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  • Review Article
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Auxin in action: signalling, transport and the control of plant growth and development

Key Points

  • Auxins form a class of small indolic plant growth regulators that was initially identified as the motile stimulus that causes plants to bend towards the light. Auxins have profound effects on many aspects of plant development — they affect cell division, elongation and differentiation — but their modes of action are complicated.

  • The most well-characterized auxin signalling events are mediated by auxin-responsive elements (AREs) in the promoters of auxin primary-response genes. ARE-mediated transcription is initiated through the action of auxin response factors (ARFs) to AREs. ARE-mediated transcription is inhibited by the binding of Aux/IAA proteins to ARFs.

  • Auxin functions by stimulating the ubiquitin-mediated proteolysis of Aux/IAAs. Aux/IAAs are marked for proteolysis by the action of the SCFTIR1 E3 ubiquitin ligase. The association between TIR1 and Aux/IAAs is enhanced by the direct binding of auxin to TIR1. TIR1 is one of a family of four similar F-box-domain-containing proteins, which all mediate an auxin response and represent the first confirmed auxin receptors.

  • These F-box proteins probably do not represent the only mechanism of auxin perception. Other auxin-binding proteins such as AUXIN-BINDING PROTEIN-1 (ABP1) also confer auxin sensitivity and might also represent auxin receptors. These other pathways are likely to be extremely rapid, and certain auxin responses are seen almost instantaneously.

  • The phytohormone that best fits the classical definition of a hormone is auxin as it is transported between its site of synthesis and site of action. This transport is mediated by several transporters and signalling events that are separate from ARE-mediated gene transcription.

  • Although not traditionally considered together, it is becoming increasingly clear that auxin signalling and auxin transport are linked. The involvement of an increasing number of proteins that were previously considered as components of signalling networks that are also involved in auxin transport is currently opening a new chapter in auxin biology.

Abstract

Hormones have been at the centre of plant physiology research for more than a century. Research into plant hormones (phytohormones) has at times been considered as a rather vague subject, but the systematic application of genetic and molecular techniques has led to key insights that have revitalized the field. In this review, we will focus on the plant hormone auxin and its action. We will highlight recent mutagenesis and molecular studies, which have delineated the pathways of auxin transport, perception and signal transduction, and which together define the roles of auxin in controlling growth and patterning.

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Figure 1: SCFTIR1-mediated auxin signalling.
Figure 2: The 'auxin code' as determined by hierarchical cluster analysis of the expression patterns of ARF genes.
Figure 3: The 'auxin code' as determined by hierarchical cluster analysis of the expression patterns of Aux/IAA genes.
Figure 4: The developmental feedback loop of auxin signalling and auxin transport in roots.
Figure 5: The developmental processes that are controlled by auxin flux.

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Acknowledgements

We thank W. Hartung, R. Hertel, S. Kepinski, J. McWilliams and P. Schopfer for critical reading of the manuscript. Our work was supported by the Deutsche Forschungsgemeinschaft (DFG), the Bundesministerium für Bildung und Forschung, Fonds der chemischen Industrie, the European Union and the Landesstiftung Baden-Württemberg GmbH. K.P. is particularly grateful for having had the opportunity to contribute to the DFG network's Molecular Mechanisms of Phytohormone Action.

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FURTHER INFORMATION

Developmental Affymetrix Gene Expression Atlas

DATABASES

TAIR

http://www.arabidopsis.org

TIR1

RUB1

CAND1

ARF4

ARF6

ARF8

ARF11

IAA6

IAA19

IAA9

IAA32

IAA34

ARF1

ARF2

ARF19

ABP1

AUX1

PIN1

PIN7

ADP RIBOSYLATION FACTOR-1

RCN1

Glossary

Regulon

A collection of separate genes, the expression of which is controlled as a unit by a specific signalling compound or factor.

Degron

A protein element, usually a sequence motif, that targets the protein for proteolytic degradation.

SCFTIR1 E3 ubiquitin ligase

A multisubunit ubiquitin ligase that consists of SKP1, CUL1 and an F-box protein (TIR1 in this case) that confers substrate specificity, as well as a RING protein that is also known as HRT1, RBX1 or ROC1.

F-box protein

A component of the machinery for the ubiquitin-dependent degradation of proteins. F-box proteins recognize specific substrates and, with the help of other subunits of the E3 ubiquitin ligase, deliver them to the E2 ubiquitin-conjugating enzyme.

26S proteasome

A protein complex that is responsible for degrading intracellular proteins that have been tagged for destruction by the addition of ubiquitin.

COP9 signalosome

An eight-subunit protein complex that regulates protein ubiquitylation and turnover in a range of developmental and physiological contexts. Extensively characterized in plants but fundamental to all eukaryotes, this complex post-translationally modifies the cullin subunit of E3-ubiquitin ligases by cleaving off the covalently coupled peptide, Nedd8/RUB1.

T-DNA mutation

A mutation that is the result of the integration of DNA from Agrobacterium tumefaciens into plant genomes. The insertion is random and might therefore disrupt genes, causing a mutation at the insertion point.

Cupin proteins

A diverse family of plant proteins, all of which contain at least one double-stranded α-helix or jelly-roll structural motif. This motif is also present in all structurally characterized 2-oxoglutarate-dependent oxygenases, including the hypoxia-inducible factor (HIF) hydroxylases, and is characteristic of the Jumonji transcription factors.

Root cap

The layers of protective cells that cover the tip of the growing root.

Expansins

A class of proteins that are able to catalyse the loosening of the cell wall, enabling cell expansion.

Extensins

Proline-rich proteins that connect the cell wall and the plasma membrane.

Meristem

A zone (for example, the apex of the shoot) that contains undifferentiated cells that continue to divide, providing cells for further growth and differentiation.

Phloem

Vascular tissue that carries organic nutrients as well as information molecules such as hormones throughout the plant.

Xylem

Vascular tissue that delivers water and mineral nutrients, which are taken up by the root system, to aerial organs. It also provides mechanical support.

Agravitropic

When a plant is unable to either perceive or respond to gravity. Typically, the roots of agravitropic plants grow in all directions.

Guanine nucleotide exchange factor

A protein that facilitates the exchange of GDP (guanine diphosphate) for GTP (guanine triphosphate) in the nucleotide-binding pocket of a GTP-binding protein.

GTPase-activating protein

(GAP). A protein that stimulates the intrinsic ability of a GTPase to hydrolyse GTP to GDP. Therefore, GAPs negatively regulate GTPases by converting them from active (GTP-bound) to inactive (GDP-bound).

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Teale, W., Paponov, I. & Palme, K. Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7, 847–859 (2006). https://doi.org/10.1038/nrm2020

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