Download Auxin signals — turning genes on and turning cells around

Auxin signals — turning genes on and turning cells around
Thomas Berleth, Naden T Krogan and Enrico Scarpella
The extremely wide spectrum of the plant processes that
are influenced by auxin raises the question of how signals
conveyed by a single molecule can trigger such a variety of
responses. Although many aspects of auxin function remain
elusive, others have become genetically tractable. The
identification of crucial genes in auxin signal transduction and
auxin transport in the past few years has led to molecularly
testable concepts of how auxin signals regulate gene activities
in individual cells, and how the polar transport of auxin could
impact on patterning processes throughout the plant.
Addresses
University of Toronto, Department of Botany, 25 Willcocks Street,
Toronto M5S 3B2, Canada
e-mail: [email protected]
Current Opinion in Plant Biology 2004, 7:553–563
This review comes from a themed issue on
Cell signalling and gene regulation
Edited by Jen Sheen and Steven Kay
Available online 31st July 2004
1369-5266/$ – see front matter
# 2004 Published by Elsevier Ltd.
DOI 10.1016/j.pbi.2004.07.016
Abbreviations
ARF
auxin-response factor
ASK
ARABIDOPSIS Skp1-LIKE
Aux
auxin
BFA
brefeldin A
CUL
CULLIN
DBD
DNA-binding domain
E1
ubiquitin-activating enzyme
E2
ubiquitin-conjugating enzyme
E3
ubiquitin-ligase
GEF
guanosine exchange factor
GN
GNOM
IAA
indole acetic acid
MR
middle region
PIN
PIN-FORMED
QC
quiescent center
RUB1 RELATED TO UBIQUITIN1
SAM
shoot apical meristem
SCF
Skp1–Cullin–F-box
TIR1
TRANSPORT INHIBITOR RESISTANT1
Introduction
Auxin has been implicated in a confounding number of
processes in plants. The continuously extending list of
auxin functions includes the relay of environmental signals such as light and gravity, the regulation of branching
processes in shoots and roots and, more recently, the
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patterned differentiation of cells in meristems and immature organs. The fact that the distribution of auxin itself
has remained largely invisible has added to the difficulty
in imagining how a single molecule could convey such a
variety of disparate signals. As a consequence, questions
directly connected to the distribution, routes of transport
and cellular sites of perception of the crucial molecule
indole acetic acid (IAA; the most important auxin in
higher plants) are still subject to debate. At the same
time, however, auxin action has become tractable on at
least two levels. First, large protein families have been
implicated in the positive and negative transcriptional
regulation of auxin-dependent gene expression, and the
molecular mechanisms through which auxin can influence the composition of relevant transcriptional complexes have been established. Second, families of
membrane proteins have been convincingly implicated
in auxin influx and efflux. The cell biology of the polar
localization of these proteins at crucial stages of development now provides a formidable tool for understanding
apical–basal polarity acquisition and its impact on patterning processes.
In this review, we exclusively focus on recent advances
made in auxin-dependent gene regulation, auxin transport and associated patterning. Other aspects of auxin
function are excellently covered in recent reviews [1–3].
Auxin-controlled gene expression
Key to our present understanding of auxin-controlled
gene expression are transcripts that are rapidly induced
by auxin, which are collectively referred to as primary
auxin-response genes [4]. In Arabidopsis, these include
several families of well-characterized genes [5], including
many of the 29 members of the Aux/IAA gene family. Aux/
IAA genes encode small nuclear proteins that have a
common four-domain (I–IV) structure (Figure 1a). They
are not only subject to auxin-mediated transcriptional
regulation but are also involved in auxin signal transduction ([6]; reviewed in [5,7–9]). Through their conserved
domains III and IV, Aux/IAA proteins can interact with
each other and with similar domains of auxin-response
factors (ARFs). The ARF family comprises 22 transcription factors in Arabidopsis that are characterized by an
amino-terminal DNA-binding domain (DBD), a long
middle region (MR), and domains III and IV near the
carboxyl terminus (Figure 1a; reviewed in [5,10]). The
DBDs of ARFs bind to conserved promoter elements that
confer auxin-responsive gene expression and, depending
on the structure of the MR, individual ARFs function as
transcriptional activators or repressors [11,12,13]. The
regulation of gene activation by ARFs is presently far
Current Opinion in Plant Biology 2004, 7:553–563
554 Cell signalling and gene regulation
Figure 1
(a)
Low auxin
Aux/IAA
(b)
AXR1
U
E1
ARF
ECR1
R
RCE1
R
X
Repression
U
E2
RBX1
High auxin
U
U
E3
U
U
U Aux/IAA
ARF
Activation
AAAAAA
AAAAAA
R
CSN
CUL1/
AXR6
R
ASK1/2
TIR1
ARF
ARF
Potentiation
AAAAAA
AAAAAA
AAAAAA
AAAAAA
AAAAAA
26S
Aux/IAA
, etc.
Current Opinion in Plant Biology
Auxin regulation of gene expression. (a) ARF activity is controlled through interaction with Aux/IAA proteins or other ARFs. Domain I (red) of
Aux/IAA proteins functions as a transferable repression domain that is capable of suppressing gene activation conferred by nearby transcription
factors of various kinds [14]. Upon auxin-mediated Aux/IAA proteolysis, ARF monomers can activate transcription, but activation seems to be
potentiated through ARF–ARF dimerization [13]. Auxin acts antagonistically by simultaneously promoting Aux/IAA protein degradation and
Aux/IAA gene transcription. This mechanism could keep Aux/IAA protein levels in a balance, and also allows for the rapid restoration of their
abundance when auxin levels subside. Domain II is shown in blue, domain III in yellow, domain IV in green, and the ARF DBD in purple. (b) Depletion
of Aux/IAA protein levels by proteolysis through the 26S proteosome is regulated through the E3 ubiquitin (U)-ligase function of SCFTIR1, which is
composed of four subunits (ASK1/2–CUL1–RBX1–TIR1). Auxin critically influences interaction between the F-box substrate recognition subunit
TIR1 and the targeted Aux/IAA protein, whose domain II (blue) appears to be necessary for this association [20,30,31]. SCFTIR1 function is
dependent upon cyclic modification of the CUL1 subunit by RUB (R) [32], whereas de-modification is dependent on the function of the COP9
signalosome (CSN) [33,34]. Mutations in RUB-specific E1-activating (AXR1-ECR1) and E2-conjugating (RCE1) enzymes are associated with
auxin-insensitivity [28,29]. Experimental evidence suggests a role for RBX1 in both ubiquitin and RUB E3 functions [29,32].
better understood than negative gene regulation, and it
will be a major challenge for the coming years to understand the in-planta functions of ARFs that have repression
MR domains. Domains III and IV not only enable interactions between ARF and Aux/IAA proteins but also
mediate ARF–ARF dimerization (Figure 1a).
Aux/IAA proteins do not seem to bind DNA directly but
instead act as transcriptional repressors through domain I
when interacting with ARFs [14]. Aux/IAAs are extremely short-lived, and their half-lives and abundance
can be dramatically increased through the application
of proteosome inhibitors or reduced by auxin [15,16].
How auxin can influence ARF activity and Aux/IAA
Current Opinion in Plant Biology 2004, 7:553–563
abundance became apparent with the identification of
genes that are defective in Arabidopsis auxin-sensitivity
mutants (Table 1). Most of these genes encode ARFs,
Aux/IAAs or proteins that are associated with ubiquitinmediated protein degradation [8,9].
As far as they have been characterized, loss-of-function
mutations in ARF genes lead to reduced responses of
auxin-regulated gene expression [17,18,19]. By and
large, diminished auxin responses are also associated with
gain-of-function mutations in Aux/IAA genes [8,9], consistent with the idea that Aux/IAA proteins typically
function as negative regulators of ARFs (Figure 1a).
Strikingly, all gain-of-function mutations in Aux/IAA
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Auxin signaling Berleth, Krogan and Scarpella 555
Table 1
Functionally characterized genes.
Gene name
Gene identifier
Auxin-response factors
ARF3/ETTa
AT2G33860
ARF5/MP
AT1G19850
ARF7/NPH4/TIR5/MSG1
AT5G20730
Aux/IAA genes
IAA3/SHY2
AT1G04240
IAA6/SHY1
AT1G52830
IAA7/AXR2
AT3G23050
IAA12/BDL
AT1G04550
IAA14/SLR
AT4G14550
IAA17/AXR3
AT1G04250
IAA18
AT1G51950
IAA19/MSG2
AT3G15540
IAA28
AT5G25890
Protein-degradation pathway
AXR1
AT1G05180
ECR1
AT5G19180
RCE1
AT4G36800
ASK1
AT1G75950
AXR6/CUL1
AT4G02570
TIR1
AT1G12820
RBX1a
AT5G20570
Auxin transport
AUX1/WAV5
AT1G77690
PIN1
AT1G73590
EIR1/PIN2/AGR1/WAV6
AT5G57090
PIN3
AT1G70940
PIN4
AT2G01420
PIN7
AT1G23080
Reference(s)
[73]
[74,75]
[17,61,62,76,77]
[78,79]
[7,78]
[80,81]
[47,82]
[83]
[84,85]
[7]
[63]
[86]
[28,87]
[88,89]
[29,90]
[91,92]
[26,27]
[25,77]
[32]
[93–95]
[96,97]
[94,98–102]
[37]
[38]
[39]
a
An atypical ARF lacking domains III and IV, therefore not discussed
in this review. AGR, AGRAVITROPIC; ARF, AUXIN RESPONSE
FACTOR; ASK, ARABIDOPSIS Skp1-LIKE; AUX, AUXIN RESISTANT;
AXR, AUXIN RESISTANT; BDL, BODENLOS; CUL, CULLIN; ECR,
E1 C-TERMINUS-RELATED; EIR, ETHYLENE INSENSITIVE
ROOT; ETT, ETTIN; IAA, INDOLE ACETIC ACID; MP, MONOPTEROS;
MSG, MASSUGU; NPH, NON-PHOTOTROPIC HYPOCOTYL;
PIN, PIN-FORMED; RBX, RING-BOX PROTEIN; RCE, RUB1CONJUGATING ENZYME; SHY, SUPPRESSOR OF HY2; SLR,
SOLITARY ROOT; TIR, TRANSPORT INHIBITOR RESISTANT; WAV,
WAVY GROWTH.
genes affect specific sites in domain II, and lead to vastly
extended life spans and presumably much greater abundance of the respective Aux/IAA proteins [15,20,21].
Therefore, both genetic and molecular data support
the notion that auxin relieves ARF repression by promoting Aux/IAA proteolysis.
Poly-ubiquitin tagging of proteins that are destined for
proteolytic degradation occurs through the activity of
three enzymes, referred to as ubiquitin-activating enzyme
(E1), ubiquitin-conjugating enzyme (E2) and ubiquitinligase (E3) (Figure 1b). Poly-ubiquitinated proteins are
then subject to degradation by the 26S proteosome. The
Arabidopsis SCF-type of E3 ubiquitin-ligase is composed
of four primary units: ASK (in yeast Skp1), CULLIN
(CUL), RBX, and an F-box protein. Generally, the substrate specificity of E3 is thought to be mediated by its Fwww.sciencedirect.com
box component (reviewed in [22–24]). Arabidopsis auxininsensitive mutants that define SCF subunits have been
isolated (Table 1). TRANSPORT INHIBITOR RESISTANT1 (TIR1) was found to be an F-box protein that is
crucial for substrate recognition in auxin responses
[20,25]. Another component, CUL1, itself identified by
an auxin-insensitive mutant axr6 [26] (which is defective
in CUL1–ASK interaction [27]), needs to be reversibly
modified by the ubiquitin-related protein RUB1 (Figure
1b). This modification involves RUB-specific activating
(E1) and conjugating (E2) activities, through which mutations in one of the E1 subunits (AXR1) and in E2 (RCE1)
affect auxin sensitivity [28,29].
Several Aux/IAA proteins have been shown to directly
interact with SCFTIR1, suggesting that they constitute
natural substrates for SCFTIR1 action [20]. This interaction is very rapidly promoted by IAA in a concentrationdependent manner, and Aux/IAA proteins have been
shown to be more stable in axr1, rce1, tir1 and axr6 mutant
backgrounds [20,27,29,30,31]. Further, the increased Aux/IAA stability conferred by gain-of-function
mutations in domain II appears to result from a reduced
association between TIR1 and the mutant protein
[20,30,31]. How auxin promotes the interaction
between SCFTIR1 and Aux/IAA proteins is less clear.
Domain II of Aux/IAA proteins contains a 13-amino-acid
sequence that functions as a transferable degradation
signal, and is necessary and sufficient to define Aux/
IAA protein stability [16]. This sequence could be subject
to auxin-mediated protein modification that affects
SCFTIR1–Aux/IAA association. Although the degradation
signal does not contain a phosphorylation site, there are
conserved proline residues that could be targets of auxinmodulated hydroxylation or isomerization [30,31].
Alternatively, modification of F-box proteins (such as
TIR1) or CUL could influence the interaction between
Aux/IAA proteins and SCFTIR1. Specifically, CUL modification seems to be subject to complex regulation, as
both RUB conjugation and deconjugation are necessary
for normal auxin response [32]. RUB deconjugation is
dependent on the activity of the CONSTITUTIVE
PHOTOMORPHOGENIC9 (COP9) signalosome ([33];
reviewed in [34]). Finally, it is possible that SCFTIR1
function and Aux/IAA stability are controlled by further
unknown proteins, which may be identified in genetic
screens. Such a role has recently been established for
SGT1b, a protein previously implicated in plant diseaseresistance signaling [35].
When attempting to pin down the role of auxin, it is
interesting to note that its effect on interactions between
Aux/IAA proteins and SCFTIR1 can be seen in crude plant
extracts [30]. Therefore, auxin signal transduction
through this important pathway seems to occur entirely
through soluble factors. Future research will precisely
assess the relevance of this pathway in natural auxin
Current Opinion in Plant Biology 2004, 7:553–563
556 Cell signalling and gene regulation
Figure 2
(a)
Nucleus
Golgi
apparatus
Actin
filament
(b)
Current Opinion in Plant Biology
Dynamic auxin transport and patterning. (a) Hypothetical cellular mechanism for PIN localization (redrawn from [43]). Top: basal localization of the
PIN protein (red) depends on BFA-sensitive vesicle transport. In BFA-treated cells, PIN accumulates in undefined endosomal membrane structures
(light blue) [40,42]. Polar auxin transport depends on an intact actin cytoskeleton, and a high-affinity 1-N-naphthylphthalamic acid (NPA)-binding
protein (green), which is known to interact with actin, may connect the respective transport vesicles (yellow) with the actin tracks. Permanent
cycling of PIN proteins between intracellular compartments and the plasma membrane could account for rapid relocation of PIN protein, which
occurs in response to tropic stimuli [37,103]. Bottom: hypothetical intercellular stabilization of PIN protein localization. If the localization of PIN
proteins (red) is responsive to external signals, it could also respond to auxin flow. This would generate a postulated feed-back mechanism [45]
that would result in the integration of apical–basal cell polarity and, further, in the reinforcement of unevenness of auxin conductivity along certain
lines of cells (as proposed in [44–46,53,57,60]). (b) In the two-cell stage embryo (left), auxin seems to be transferred from the basal to the
apical cell, the progenitor cell of the embryo proper [39]. This leads to a transient auxin-response maximum (blue) in the apical cell. In the early
globular embryo (middle), the direction of auxin flow seems to be reversed, leading to a persistent auxin maximum in the uppermost suspensor
cell, which will give rise to the central part of the primary root meristem. In the triangular-stage embryo (right), the central procambial strand
Current Opinion in Plant Biology 2004, 7:553–563
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Auxin signaling Berleth, Krogan and Scarpella 557
responses and will functionally dissect the pool of soluble
components.
Auxin transport
As is the case for auxin perception, the molecular understanding of auxin transport is far from comprehensive.
Nevertheless, the past two years have seen the detailed
characterization of several new members of the PIN
family of putative auxin-efflux membrane proteins and
the revelation of further details on how these proteins are
localized (Figure 2a, Table 1). Consistent with their
presumed function, all characterized proteins of the
PIN family show polar localization in cells, reflecting
the efflux pole of the presumed auxin flow direction in
various instances [36–38,39]. The ability of cells to
position and dynamically reposition PIN proteins has
previously been attributed to their rapid cycling between
the plasma membrane and an intracellular compartment
[40]. The vesicle transport that is crucial for proper
membrane localization of PINs has been shown to
depend on the guanosine exchange factor (GEF)
EMB30/GN [36]. In emb30/gn mutants, the localization
of PIN1 is no longer polar; hence, these mutants display
extremely strong polarity defects, similar to those caused
by strong inhibition of auxin transport [36,41]. The pin1
pin3 pin4 pin7 quadruple mutant displays similar extreme
polarity distortions, supporting a role for PIN genes in
auxin transport and suggesting that EMB30/GN-dependent vesicle transport is crucial in the localization of all
PIN proteins [39]. The GEF function of EMB30/GN is
thought to act on GTPases of the adenosyl ribosylation
factor class and is sensitive to the fungal metabolite
brefeldin A (BFA), which causes severe defects in cell
polarity [36]. It seems that BFA affects cell polarity
primarily through EMB30/GN because the localization
of PIN1 is no longer sensitive to BFA in plants expressing
a modified, BFA-resistant version of EMB30/GN [42].
The cell biology of PIN1 localization displays striking
similarities to other instances of polar membrane protein
localization in higher eukaryotes [43]. As these parallels
can serve as templates for future exploration, it can be
predicted that the organismal polarity conveyed by auxin
transport will soon find a firm molecular link to the
cytoskeletal organization of the individual cell.
Auxin in pattern formation
For years, a role for auxin in tissue patterning was suggested by auxin application and vascular severance
experiments, which led to a concept of auxin as an
integrator of apical–basal plant cell polarity ([44,45];
Figure 2a). This basic concept has subsequently been
supported by genetic [26,36,46,47] and pharmacological
[41,48,49] evidence. More recently, detailed studies have
investigated the role of directional auxin signals and cell
polarity in pattern formation in early embryos and apical
meristems, as described below.
It has been revealed that strongly diminished auxin signal
transduction is associated with incomplete vascular systems and, in extreme cases, with failure to differentiate
hypocotyl and root meristem and to properly position
cotyledons in the early embryo. This triple-defect is
observed in seedlings in which the ARF5/MP, IAA12/
BDL or CUL1/AXR6 gene is mutated [26,46,47]. How
are these seemingly disparate traits connected to diminished auxin signaling and impaired vascular development? Results from investigations of post-embryonic
organs provide a plausible explanation for the distortions
observed in early embryos (Figure 2b; reviewed in [50]).
First, the specification of root meristem initials is dependent upon a signaling source in the quiescent center
(QC), which is represented in the embryo by the progenitor hypophyseal cell [51]. The position of this signaling source, in turn, seems to be strictly correlated with the
location of an auxin-response reporter gene expression
maximum formed at the basal end of the central vascular
system [52], apparently in response to auxin supplied
from apical sources. These findings link formation of the
root apical meristem to apical–basal auxin signaling
through a central vascular strand, a correlation that also
seems to hold for the post-embryonic formation of lateral
roots [53]. Second, independent evidence has demonstrated how the central vascular tissue serves as a signaling source for cell division and patterning of the overlying
ground tissue through the action of the non-cell-autonomous SHORT-ROOT protein [54]. This could explain
why basal domains fail to differentiate in highly auxininsensitive mutant embryos. Finally, the application of
auxin to post-embryonic shoot apical meristems (SAMs)
has implicated auxin not only in the initiation of lateral
organ primordia but also in their proper spacing [55].
This emerging picture was largely confirmed and
extended through the use of molecular probes, including
the presumed auxin (response) distribution indicator
DR5-GFP, and antibodies against IAA or against presumptive auxin-transport proteins, such as PIN1 or AUX1
(Figure 2 Legend Continued) (orange), which is possibly established through auxin canalization in the early globular embryo, seems to be a
pre-requisite for three subsequent patterning processes. First, it may supply auxin to sustain the basal auxin maximum and the associated
acquisition of QC identity by cells in this region [52]. Signals from the QC, in turn, confer stem-cell identity to the neighboring cells (black arrows).
Second, the central procambial strand also serves as a signaling source for ground tissue (yellow) proliferation and patterning (blue arrows) [54].
Third, self-canalizing auxin transport (red arrows) positions lateral shoot organs (here cotyledons) and could establish phyllotactic patterns by
generating lateral-inhibitory fields of auxin depletion around newly initiated primordia [57]. Directions of auxin flow are predicted from the
intracellular positions of auxin-efflux proteins of the PIN family, whereas auxin concentrations are deduced from the expression levels of the
DR5 auxin-response marker [39,52,57].
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Current Opinion in Plant Biology 2004, 7:553–563
558 Cell signalling and gene regulation
(Table 1). Auxin-response maxima in preglobular
embryos have been visualized in the apical cell of the
two-cell embryo and may be established by the apical
flow of auxin from the basal cell, as suggested by the
intracellular localization of the newly characterized PIN
protein PIN7 ([39]; Figure 2b). Later, once a globular
embryo proper has been established, an anatomically
recognizable axis is associated with basally positioned
PIN1 protein in central cells, presumably reflecting an
apical–basal auxin flow that is associated with the emergence of procambium in the center of the embryo. It is at
the bottom of these cell files, before the differentiation of
functional vasculature, that the embryonic basal auxinresponse maximum emerges (Figure 2b).
Visualization of auxin-transport membrane proteins, such
as PIN1 or the presumed auxin-influx protein AUX1, also
suggests routes for canalized auxin in the shoot meristem.
On the basis of the intracellular position of the PIN1
protein (and supported by independent evidence of the
importance of the epidermis in the initiation of shoot
lateral organs [56]), a tip-directed flow in the epidermal
layer seems to supply IAA to the SAM surface, from
where it appears to become redirected to inner cells at
distinct spots [57]. Lateral organs (leaves or flowers) are
initiated at these sites. During organ outgrowth, PIN1 is
first found in the organ center and then along the organ
midline. The net result is the local concentration of
initially dispersed auxin in emerging organs, which function as auxin sinks. This could result in depletion of auxin
in surrounding regions and thereby generate a phyllotactic pattern through lateral inhibition, as proposed in
various models [58,59]. Most excitingly, auxin, and the
probable feed-back associated with its transport, seems to
have an instructive role in assigning differential identities
to distinct areas within the meristem [57]. In pin1
(auxin-transport defective) mutants, lateral organs can
still be initiated by the local application of IAA, but
PIN1 mRNA expression does not become restricted to
individual spots, indicating that auxin transport feedsback on its own routes.
Self-regulation of auxin transport may not end with the
specification of organ initiation sites. Instead, reproducible patterns of auxin distribution (suggested by the expression of the DR5 auxin-response marker), with
maxima at organ tips, are observed in various kinds of
lateral shoot organs as well as in lateral root primordia
[60]. The formation of these maxima is usually correlated with a corresponding polar intracellular localization
of PIN proteins, and is obstructed in plants carrying
multiple mutations in PIN genes.
Separation of auxin pathways
Genetic dissection of signaling pathways should eventually determine whether auxin directly regulates the
extreme diversity of functions that it is alleged to medCurrent Opinion in Plant Biology 2004, 7:553–563
iate. For example, are there specific auxin signal transduction pathways for patterning events as opposed to
other kinds of auxin responses? Although the fairly small
number of mutants that have auxin-related patterning
defects might suggest the involvement of only a few
specific genes in patterning, more recent genetic studies
point in the opposite direction. Embryonic and postembryonic patterning defects associated with loss of
ARF5/MP function are enhanced by mutations in
ARF7/NPH4 [19], although the phenotype of the
nph4 single mutant implicates the NPH4 gene specifically
in auxin-controlled cell expansion [61,62,63]. Conversely, ARF5/MP functions in the post-embryonic control of
cell expansion. Further, an increasing number of doublemutant combinations of auxin-response mutants, each
with no apparent patterning defect, result in rootless,
mp-like seedlings [20,29]. It therefore seems possible
that common auxin signaling pathways successively operate in the same organ: first, to execute genetic patterning
programs in the primordium, and then to relay auxin
responses to environmental signals in the mature organ.
Tracing in vivo interactions among ARF and Aux/IAA
proteins will be crucial for dissecting the genetic complexity of auxin-mediated gene regulation in auxin
responses. ARF–ARF interactions are already known to
display some degree of specificity in yeast two-hybrid
assays, whereas no discriminating interaction properties
of Aux/IAA proteins are apparent in single-cell assays
[19]. Future research will determine whether specific
expression profiles, or other unknown influences, impart
greater selectivity and correlate specific interactions to
individual auxin responses.
Conclusions
Recent research has generated strong confidence that the
details of auxin-mediated gene regulation, if not the
entire signal transduction chain, and of the cell biological
mechanisms underlying auxin transport will be explored
in molecular detail within the next few years. Moreover,
there is increasing evidence that similar principles apply
across the angiosperms and beyond. The ARF gene
family, for example, is highly conserved from Arabidopsis
to rice [64], and an instrumental role of auxin transport in
embryo polarity has been demonstrated even in the
brown alga Fucus distichus [65]. This could also be true
for other elements of auxin signal transduction
[66,67,68,69,70] and auxin-regulated gene activities
[71], some of which seem to affect morphogenesis
through the control of cell proliferation [68,72]. Most
importantly, it can be expected that analogies in the cell
biology of the polarization processes in animals and fungi
will strongly promote our understanding of auxin functions in plants. Ironically, therefore, research in the near
future may rapidly elucidate the roles of the identified
auxin signaling and transport proteins in their cell biological context, whereas IAA itself, as the genetically least
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Auxin signaling Berleth, Krogan and Scarpella 559
tractable element, may be the last piece to be integrated
into the puzzle.
Acknowledgements
We thank Dinesh Christendat (Toronto) and Hanjo Hellmann (Berlin)
for valuable comments on the manuscript. We apologize to colleagues
whose results could not be included in the available space. The authors’
signal transduction research has been supported by grants from the
Natural Science and Engineering Research Council of Canada (NSERC)
to T Berleth, as well as by an NSERC long-term postgraduate fellowship
and a Government of Ontario/Dr FM Hill Scholarship in Science and
Technology (OGSST) to NT Krogan.
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www.sciencedirect.com
strong transcriptional repressor, and the presence of an LxLxL motif is
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Current Opinion in Plant Biology 2004, 7:553–563
560 Cell signalling and gene regulation
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several auxin-response mutants that are seedling lethal, lack hypocotyl
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Current Opinion in Plant Biology 2004, 7:553–563
562 Cell signalling and gene regulation
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www.sciencedirect.com
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Current Opinion in Plant Biology 2004, 7:553–563