Auxin and cytokinin regulate each other's levels via a metabolic feedback loop

Abstract

The hormones auxin and cytokinin are key regulators of plant growth and development. As they are active at minute concentrations and regulate dynamic processes, cell and tissue levels of the hormones are finely controlled developmentally, diurnally, and in response to environmental variables. This fine control, along with a regulation of the capacity to respond ensures that the appropriate type, duration and intensity of responses are elicited. We have recently discovered that cytokinin and auxin regulate the synthesis of each other, demonstrating a mechanism for mutual feed back and feed forward control of auxin and cytokinin levels. This regulatory loop could be important for many developmental processes in plants, i.e., in fine-tuning plant hormone levels in the developing meristems of the root and shoot apex. These findings could also give a molecular explanation for earlier observations of auxin and cytokinin effects on cell cultures,1 where specific auxin and cytokinin ratios have been used to trigger different morphological events.

Figure 1

Subcellular localization of auxin (IAA) and cytokinin (CK) metabolism, transport and signaling in Arabidopsis. IAA and CK biosynthesis. Biosynthesis of aromatic amino acids, including tryptophan, is located to plastids, while the final steps in IAA biosynthesis is believed to take place in the cytoplasm. CKs are biosynthesized in plastids and then transported to the cytoplasm. IAA downregulates CK biosynthesis, while CK on the other hand induces IAA biosynthesis. IAA and CK transport and signaling. IAA binds to the nuclear IAA receptors (TIR1/AFB's) and to Aux/IAA proteins that are subsequently degraded by the 26S proteasome complex. The AuxIAA proteins interact with ARF transcription factors to regulate gene transcription. The other putative IAA receptor (ABP1) is located both to the plasma membrane and to the endoplasmic reticulum (ER), where a part of the intracellular IAA pool is located as IAA amino acid conjugates. The CK receptors (AHKs) are also located to the plasma membrane, while AHP and ARR proteins transmit the CK signal to the nucleus. Both IAA and CK are actively transported across the plasma membrane. ABP1, auxin-binding protein 1; AFB, auxin F box; AHK, Arabidopsis histidine kinase; AHP, Arabidopsis histidine phosphotransfer proteins; ARF, auxin response factor; ARR, Arabidopsis response regulators; Aux/IAA, auxin/indole-3-acetic acid; CK-M,D,T-P, cytokinin-mono,di,tri-phosphates; CK-R, cytokinin ribosides; DMAPP, dimethylallyl diphosphate; HMBDP, hydroxymethylbutenyl diphosphate; MEP, methylerythritolphosphate; Phe, phenylalanine; TIR1, transport inhibitor resistant 1; Trp, tryptophan; Tyr, tyrosine.

Figure 2

Genes involved in auxin metabolism differentially expressed in response to altered cytokinin levels and/or responsiveness in Arabidopsis. The Genevestigator Microarray Database was used to identify auxin metabolic genes that were affected by experimental conditions where cytokinin levels and/or responsiveness were manipulated. AT5G43890 (YUCCA5) and AT1G04180 (YUCCA9) Flavin monooxygenases; AT1G23320 (TAR1) Pyridoxal phosphate-dependent aminotransferase; AT1G23160, (GH3-7), AT1G48670 (GH3-18), AT1G48690 (GH3-20), AT2G23170 (GH3-3) and AT5G51470 (GH3-8) IAA amino acid conjugation GH3 family proteins. GV Exp. Key, Genevestigator experiment identification number.

Figure 3

Genes involved in cytokinin metabolism differentially expressed in response to altered auxin levels and/or responsiveness in Arabidopsis. The Genevestigator Microarray Database was used to identify cytokinin metabolic genes that were affected by experimental conditions where auxin levels and/or responsiveness were manipulated. At5g26140 (LOG9) Cytokinin nucleoside 5′-monophosphate phosphoribohydrolase; At2g41510 (CKX1) and At3g63440 (CKX6) Cytokinin oxidase/dehydrogenases; At2g36750 (UGT73C1) Zeatin-O-glucosyltransferase. GV Exp. Key, Genevestigator experiment identification number.