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The word in Greek, or to grow in English, of auxin and to the story of its discovery. The effect of
gives us auxin: the name of a small class of molecules auxin was first documented when Charles and Francis
with a powerful ability to induce growth responses in Darwin published The Power of Movement in Plants.
plants. In plants, growth is defined as an irreversible They noted that after the perception of light in one
increase in size, and is achieved by the enlargement of area of a grass coleoptile, an influence is transported
individual cells driven by the uptake of water. Auxin that causes bending towards the light in another 2.
refers to an important group of phytohormones that Forty-five years later, in 1926, this messenger was
has been implicated in most of the quantitative growth separated from plant tissues simply by being allowed to
changes that occur during a plants life cycle. Exactly diffuse into agar blocks, which then retained a growth-
how these changes are brought about is now becoming promoting activity 3,4. Three kinds of auxin were ini-
clear after more than a century of research. We will tially found in plants, of which one was also found in
give an overview of auxin research, and summarize the human urine. Subsequently, the first published reports
remarkable advances that have been made over the past began to appear on the crystallization and structural
few years. This recent progress will be the foundation characteristics of auxin. In those early days, only one of
on which our understanding of the molecular mecha- the structures, that of indole-3-acetic acid (IAA), was
nisms of auxin signal transduction is built, and is begin- correctly identified.
ning to explain how auxin can not only have a direct Auxin is now used as the generic name for a group
influence on cell growth, but also control numerous of important molecules in plants, which can also be
and diverse aspects of plant development. found in humans, animals and microorganisms. IAA
is the predominant auxin in plants (TABLE 1), and is an
Auxin and its effects on plants indispensable phytohormone with a well-documented
Since Julius von Sachs first discussed the concept ability to regulate many aspects of plant development.
of a phytohormone in 1887 (REF. 1), several chemi- Synthetic auxin derivatives are still important herb-
cal growth regulators have been identified in plants. icides; for example, 2,4-dichlorophenoxyacetic acid is
Phytohormones are chemicals that have specific effects one of the worlds most widely used weed-killers. The
on plant growth, and are active at low concentrations. effect of auxin on a growing plant depends on the type
Institut fr Biologie II/Botanik,
Schnzlestrasse 1, Plants use a wide variety of hormones, including ster- of auxin applied and its concentration. Endogenous IAA
79104 Freiburg, Germany. oids and peptides, as well as the five classical classes has been implicated in embryonic and post-embryonic
Correspondence to K.P. of phytohormones (auxins, abscisic acid, cytokinins, development, and tropisms such as movement in rela-
e-mail: klaus.palme@biologie. ethylene and gibberellins), which are all relatively tion to light and gravity. So, auxin influences aspects
uni-freiburg.de
Published online
small molecules. The extent and significance of phy- of cell division, cell elongation and cell differentiation,
20 September 2006 tohormone transport is not well understood for all of although exactly how it is involved in each process (and
doi:10.1038/nrm2020 these classes, but is particularly significant to the action to what extent they are intertwined) is not completely
Table 1 | Properties of three commonly used auxins Aux/IAA genes. The Aux/IAA family forms a group of
early auxin-response genes. The variation in amino-
Properties Natural Synthetic
acid identity among them is high and ranges from
Chemical structure COOH O COOH COOH 10% to 83%. However, even poorly conserved family
Cl members seem to have compensatory functions,
which means that despite their distinct induction
N kinetics, dose responses and expression profiles,
H
Cl obtaining conclusive functional information for the
Aux/IAAs using loss-of-function mutants has been
IAA 2,4-D NAA
difficult18. Each individual Aux/IAA gene might have
Affinity to receptors a set of non-essential functions, but these functions
TIR1 binding (Kd) High Low Middle combine to form an important regulatory programme.
ABP1 binding (Kd) Middle Low High Similar observations have been made in studies of the
yeast oxysterol-binding protein family 19 (discussed
Transport capacity in REF. 18), in which a functional analysis of various
Influx carriers Yes Yes No (by diffusion) sets of different proteins, which individually perform
Efflux carriers Yes No Yes non-essential functions, revealed that they combine
Indole-3-acetic acid (IAA) is considered to be the most important natural auxin, to perform essential regulatory functions. In the
1-naphthaleneacetic acid (NAA) is a horticulturally important auxin, and 2,4-dichlorophenoxy- future, extensive multidimensional expression maps
acetic acid (2,4-D) is a common selective herbicide. and genetic studies of Aux/IAAs and ARFs might be
necessary to tackle this difficult problem.
understood. Its diverse effects in plants might also Aux/IAA genes encode proteins that generally have
extend to animals, as photoactivated auxin seems to have nuclear localization signals and four conserved domains
potential as a cytotoxin in cancer therapy 5,6. (IIV). Domain III has a predicted ribbonhelixhelix
The reason why auxins have attracted so much DNA-binding domain that is found in bacterial tran-
attention for almost a century is not only that they scriptional regulators (although it is not thought that
have the capacity to influence growth, but that they have Aux/IAAs bind DNA in plants) 20. Aux/IAAs have
additional farther-reaching effects on the life cycle of indeed been found in the nucleus. Several Aux/IAA
plants. Recent evidence shows that, through a unique genes are transcribed within minutes of plants or cells
mechanism of perception and elicitation, the physiological being exposed to exogenous auxin or protein synthesis
responses that auxin governs are central to a plants inhibitors. Most strikingly, they were shown to form
structure and functioning. homo- and heterodimers not only with one another, but
also with members of the ARF family.
Auxin-mediated regulation of gene expression
For a long time it was thought that, like steroid receptors ARF genes. ARFs are transcription factors that contain
in animals, dedicated plant-receptor proteins initiate an amino-terminal B3-like DNA-binding domain, which
the transduction of the auxin signal into numerous binds to an auxin-responsive element (ARE; TGTCTC)
physiological responses. Finally, and after decades of in the promoter of auxin-response genes in an auxin-
research, two separate approaches yielded valuable independent manner21,22. The carboxy-terminal domain
information on the nature of how auxin functions. The is similar to the carboxy-terminal region of the Aux/IAA
first approach was based on observations made more proteins and is likely to promote direct interaction between
than 20 years ago, which showed that auxin alters gene both groups of proteins while bound to the ARE23.
expression after only minutes in a selective and dramatic This interaction blocks ARE-mediated transcription20.
Regulon way 710. The second approach was based on the analysis
A collection of separate genes,
of a series of auxin-resistant mutations. Many of these Auxin-mediated gene regulation. Aux/IAA proteins
the expression of which is
controlled as a unit by a different mutant plants lacked functional components of have been shown to function as negative regulators
specific signalling compound or the ubiquitin-mediated proteolytic pathway, indicating of gene expression 20. Semi-dominant alleles (that
factor. that selective protein degradation is a crucial regulator show intermediate phenotypes) with mutations in
of many aspects of the auxin response1113. the GWPPV motif of the conserved domain II cause
Degron
A protein element, usually a
Whereas the levels of some mRNAs decrease many severe auxin-related phenotypes as they affect the
sequence motif, that targets fold in response to auxin, those of other mRNAs increase stability of these repressors24. In some cases, this can
the protein for proteolytic many fold (for example, Aux/IAA, GRETCHENHAGEN-3 result in contradictory regulatory phenomena in which
degradation. (GH3) and members of the small auxin up RNA (SAUR) the sensitivity of the mutant to exogenously applied
gene family)10,14,15. Furthermore, auxin activates regulons auxin is reduced, whereas the auxin-related pheno-
SCFTIR1 E3 ubiquitin ligase
A multisubunit ubiquitin ligase directly and rapidly. The genes that are activated or type is simultaneously enhanced25. The core region of
that consists of SKP1, CUL1 repressed during this process are ultimately respon- domain II was mapped to a 13-amino-acid sequence,
and an F-box protein (TIR1 in sible for the many physiological effects of auxin. The known as the degron: a motif that is sufficient to confer
this case) that confers complex auxin responses are mediated by two groups instability, even when fused to other proteins such as
substrate specificity, as well as
a RING protein that is also
of well-studied genes: the Aux/IAA genes, which consist of -glucuronidase or luciferase2628. Proteins that contain
known as HRT1, RBX1 or 29 members, and the auxin response factor (ARF) genes this degron sequence are an efficient target of the SCFTIR1
ROC1. with 23 members, in Arabidopsis thaliana1618. E3 ubiquitin ligase complex29.
ARFs, Aux/IAAs and the auxin response showed that different ARF proteins as well as different
With the potential involvement of many F-box proteins, ARFARF and ARFAux/IAA combinations function in
proteasome-mediated auxin signalling is unexpectedly particular developmental windows to form a regulatory
complicated. This auxin-receptor-binding signal is then code that programmes the expression of not only auxin-
relayed to the subsequent phase of auxin-responsive sensitive genes but also genes that are regulated by auxin
gene expression, which is anticipated to be an intricately in a more indirect manner 17,18. Further global expression
intertwined set of processes. The effects of auxin are studies with multiple higher-order (for example, double
thought to depend on its concentration, with high and or triple) mutants are likely to provide detailed expres-
low doses eliciting different responses. A framework for sion maps of distinct tissues and cells that might point
understanding how auxin can have such different roles to the regulatory targets of these genes.
in plant development is now in place. At basal auxin Auxin concentration also influences cell patterning,
levels, Aux/IAAs are relatively stable, homodimerize as the highest levels of auxin signalling proteins corre-
and heterodimerize with ARFs that can bind to AREs spond to the sites of new lateral roots and leaves, which
in the promoters of auxin-responsive genes20,54. The has been shown to be functionally significant61,62. In the
ARF-bound Aux/IAA proteins block transcription from A. thaliana root tip, the relationship between the forma-
auxin-responsive promoters by controlling the amount tion and structuring of new organs has been studied in
of free ARF transcription factors to the promoters23. detail. Here, the Aux/IAAARF signalling pathway is
An increase in auxin levels causes the proteasome- necessary for the expression of transcription factors that
mediated degradation of Aux/IAAs, which in turn determine the correct differentiation of the various cell
allows for a gradually increasing number of functionally types that are present in roots. PLETHORA proteins, for
active ARF proteins and the transcriptional activation of example, provide positional information that is neces-
auxin regulons. ARFs can be grouped into three subsets sary for proper root development and depend on auxin
and vary between 57 and 129 kDa in size. The amino- (through ARF5 and ARF7) for their expression63.
acid content in the variable middle region determines
whether a particular ARF functions as a repressor or Alternative signalling pathways
an activator17,55. Glutamine-rich ARFs such as ARF5 Aux/IAAARE-mediated signalling is probably not
and ARF7 activate transcription. When mutated, they the only pathway through which auxin functions.
often give remarkable phenotypes; for example, those Compelling reasons come from many studies: those in
seen in monopteros (ARF5) (rootless) and those seen which impermeable auxins show their effects without
in nonphototropic hypocotyl4 (ARF7) (unable to bend entering the cell 64, or in which auxin responses are
towards light)56. There is emerging evidence that ARFs simply too fast to be mediated by gene transcription,
that lack a glutamine-rich middle region function as for example, in membrane depolarization65. Decades of
transcriptional repressors55. auxin research have shown that auxin controls numer-
The expression patterns of ARF and Aux/IAA genes ous cellular processes, although the features of some
vary and depend on the tissue and stage of development responses indicate that they might not be the subject
(FIGS 2,3). Moreover, some of the most related ARF and of transcriptional control (see also BOX 1). The effects of
Aux/IAA proteins (ARF3 and ARF4, ARF6 and ARF8, auxin on the abundance and activity of the plasma-
ARF10 and ARF17, and ARF11 and ARF18; IAA6 membrane-located H+-ATPase are particularly well
and IAA19, IAA8 and IAA9, and IAA32 and IAA34) studied6669. Other regulatory targets are the potassium
(REF. 16) also share similar expression patterns. ARFs are and chloride channels and chloride-uptake transport-
specific to particular plant responses; for example, ARF1 ers7073. This auxin-mediated stimulation of ion uptake
and ARF2 regulate floral senescence57,58, and ARF7 and correlates with the idea that auxin either controls or sus-
ARF19 regulate leaf expansion and lateral root devel- tains the intracellular turgor pressure that is necessary
opment17,59. The picture is further complicated by the for plant cell growth74.
discovery that specific pairs of ARFs and Aux/IAAs In addition to the chain of events that is initiated by
can preferentially bind to each other and can also the binding of auxin to F-box proteins in the nucleus,
mediate specific processes60. Unravelling these further alternative modes of auxin perception have been
layers of regulation, analysing the possible combina- proposed. Many of these mechanisms are based on
tions of ARF and Aux/IAA interaction, and assigning proteins that have been shown to bind auxin directly.
specific pairs of ARF and Aux/IAA proteins that have Many auxin-binding studies have been carried out,
a functional significance in planta promises to take our and more than 30 years ago several binding sites were
understanding of auxin signalling to unprecedented identified in the cellular membrane system (in line with
levels of detail. the classical idea that a signal-transduction pathway
Why do plants need so many different ARF proteins, begins with ligand binding to a membrane-bound
and what are their specific regulatory targets? As has receptor) in the plasma membrane, the endoplasmic
been observed in the case of Aux/IAA loss-of-function reticulum (ER) and the vacuole75,76. Although several
mutants, systematic forward-genetics approaches with proteins with clear binding specificities were identi-
ARF genes has also failed to reveal additional growth fied, the functional characterization focused on one
phenotypes, which indicates that ARFs have redundant of them, AUXIN-BINDING PROTEIN-1 (ABP1), as
and probably compensatory functions. Direct evidence it binds auxins with high specificity and affinity (Kd in
for this was provided by microarray studies, which the 108 M range)77.
ABP1 is a soluble, ER-located, dimeric glycoprotein, seed-storage proteins of the ancient family of cupin
which forms a -jellyroll barrel that carries auxin in proteins that is functionally highly diversified78. Cupins
a central hydrophobic pocket. It resembles the 7S and triose isomerase barrel proteins form a superfamily
ARF1
ARF18
ARF11
ARF3
ARF4
ARF2
ARF5
ARF6
ARF8
ARF7
ARF16
ARF19
ARF9
ARF10
ARF17
ARF12
ARF13
ARF23
ARF21
1
12
13
21
100
101
91
96
97
10
5
17
14
15
16
20
22
23
24
25
26
77
78
79
81
82
83
84
7
87
89
90
73
76
19
40
34
39
42
43
35
2
27
28
3
9
93
94
95
98
99
41
28
8
31
32
92
4
6
33
37
45
36
in plants with possibly the widest range of biochemi- an involvement of ABP1 in cell expansion, stomatal
cal functions known for any superfamily described closure, plasma-membrane hyperpolarization and
to date79. It is thought that many of these proteins are cell division68,8084. Although most of these responses
important for cell survival through their involvement are mild, some effects seem striking, with a complete
in cell-wall structure, modification or maintenance. In loss-of-function mutation of the A. thaliana ABP1 gene
line with structural data, numerous observations show conferring embryo lethality, which indicates an essential
IAA1
IAA7
IAA2
IAA3
IAA6
IAA19
IAA4
IAA16
IAA18
IAA11
IAA8
IAA9
IAA12
IAA26
IAA27
IAA5
IAA29
IAA10
IAA30
IAA34
IAA32
IAA20
IAA33
IAA13
IAA28
IAA31
IAA14
IAA17
1
10
5
91
87
89
90
7
29
8
6
4
100
101
96
97
26
12
13
14
15
22
16
20
21
23
24
17
39
42
43
25
41
34
36
79
81
82
83
84
73
31
92
32
33
35
19
2
3
9
93
95
94
98
99
27
28
40
37
45
76
77
78
function for this protein in plant development 85. There is which protect cells directly against oxidative stress by
no direct evidence for any downstream signalling events decreasing the formation of reactive oxygen species
that are thought to occur after the binding of auxin to (ROS)86. ROS species mediate cell-wall loosening and
ABP1, or regarding the extent to which this signalling extension growth87 in a process that has been linked
pathway mediates different auxin responses compared with auxin for a long time88. The effects of ROS could
with the SCFTIR1 pathway. However, given the almost be caused either directly as a consequence of the oxida-
instantaneous auxin responses that ABP1 can mediate, tive effects of ROS on cell-wall proteins and structures88,
it is clear that gene expression need not be involved in or indirectly through the activation of signalling path-
certain aspects of auxin signalling. ways and intermediate kinases and phosphatases: these
would in turn regulate gene expression89. It has been
Downstream auxin signalling suggested that the translation of enzymes such as the
The effects of auxin are many and diverse, and have been quinone reductases protects the cell against damage
difficult to separate. They can, however, be divided into from auxin-induced oxidative stress86.
two broad categories: effects on cell expansion and effects
on cell division. There is also evidence that auxin might Auxin and cell division. Auxin also promotes cell divi-
have morphogenetic properties that are analogous to sion. Although this relationship is well known, its exact
Cupin proteins chemicals found in the animal kingdom, but the ability molecular basis is not understood. It is not yet clear
A diverse family of plant of auxin to change directly the developmental fate of cells how closely auxin is linked to progression of the cell
proteins, all of which contain at has not yet been conclusively demonstrated. cycle, even though the expression of many cell-cycle
least one double-stranded
-helix or jelly-roll structural
genes is induced by auxin90,91. There is evidence that
motif. This motif is also present Auxin and cell expansion. Consequences of ABP1- this induction is mediated through both proteasome-
in all structurally characterized mediated auxin signalling, such as cell expansion and dependent92 and ABP1-dependent85 pathways, and that
2-oxoglutarate-dependent membrane hyperpolarization, are evident at the cell auxin has many potential targets. These targets include
oxygenases, including the
periphery. Furthermore, genes that encode extracellu- proteins that are involved in transitions throughout
hypoxia-inducible factor (HIF)
hydroxylases, and is lar proteins for example, those involved in cell-wall the cell cycle, for example, entry into S phase92 and the
characteristic of the Jumonji degradation, expansins and arabinogalactans (which are G2M transition93.
transcription factors. cell-wall proteins), extensins, Pro-rich proteins (which
function as links between the cell wall and the plasma Biosynthesis and distribution of auxin
Root cap
The layers of protective cells
membrane), and class III peroxidases (which are involved The fate of developing tissue can be determined by the
that cover the tip of the in lignification, pathogen defence and wound healing) sensitivity of the growing cells to auxin (as indicated by
growing root. are affected in a gain-of-function iaa17 mutant18. This the relative expression of the various components of its
implicates at least two distinct auxin signalling pathways signalling machinery), the concentration of active auxin
Expansins
in plant structure and function through changes to the and the relative concentrations of other phytohormones.
A class of proteins that are
able to catalyse the loosening cell wall and the plasma membrane. This can also vary widely in different tissues at different
of the cell wall, enabling cell Less clear, but probably just as significant, are the developmental stages. Auxin is readily conjugated to a
expansion. responses that might be mediated by other, less well- wide variety of larger molecules, rendering it inactive.
studied groups of enzymatic early auxin-response genes. Indeed, the majority of IAA in the plant is in the form of
Extensins
Proline-rich proteins that
Two of these groups are the glutathione-S-transferases, inactive conjugates. Auxin conjugation and catabolism
connect the cell wall and the which are involved in the metabolism and detoxification can therefore decrease active auxin levels. De novo
plasma membrane. of xenobiotic compounds, and the quinone reductases, synthesis and hydrolysis of conjugates contribute to
the developmental regulation of auxin homeostasis by AUX1 has a strongly agravitropic phenotype and has a
increasing active auxin levels9498. There is a high capacity role in auxin influx110,117, but exactly how the phenotype
for auxin biosynthesis not only in young aerial tissues, is caused is unknown. The characterization of other
but also in roots, particularly in the meristematic primary members of the LAX gene family should improve our
root tip98. Auxin is synthesized from indole through understanding of auxin influx.
tryptophan-dependent and tryptophan-independent PIN proteins are related to bacterial transporters and
pathways, and has been recently reviewed99. The fact are commonly distributed polarly in the plasma mem-
that no fully auxin-deficient mutant plants have been brane, which correlates with the expected direction of
identified reflects the importance of auxin in plant polar auxin flux105108,120. Loss-of-function pin1 mutants
development. show a distinctive phenotype after the floral transition:
they often grow a single pin-shaped stem, with none of
Distribution of auxin. Auxin is unusual among phyto- the flowers or characteristic branching of the wild-type
hormones in that it has been shown to be specifically plant112. It has subsequently been shown that this pheno-
and actively transported. Indeed, the pattern of a plants type is due to lower rates of auxin transport107. Indeed, if
response to auxin is not so much determined by the auxin is applied to this pin-shaped stem, lateral growth
relative rates of auxin synthesis and catabolism as by is stimulated61.
the cells capacity for auxin influx and efflux. Although the
rates of synthesis and conjugation are undoubtedly PIN-mediated auxin transport
important for the overall auxin status of the plant, it is There are eight PIN proteins in A. thaliana, and they
the fine concentration gradients across only a few cells are expressed at distinct times and locations111. Five
that have powerful effects on plant development. These have been well characterized and show a distinctive
observations have made auxin transport one of the most polar subcellular localization. Although data for PIN1
studied topics in plant development. (the knockout of which gives rise to the most dramatic
Auxin redistribution involves many proteins100110; phenotype) have not been reported, when expressed
among them, the most investigated belong to a family in heterologous systems, two other PINs PIN2
of polarly localized plasma-membrane proteins, the PIN and PIN7 transport IAA121. Therefore, it has been
proteins. PINs are found throughout the plant kingdom111 suggested that these proteins at least do not need any
and mediate auxin efflux105108,111114. Over short dis- other plant-specific co-factors for auxin efflux. However,
tances, PIN-dependent auxin transport mediates many heterologous expression results in a reduction of their
developmental processes, including root development106 substrate specificity, which implies that plant-specific
and organogenesis61,109. co-factors might still have a role. Furthermore, it has
been shown that at least four PINs (PIN1, PIN4, PIN6
Sites of auxin transport. Ever since its discovery, auxin and PIN7) are rate-limiting for auxin efflux from plant
has been considered a highly mobile signalling molecule. cells121.
Implicit in its role in tropic growth is a requirement for The localization of PINs is extremely dynamic and
directional and responsive transport. Such a mechanism can change rapidly; such changes and the associated
needs specific and active transporters, the existence of repositioning of peaks of auxin concentration are asso-
which was predicted long before their discovery. However, ciated with important developmental events, such as
Meristem as the involvement of auxin in root specification illus- embryonic development109 and the response to gravity105.
A zone (for example, the apex trates, it is not limited to growth in response to external The mechanism that underlies the polar localization of
of the shoot) that contains
undifferentiated cells that
cues such as light and gravity, as was observed by Francis PIN proteins and their ability to relocalize rapidly is
continue to divide, providing and Charles Darwin2 its capacity for redistribution is the recycling of PIN-containing endocytotic vesicles
cells for further growth and at the heart of plant development. to and from the plasma membrane. There is evidence to
differentiation. In trees, as well as moving passively in the bulk indicate that auxin can directly influence endocytosis.
flow, auxin is transported actively through the vascular After blocking the return of endosomes to the plasma
Phloem
Vascular tissue that carries cambium a cylinder of meristematic tissue that gives membrane122, visible changes in the distribution of PINs,
organic nutrients as well as rise to (and is sandwiched between) the phloem and the as well as more general endosome markers, between the
information molecules such xylem. In A. thaliana, a plant that normally contains no endosome and the plasma membrane could be observed
as hormones throughout the woody tissue, auxin is actively transported through the at 5 M auxin123 (although this is a high concentration
plant.
vascular parenchyma. This conclusion is supported by for root growth inhibition99). The discovery that the
Xylem the cellular location of AUX1, an auxin cellular influx application of inhibitors of endosomal trafficking also
Vascular tissue that delivers carrier that is seen in positions that are consistent with inhibited polar auxin flux revealed a close relationship
water and mineral nutrients, vascular loading (in the leaves) and unloading (in the between the two processes122. It is still not clear to what
which are taken up by the root
roots)115117. AUX1 transports auxin directly, and this extent these processes can be separated.
system, to aerial organs. It also
provides mechanical support. capacity was demonstrated in Xenopus laevis oocytes at The relationship between PINs and other auxin
physiologically significant concentrations118. The asym- transporters is still unclear. For example, in A. thaliana
Agravitropic metrical subcellular localization of AUX1 (a member two multiple drug resistance/P-glycoprotein-like pro-
When a plant is unable to of the LAX family of transporters) is thought to have teins (PGPs), PGP1 and MDR1, transport auxin 100.
either perceive or respond
to gravity. Typically, the roots of
functional significance, and its localization is depend- It has been reported that PIN1 is mislocalized in a pgp1
agravitropic plants grow in all ent on an ER protein, AXR4, which has been shown mdr1 double mutant, which indicates a certain extent of
directions. to be responsible specifically for AUX1 distribution119. control over PIN function124. However, this finding has
c Shoot apical
meristem
P2
I1
P1
d Leaves
e Main root
Figure 5 | The developmental processes that are controlled by auxin flux. a | Lateral root. PINs conduct auxin from
the centre of the root (stele) to the new root tip (auxin is indicated in green and auxin transport is indicated by red
arrows), and then away again through the epidermis. This forms the basis of the fountain model of lateral root
formation62. b | Embryo. Auxin is taken to the very young embryo by PIN7 (left). At a later stage (right), the auxin flux is
reversed as PIN1, PIN4 and PIN7 conduct auxin out of the embryo. Transport by PIN1, PIN4 and PIN7 is indicated by
blue, green and red arrows, in corresponding order. c | Shoot apical meristem. Auxin is redirected towards the site of
new leaf formation (primordial P1 and P2 and the incipient primordium I1) in the epidermal layer. The shoot apex is
indicated in blue. d | Leaves. Auxin mediates vascular tissue development (indicated as uninterrupted green lines) and
patterning in the developing leaf through non-polar PIN1. The arrows indicate sites of auxin production and the red
circles indicate auxin accumulation. e | Main root. PINs determine the flux of auxin towards the root tip in the centre of
the root, and back again in the epidermis. This movement forms the basis of the roots ability to respond quickly to
gravity. Parts ae adapted, with permission, from REFS 62,125,153155 (2003) Cell Press, (2005) Company of
Biologists Ltd, (2005) Current Biology Ltd, (2004) Kluwer Academic Publishers, and (2005) Scandinavian Society for
Plant Physiology, in corresponding order.
only underline the gaps in our understanding of these negative-feedback loop for the maintenance of
processes144. Another surprising link indicates a role cellular auxin concentration but, significantly, has not
for Rac-like (ROP) GTPases in auxin action. Auxin been shown to be affected by SCFTIR1 (REF. 123). The
activates ROP3 (REF. 145); and both auxin and active regulation of auxin transport, and specifically the role
ROP3 (or RAC1) cause Aux/IAA proteins to aggre- of auxin itself in its own transport, is beginning to be
gate into discrete nuclear bodies. These structures are uncovered. This area of research promises to teach us
proteolytically active, resulting in the 26S proteasome- much about how plant growth is controlled.
mediated degradation of Aux/IAA proteins. This
potentially provides a link between auxin perception Concluding remarks
at the plasma membrane and the regulation of genes in Almost 40 years ago it was proposed that the auxin
the nucleus145,146. Proteasome-dependent auxin signal- efflux carriers and auxin receptors were closely linked,
ling does not seem to be in exclusive control of auxin if not identical157. And although this proposition has
transport. As previously discussed, synthetic auxins not found widespread support, the fact that it cannot
have been shown to slow the rate of PIN endocytosis, be fully dismissed illustrates just how closely auxin
thereby increasing the amount of PIN at the plasma signalling and auxin transport are intertwined. Indeed,
membrane. This mechanism outlines a potential many data now point to a crucial and central role of
auxin carriers such as the PIN proteins in mediating the surprising perspectives for understanding auxin action
bewildering array of developmental processes triggered and cell polarity control. Along with multiple layers
by auxin. Moreover, the recent findings on the role of of transcriptional control, these ideas will need to be
endo- and exocytotic processes that are involved in the incorporated into any tentative new models that attempt
polar localization of auxin efflux carriers opens new and to explain auxin action.
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affecting protein synthesis regulation. Physiol. 939944 (2006). larly grateful for having had the opportunity to contribute to
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activated protein kinase cascade in plants. Proc. Natl lateral root development. Plant Cell 17, 13761386 Competing interests statement
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