues. Together with inter- and intracellular transport, IAA metabolism-which comprises biosynthesis, conjugation, and degradation-modulates auxin gradients and is therefore critical for plant growth. It is now very well established that IAA is mainly produced from Trp and that the IPyA pathway is a major and universally conserved biosynthetic route in plants, while other redundant pathways operate in parallel. Recent findings have shown that metabolic inactivation of IAA is also redundantly performed by oxidation and conjugation processes. An exquisite spatiotemporal expression of the genes for auxin synthesis and inactivation have been shown to drive several plant developmental processes. Moreover, a group of transcription factors and epigenetic regulators controlling the expression of auxin metabolic genes have been identified in past years, which are illuminating the road to understanding the molecular mechanisms behind the coordinated responses of local auxin metabolism to specific cues. Besides transcriptional regulation, subcellular compartmentalization of the IAA metabolism and posttranslational modifications of the metabolic enzymes are emerging as important contributors to IAA homeostasis. In this review, we summarize the current knowledge on (1) the pathways for IAA biosynthesis and inactivation in plants, (2) the influence of spatiotemporally regulated IAA metabolism on auxin-mediated responses, and (3) the regulatory mechanisms that modulate IAA levels in response to external and internal cues during plant development.

Figure 1.

Main pathways for indole-3-acetic acid (IAA) metabolism in plants. Biosynthesis of the IAA precursor l-tryptophan (Trp) takes place in the plastid (green oval). Subsequent IAA biosynthesis, catabolism, and conjugation reactions commonly operate in the cytoplasm. IAA molecules are indicated as red hexagons and IAA-related metabolites are shown in black. Enzymes catalyzing the metabolic reactions are indicated in purple. Major components for IAA biosynthesis and inactivation are indicated with red arrows. Solid arrows indicate pathways in which the enzymes, genes, or intermediates are known, while dashed arrows indicate pathways that are not yet well defined. Brassica-specific metabolites are indicated in orange. Green cylinders indicate intracellular IAA transporters and the attached arrows indicate the IAA movement direction. The blue circle, the gray oval, and the pale orange square indicate peroxisome, nucleus, and vacuole, respectively. Endoplasmic reticulum (ER) is indicated by the dark yellow structure attached to the nucleus. Organelles are not drawn to scale. (AMI1) AMIDASE-LIKE PROTEIN 1, (ANT) anthranilate, (ASA1) ANTHRANILATE SYNTHASE α SUBUNIT 1, (ASB1) ANTHRANILATE SYNTHASE β SUBUNIT 1, (CYP79B2/B3) CYTOCHROME P450, family 79, subfamily B, polypeptides 2 and 3, (DAO) DIOXYGENASE FOR AUXIN OXIDATION, (GH3) GRETCHEN HAGEN3, (IAA-glc) IAA-glucose, (IAM) indole-3-acetamide, (IAMT1) indole-3-acetate O-methyltransferase 1, (IAN) indole-3-acetonitrile, (IAOx) indole-3-acetaldoxime, (IBA) indole-3-butyric acid, (IAR3) IAA-ALANINE RESISTANT3, (ILLs) ILR1-LIKE, (ILR1) IAA-LEUCINE RESISTANT1, (IPyA) indole-3-pyruvic acid, (meIAA) methylindole-3-acetic acid, (MES17) METHYLESTERASE 17, (oxIAA) 2-oxindole-3-acetic acid, (Phe) phenylalanine, (PILS) PIN-likes, (PIN) PIN-FORMED, (TAA1) TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1, (TAR) TRYPTOPHAN AMINOTRANSFERASE-RELATED PROTEIN, (Trp-AT) TRYPTOPHAN AMINOTRANSFERASE, (UGTs) URIDINE-DIPHOSPHATE GLYCOSYLTRANSFERASE, (VAS1) REVERSAL OF SAV3 PHENOTYPE 1, (WAT1) WALLS ARE THIN1, (YUC) YUCCA flavin-containing monooxygenases.

Figure 2.

Relative expression level of the main genes for auxin metabolism in different developmental stages, organs, and tissues from Arabidopsis. Data was retrieved from Genevestigator (genevestigator.com; Hruz et al. 2008) using datasets from (A) RNA-seq experiments, and (B) Affymetrix Arabidopsis ATH1 Genome Array. Results are expressed in percentage of expression potential (the maximum expression a gene reaches across all experiments). GH3.2 and GH3.4 share array probes in the results shown in B. AGI codes: YUC1 (At4G32540), YUC2 (At4G13260), YUC3 (At1G04610), YUC4 (At5G11320), YUC5 (At5G43890), YUC6 (At5G25620), YUC7 (At2G33230), YUC8 (At4G28720), YUC9 (At1G04180), YUC10 (At1G48910), YUC11 (At1G21430), TAA1 (At1G70560), TAR1 (At1G23320), TAR2 (At4G24670), CYP79B2 (At4G39950), CYP79B3 (At2G22330), DAO1 (At1G14130), DAO2 (At1G14120), GH3.1 (At2G14960), GH3.2 (At4G37390), GH3.3 (At2G23170), GH3.4 (At1G59500), GH3.5 (At4G27260), GH3.6 (At5G54510), GH3.9 (At2G47750), and GH3.17 (At1G28130).