REVIEW
Hormone interactions at the root apical meristem
Eva Benkova´ Æ Jan Heja´tko
Received: 23 May 2008 / Accepted: 27 August 2008
Ó Springer Science+Business Media B.V. 2008
Abstract Plants exhibit an amazing developmental flexibility.
Plant embryogenesis results in the establishment of
a simple apical–basal axis represented by apical shoot and
basal root meristems. Later, during postembryonic growth,
shaping of the plant body continues by the formation and
activation of numerous adjacent meristems that give rise to
lateral shoot branches, leaves, flowers, or lateral roots. This
developmental plasticity reflects an important feature of the
plant’s life strategy based on the rapid reaction to different
environmental stimuli, such as temperature fluctuations,
availability of nutrients, light or water and response
resulting in modulation of developmental programs. Plant
hormones are important endogenous factors for the integration
of these environmental inputs and regulation of
plant development. After a period of studies focused primarily
on single hormonal pathways that enabled us to
understand the hormone perception and signal transduction
mechanisms, it became obvious that the developmental
output mediated by a single hormonal pathway is largely
modified through a whole network of interactions with
other hormonal pathways. In this review, we will summarize
recent knowledge on hormonal networks that regulate
the development and growth of root with focus on the
hormonal interactions that shape the root apical meristem.
Keywords Root meristem Á Hormonal cross-talk Á
Abscisic acid Á Auxin Á Brassinosteroid Á Cytokinin Á
Ethylene Á Gibberellin Á Arabidopsis
Introduction: when root grows
The root meristem is an organ of well-defined structure
with stereotypical patterns of cell types along radial and
longitudinal axes. The radial pattern is organized in concentric
rings of lateral root cap, epidermis, ground tissue
(cortex and endodermis) and a pericycle surrounding a
central stele (Dolan et al. 1993; van den Berg et al. 1998).
The radial patterning is laid down during embryogenesis
and maintained by stem cell niche activity consisting of
four sets of initials: the lateral root cap/epidermal, the
cortical/endodermal, the columella and the pericycle/vascular
initials surrounding quiescent centre (QC) (Dolan
et al. 1993; van den Berg et al. 1998). Stem cells have the
capacity for prolonged self-renewal (Watt and Hogan
2000). Each stem cell undergoes an asymmetric division to
produce one daughter cell that remains under the influence
of a short-range signal from the QC, preventing differentiation
and maintaining the stem cell status and the other
daughter cell becomes part of differentiated tissues (van
den Berg et al. 1998).
Along the longitudinal axis, the root meristem forms a
distal root tip, including stem cell niche, columella and
lateral root cap, proximal meristem with a population of
rapidly dividing cells and elongation zone where cells
leaving the root meristem undergo rapid elongation and
mature (Dolan et al. 1993). The longitudinal root meristem
organization is completed during the postembryonic
development when the balance in the rate of generation
of new cells in the proximal root meristem and the
E. Benkova´ (&)
Department of Plant Systems Biology, Flanders Institute for
Biotechnology (VIB), Gent University, Technologiepark 927,
9052 Gent, Belgium
e-mail: eva.benkova@psb.ugent.be
J. Heja´tko
Laboratory of Molecular Plant Physiology, Department of
Functional Genomics and Proteomics, Institute of Experimental
Biology, Masaryk University, Kamenice 5 62500, Brno,
Czech Republic
123
Plant Mol Biol
DOI 10.1007/s11103-008-9393-6
differentiation of daughter cells leaving root meristem is
established, resulting in the formation of the root meristem
of stable size (Dello Ioio et al. 2007; Dolan et al. 1993).
The identification of mutants with defects in the root
meristem organization has provided a basis for understanding
the mechanisms of radial and longitudinal
patterning in the root. Organization of root meristem along
the longitudinal axis is primarily under the control of the
plant hormone auxin and of the downstream auxin-acting
family of PLETHORA (PLT) (AP2-like transcription factors)
genes. The PLT expression follows the auxin gradient
along the root meristem with its maxima in the stem cell
niche region. PLT genes have been shown to act in a
dosage dependent manner, high activity promotes stem cell
identity and maintenance, whereas low levels promote
mitotic activity of stem cell daughters; and even lower
levels are required for cell differentiation (Aida et al. 2004;
Galinha et al. 2007).
In parallel with the auxin and PLT pathway, the
SHORTROOT/SCARECROW (SHR/SCR) pathway regulates
the radial patterning, and they converge to specify and
regulate function of the stem cell niche. Plants homozygous
for the scr and shr mutations are defective in the division of
the cortex/endodermis initial daughter cell, resulting in the
formation of a single layer of ground tissue instead of two
(Benfey et al. 1993; Scheres et al. 1995). Functional
studies revealed that SHR, a transcription factor of the
GRAS family, acts upstream of the SCR transcription
factor (Helariutta et al. 2000). SHR moves from the central
vasculature, place of its transcription, into the surrounding
tissue layer, where after heterodimerization with SCR, it
stimulates by a positive feedback loop the expression of
SCR gene (Cui et al. 2007; Di Laurenzio et al. 1996;
Nakajima et al. 2001). Ectopic expression experiments
suggested that the SHR movement is limited to a single cell
layer and that heterodimerization with SCR might be the
mechanism to sequester the SHR protein in the nucleus and
restrain its movement to a single cell layer adjacent to the
stele (Cui et al. 2007). Recently, two zinc-finger proteins,
MAGPIE (MGP) and JACKDAW (JKD), have been
identified as factors required for radial patterning and
contribute to refining the SHR and SCR action range
(Welch et al. 2007).
Both auxin/PLT and SHR/SCR pathways are closely
interconnected with the activities of several hormonal
pathways. The PLT pathway acts downstream of the auxin
signalling (Aida et al. 2004; Galinha et al. 2007), whereas
among the eight direct targets of SHR, as elegantly identified
by a set of microarray analyses (Levesque et al.
2006), one is involved in the brassinosteroid pathway
(cytochrome P450/BRox62 regulating brassinosteroid biosynthesis;
(Shimada et al. 2003)) and the other in the
gibberellin signalling (SNEEZY/SLEEPY2 (SNE) F-box
protein (Levesque et al. 2006)). Several other indirect targets
are the molecular components of auxin biosynthesis
SUR2(SUPERROOT) (Barlier et al. 2000), signalling
IAA12/BDL(BODENLOS) and ARF5/MP(MONOPTEROS)
(Hamann et al. 2002; Hardtke and Berleth 1998) and
transport PIN3 and PIN7 (Friml et al. 2003a; Friml et al.
2002b); brassinosteroid perception BRL3 (Cano-Delgado
et al. 2004) and biosynthesis Cyp90D1 (Kim et al. 2005)
and gibberellin signalling RGL1 and RGL2 (Lee et al.
2002; Wen and Chang 2002); and GA3 biosynthesis
(Helliwell et al. 1998; Levesque et al. 2006). This clearly
reflects that root development requires not only transcriptional
network but also network of hormonal signalling.
Indeed, besides the plant hormone auxin, the key hormonal
regulator of the root organogenesis, other plant
hormones, e.g. cytokinin (Dello Ioio et al. 2007; Mahonen
et al. 2006; Werner et al. 2003), ethylene (Ortega-Martinez
et al. 2007; Swarup et al. 2007), brassinosteroids (Mouchel
et al. 2006), gibberellin (Fu and Harberd 2003; UbedaTomas
et al. 2008) and abscisic acid (Achard et al. 2003)
also participate in the regulation of different aspects of root
organogenesis and activity. Lately, it became obvious that
single hormone input is strongly modulated by other hormonal
pathways acting in parallel. Characterization of
these interactions and their impact on the root meristem
development will be discussed in detail in the following
sections.
Auxin: the hormonal regulator of root development
Auxin has been shown to regulate an extremely broad
range of developmental processes, such as embryogenesis,
organogenesis of leaves, flowers, ovules or lateral roots,
gravitropic responses and apical hook formation. The
whole process of root organogenesis, begining with the
establishment of the root pole in embryos (Friml et al.
2003a; Weijers et al. 2006), positioning and formation of
stem cell niche (Blilou et al. 2005; Sabatini et al. 1999),
maintenance of mitotic activity in proximal meristem
(Beemster and Baskin 2000; Dello Ioio et al. 2007; Galinha
et al. 2007; Stepanova et al. 2008) and rapid elongation
and differentiation of cells leaving the root meristem
(Rahman et al. 2007) has been shown to be under the
control of auxin. A real breakthrough in our understanding
of how auxin molecule can lead to such a variety of
developmental responses is the discovery of the instructive
function of the auxin gradient formed along the longitudinal
axis of the root meristem (Benkova et al. 2003; Friml
et al. 2002a; Sabatini et al. 1999). The auxin gradient is
generated by the concerted action of AUX/LAX auxin
influx carriers (Bennett et al. 1996; Yang et al., 2006), PIN
auxin efflux carriers (Galweiler et al. 1998; Luschnig et al.
1998; Friml et al. 2002a, b; Friml et al. 2003b; Petra´sˇek
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et al. 2006) and members of the multi-drug-resistant/
P-glycoprotein (MDR/PGP) subfamily of ATP-binding
cassette (ABC) proteins (Blakeslee et al., 2007). Interference
with its establishment results in dramatic patterning
and developmental defects in the root meristem (Blilou
et al. 2005; Friml et al. 2002a; Sabatini et al. 1999).
It is still not precisely known how the auxin gradient
achieves the specificity of the response required for the
different aspects of the root meristem development by
using the signal transduction pathway consisting of four
TIR/AFB auxin receptors of the F-box protein family
(Dharmasiri et al. 2005), 29 AUX/IAA negative regulators
(Overvoorde et al. 2005) and 23 ARF (AUXIN
RESPONSE FACTORS) transcription factors (Okushima
et al. 2005), activating the expression of downstream auxin
response genes. It has been proposed that certain combinations
of AUX/IAAs and ARFs determine the response
specificity (Hamann et al. 2002; Knox et al. 2003; Weijers
et al. 2005). In the case of root development, the specific
pair of IAA12/BDL and ARF5/MP was identified to
determine the establishment of root pole in early embryogenesis
(Hamann et al. 2002). Beside the BDL-MP pair,
some other genes of the auxin signalling pathway (SHY2/
IAA3, AXR3/IAA17 and AXR2/IAA7) were shown to be
involved in different aspects of root growth (Leyser et al.
1996; Nagpal et al. 2000; Tian and Reed 1999), although
their direct ARF counterparts are still unknown. The PLT
gene family seems to play an important role in the developmental
interpretation of the auxin gradient. PLT genes
respond in an auxin concentration-dependent manner to
regulate stem cell identity and maintenance, mitotic
activity of stem cells’ daughters and cell differentiation
(Galinha et al. 2007).
Auxin: universal partner in hormonal interactions?
Interestingly, many mutants in the auxin pathway exhibit not
only auxin-related root phenotypes but also an altered sensitivity
to other hormones. For example, root growth of the
auxin transport mutants aux1 and pin2 is also ethylene
resistant (Roman et al. 1995). Similarly, mutants in the auxin
signalling shy2-2/iaa3, axr2/iaa7 and tir1 do not exclusively
exhibit an auxin-resistant root phenotype, but also exhibit a
changed sensitivity to other hormones such as cytokinins,
abscisic acid or ethylene (Alonso et al. 2003; Tian and Reed
1999; Wilson et al. 1990). This promiscuous behaviour of
mutants points out that auxin regulated events in root growth
are tightly interconnected with other hormonal pathways and
in many interactions auxin seems to act downstream of other
hormonal pathways. From longstanding investigations on
regulatory pathways in root development, auxin has emerged
as one of the key factors involved in many very specific
aspects of root organogenesis. Therefore, from practical
reasons, auxin and its interactions will be discussed in the
context of respective hormonal pathways (see Fig. 1).
Ethylene is all around … and interacts
Typically, seedlings germinated at high ethylene concentrations
have short hairy roots, a phenotype in some aspects
resembling auxin-treated roots. Detailed developmental
studies revealed that ethylene affects root growth primarily
by inhibiting the rapid expansion of cells leaving the root
meristem (Le et al. 2001; Ruzicka et al. 2007; Swarup
et al. 2007). More recently, ethylene has also been demonstrated
to participate in the regulation of the cell division
activity of the QC. Manipulation of the ethylene pathway
by genetic or chemical tools affected the division activity
of the QC suggesting its functions in maintenance of stem
cell niche by regulating the balance between proliferation
and quiescence of stem cells (Ortega-Martinez et al. 2007).
As mentioned above mutations in many auxin transport
or signalling components cause aberrant responses to ethylene,
thus pointing to an ethylene–auxin interaction.
Mutations in the auxin influx and efflux carrier genes
AUX1 and EIR1/AGR/PIN2 (Luschnig et al. 1998; Pickett
et al. 1990; Roman et al. 1995), several components of the
auxin signalling cascade, including the auxin receptor TIR1
(Alonso et al. 2003) and the AUX/IAA regulators axr2/
iaa7 (Wilson et al. 1990) and axr3/iaa17 (Leyser et al.
1996; Swarup et al. 2007) confer ethylene insensitive root
growth phenotypes. Stepanova et al. (2005) demonstrated
that mutations in two Arabidopsis genes ASA1 and ASB1
encoding subunits of the anthranilate synthase enzyme that
synthesizes an auxin precursor also confer ethylene
insensitive root growth phenotypes. Gene interaction
studies have positioned these auxin pathway components
downstream of the ethylene signal transduction pathway
(Roman et al. 1995; Stepanova et al. 2005), suggesting that
ethylene inhibition of root growth requires auxin biosynthesis,
transport and responses. The hypothesis is further
corroborated by other findings. As indicated by Rahman
et al. (2001), aux1 root growth can be sensitized to ethylene
when cultured in the presence of auxin. Accordingly,
ethylene sensitivity of the ethylene response reporter EBS
in roots depends on auxin (Stepanova et al. 2007). Measurements
of the auxin biosynthesis rate upon ethylene
treatment revealed a stimulatory effect of ethylene on the
auxin biosynthetic pathway (Swarup et al. 2007). Indeed,
several genes of the auxin biosynthesis pathways were
isolated and found to be under transcriptional control of
ethylene. Beside ASA1 and ASB1, (Stepanova et al. 2005),
recently, a small family of genes encoding a long-anticipated
tryptophan aminotransferase, TAA1, regulating the
indole-3-pyruvic acid branch of the auxin biosynthetic
pathway (Stepanova et al. 2008; Tao et al. 2008) has been
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identified. Interestingly, TAA1 and its close homologue
TAR2 are expressed in different organs including root
meristem. Lack of their functions caused a drastic reduction
in the meristem size and collapse of the root meristem,
similar to mutants with reduced auxin levels due to a
defective auxin transport (Benjamins et al. 2001; Blilou
et al. 2005). Thus, analysis of TAA1 and its homologues
represents an important and for a long time missing link
between local auxin production, tissue-specific ethylene
effects and organ development, including root meristem
(Stepanova et al. 2008).
A mechanistic model integrating our recent knowledge
on the auxin - ethylene cross talk in roots has been proposed
(Ruzicka et al. 2007; Stepanova et al. 2007; Swarup
et al. 2007). According to this model, ethylene stimulates
auxin biosynthesis in different plant organs via its known
signalling pathway. In addition, ethylene increases the
auxin transport capacity by regulating the transcription of
several auxin transport components, including PIN1, PIN2
and AUX1 (Ruzicka et al. 2007). The additionally produced
auxin is redistributed by polar auxin transport
towards the root tip. The major components of the auxin
transport in these tissues, AUX1 and PIN2, mediate the
auxin delivery into cells of the elongation zone, where
auxin accumulates and induces local auxin responses that
inhibit cell elongation and overall root growth (Ruzicka
et al. 2007; Stepanova et al. 2007; Swarup et al. 2007).
Thus, inhibition of auxin responses in several mutants of
the auxin signalling results in ethylene insensitive root
growth. As revealed by tissue targeted inhibition of auxin
responses, ethylene inhibition of root growth requires auxin
responses in multiple cell layers of the elongation zone
tissues (Swarup et al. 2007). However, this mechanism can
account for most, but not all, ethylene effects on the root
Fig. 1 Scheme of the hormonal cross-talk involved in the regulation
of the root apical meristem growth and development. Selected
regulators of the cross-talk are highlighted. Dashed lines correspond
to not completely clear or mostly indirect regulations. c.d. is transition
zone where differentiation starts
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growth. Some of the auxin insensitive mutants, e.g. slr/
iaa14 (Fukaki et al. 2002), shy2-2/iaa3 (Tian and Reed
1999) or nph4-1/arf7, arf19 (Okushima et al. 2005) are
strongly resistant to auxin, but not or weakly to ethylene
(Li et al. 2006a; Ruzicka et al. 2007). In addition, auxin
transport mutants aux1 and pin2 do not exhibit complete
ethylene resistance. Based on the extensive gene expression
analysis, Stepanova et al. (2007) predicted that
besides an auxin-mediated ethylene response there are at
least three other types of interactions between auxin and
ethylene. Thus, although an important part of the ethylene
effect on root growth is performed through the auxin
pathway, there appears to be a direct ethylene-specific,
auxin response-independent component for this regulation.
Maintenance of a proper ethylene–auxin concentration
balance along the root meristem seems to be one of the
important mechanisms involved in ethylene–auxin regulated
root growth. Besides the previously described control
of the auxin biosynthesis by ethylene, auxin control over
ethylene biosynthesis is also well established (Bleecker and
Kende 2000; Liang et al. 1992; Yang and Hoffman 1984).
One of the rate-limiting enzymes in the ethylene synthesis
pathway is 1-aminocyclopropane-1-carboxylate synthases
(ACS). Numerous ACS genes are expressed in the root
meristem in a tissue-specific manner (Tsuchisaka and
Theologis 2004) and their expression is enhanced upon
auxin treatment (Tsuchisaka and Theologis 2004). This
complicated regulatory loop between auxin and ethylene
biosynthetic pathways suggests the presence of a complex
feedback mechanism involving components that tightly
control the actual auxin–ethylene level in root cells. One of
the candidates for such a component might be the
POLARIS (PLS) gene encoding a short 36-amino acid
peptide. Mutation in PLS results in an enhanced ethylene
phenotype, repressed auxin transport and auxin accumulation
(Casson et al. 2002; Chilley et al. 2006). PLS
transcription itself is under the negative control of ethylene
and is stimulated by auxin. The pls mutant phenotype can
be restored by genetic and pharmacological inhibition of
the ethylene action, implicating PLS as a negative regulator
of ethylene responses. Chilley et al. (2006) proposed a
model in which the PLS transcription is activated at the
root tip by the relatively high auxin concentration that
accumulates and is required for correct cell division at that
position (Blilou et al. 2005; Friml et al. 2002a; Sabatini
et al. 1999). Here, PLS acts as a negative regulator of
ethylene signalling, which is inhibitory to cell division and
expansion, and therefore root growth. Although some
aspects of pls phenotype are seemingly in contradiction
with previously shown stimulatory effect of ethylene on
auxin biosynthesis, PLS might be an important component
of the ethylene sensing mechanism for the tuning auxin
pathway action during root development.
Cytokinin: antagonist in root
The negative role of cytokinin (CK) on root growth is a
long-known phenomenon that has been proven by both
exogenous CK application and overexpression of the bacterial
ISOPENTENYLTRANSFERASE (IPT) gene (Hewelt
et al. 1994; Kuderova et al. 2008; Li et al. 2006b; Medford
et al. 1989; Smigocki 1991). Accordingly, decreased
endogenous CK levels via overexpression of the CYTOKININ
OXIDASE/DEHYDROGENASE (CKX) gene results
in an opposite effect i.e. enhanced root meristem and the
root growth (Werner et al. 2003; Yang et al. 2003).
Interestingly, studies on mutants of CK signalling
revealed a positive role of CK in the root meristem. The
root meristem was reduced in the triple cytokinin receptor
mutant ahk2,ahk3,ahk4 and multiple mutant in ahp members
of the signal transduction cascade (Higuchi et al.
2004; Hutchison et al. 2006; Nishimura et al. 2004; Riefler
et al. 2006; To et al. 2004). Based on the phenotypes of CK
signalling mutants, the modulation of CK levels led to the
hypothesis of ‘‘supraoptimal’’ CK concentration in the root
meristem (Ferreira and Kieber 2005), according to which,
downregulation of the endogenous CK levels to optimal
levels via CKX overexpression enhances root growth.
However, both complete absence of the CK signal in CK
signalling mutants and its abundance after IPT overexpression
and/or exogenous application, respectively, exert
optimal levels and lead to inhibitory effects (Ferreira and
Kieber 2005).
A role for CK during embryonal root formation has been
suggested by the wooden leg (wol) mutant identified for its
defect in the radial root patterning (Scheres et al. 1995). In
the wol embryos, the last series of divisions in the stele is
missing, leading to the formation of the pericycle with a
reduced cell number (Scheres et al. 1995). In the postembryonal
development, wol mutation affects the asymmetric
division of the procambium, resulting in a defective vasculature
without phloem and formed exclusively by the
protoxylem (Mahonen et al. 2000; Scheres et al. 1995).
WOL was found to be allelic to the CK receptor AHK4/
CRE1, thus pointing to a role for CK as a negative regulator
of the protoxylem differentiation from the
procambium. CK inhibition of the protoxylem differentiation
allows procambial cells to undergo another
developmental pathway, leading to phloem formation.
AHP6, the downstream component of the CK transduction
pathway, has been revealed to act in a negative regulatory
feedback loop, antagonizing the CK effects (Mahonen et al.
2006).
Interestingly, the wol defect in the vasculature formation
is rescued by the fass (fs) mutation (Scheres et al. 1995),
allelic to TONNEAU2 that codes for the putative novel
protein phosphatase 2A regulatory subunit (Camilleri et al.
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2002). It seems that additional cell layers in the radial
pattern of the fs mutant (Torres-Ruiz and Jurgens 1994)
allow phloem differentiation while the reduced number of
cells in the stele of wol is ‘‘used up’’ by xylem poledirected
protoxylem differentiation (Scheres et al. 1995).
However, missexpression of AHP6 in wol embryos
(Mahonen et al. 2006) suggests that positional, CK-mediated
information rather than the cell number is critical for
the proper vascular specification. As demonstrated also by
the conditional expression of CKX, phenocopying wol, CK
is a sufficient and necessary signal to provide this information
during both embryonal and postembryonal root
meristem development (Mahonen et al. 2006). That fs
mutation is accompanied with increased levels of auxin and
ethylene (Fisher et al. 1996) might imply a hormonal origin
of wol complementation and suggest a role for CK/auxin/
ethylene interplay during embryonal radial root pattern
specification.
The role of CK in the embryonal specification of the root
meristem stem cells was recently described (Muller and
Sheen 2008). In the set of elegant experiments using CKresponsive
synthetic reporter, authors have shown that
output of CK signalling is antagonized by auxin. This effect
is mediated by auxin-inducible expressions of ARR7 and
ARR15 type-A response regulators acting as negative regulators
of CK signalling. In the absence of auxin, expression
of ARR7 and ARR15 are balanced with CK signalling levels
(CK induce expression of type-A ARRs, which in turn
inhibit CK signalling phosphorelay). However, auxinmediated
local expression of ARR7 and ARR15 bypasses the
CK feedback loop and counteracts CK signalling. In conditional
arr7 and arr15 double mutants, ectopic CK
phosphorelay output was detected, accompanied with
defects in root stem cell region and misexpression of SCR,
PLT1 and WUSCHEL_RELATED-HOMEOBOX 5 (WOX5)
genes (Muller and Sheen 2008). These results provide
insight into the molecular mechanism of long-known
antagonistic effects of CK and auxin interaction and introduce
the role of these interactions in root meristem
establishment during the early embryogenesis.
Biometric analysis on root growth (Beemster and Baskin
2000) demonstrated that CK reduces the relative elongation
rate and blocks the increase of the meristem size. In some
aspects, CK regulated root growth resembles typical ethylene-induced
inhibition. CK was found to stimulate
ethylene production and root growth of ethylene insensitive
mutants to be CK resistant (Cary et al. 1995). Moreover,
inhibitors of ethylene signalling and biosynthesis partially
relieve roots from CK inhibition. These results suggest that
part of the CK effects on root growth is mediated through
ethylene. Molecular characterization of the ACS5 and
ACS9 genes in ethylene overproduction (eto2 and eto3)
mutants revealed that dominant eto2 mutation does not
increase the specific activity of the ethylene biosynthesis
ACS5 enzyme, rather it increases the half-life of the protein.
Similarly, CK treatment was shown to enhance the
stability of ACS5 by a mechanism that is at least partially
independent of the eto2 mutation (Chae et al. 2003).
Altogether, rapid expansion of cells in the root transition
zone seems to be under the control of at least three hormonal
pathways––cytokinin, ethylene and auxin
downstream of this regulatory chain. Importantly, feedback
loop mechanisms comprising control of the CK biosynthesis
by auxin (Eklof et al. 1997; Nordstrom et al. 2004),
or the ethylene biosynthesis by auxin (Tsuchisaka and
Theologis 2004; Yang and Hoffman 1984) represent an
important part of the homeostatic mechanism.
Recently, Dello Ioio et al. (2007) have analysed the role
of CK in the root meristem formation and have demonstrated
that CK does not interfere with specification of the
QC and stem cell function, nor with the overall division
rate in the proximal meristem. CK affects primarily the rate
of meristematic cell differentiation, resulting in shortening
of the meristematic zone. Accordingly, depletion of CK by
overexpression of CKX or by mutation of three Arabidopsis
cytokinin biosynthesis genes ipt2,ipt3,ipt7 increases the
root meristem size (Dello Ioio et al. 2007; Werner et al.
2003). The role of CK signalling in longitudinal root patterning
has been further confirmed by the expansion of the
root meristem in the ahk3 and response regulator mutants
arr1 and arr12.
Important knowledge on the CK control mechanism on
the root meristem development has arisen from the targeted
depletion of CK in different root meristem tissue layers.
Depletion of CK restricted to the vasculature of the transition
zone was sufficient to reduce the rate of cell
differentiation of all other tissues and, thus, to diminish the
root meristem size. Such a type of non-cell autonomous
effect suggests that CK acts by antagonizing other signals.
As proposed by Dello Ioio et al. (2007), a candidate for
such a signalling molecule would be auxin, which as
described above, is critical for the control of cell division
and root meristem size. Application of auxin at low concentrations
causes an increase in the meristem size
(Beemster and Baskin 2000; Dello Ioio et al. 2007). On the
other hand, depletion of CK by CKX has no additional
effects on the meristem size in the auxin efflux carrier triple
mutant pin2,pin3,pin7. Thus, the balance between the auxin
and cytokinin pathways regulates important aspects of root
development and establishment and maintenance of the
meristem size. The molecular mechanisms are so far illusive,
although several modes of interaction are conceivable.
First, CK and auxin biosynthesis are dependent on each
other and perturbation in the abundance of one affects the
other. An increase in auxin concentration leads to a
decrease in the CK level (Eklof et al. 1997; Nordstrom
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et al. 2004), and slow inhibitory effect of CK on auxin
biosynthesis was described (Nordstrom et al. 2004). Auxin
has also been shown to contribute to the CK degradation
via stimulation of the CKX activity (Palni et al. 1988). In
contrast, expression of two genes for CK biosynthetic
enzymes AtIPT5 and AtIPT7 in Arabidopsis is induced by
exogenous auxin (Miyawaki et al. 2004).
Second, the activity of the polar auxin transport
machinery, the principal director of the auxin distribution
in the root meristem, might be modulated by CK. Recently,
CK has been shown to affect the local auxin gradient formation
and expression of PIN auxin efflux carriers during
lateral root development (Kuderova et al. 2008; Laplaze
et al. 2007).
Third, auxin and cytokinin can regulate a common set of
genes. A promising candidate for the downstream molecular
component is PROPORZ1 (PRZ1). This putative
transcriptional adaptor protein has been shown to be
essential for the developmental switch from cell proliferation
to differentiation in response to variations in auxin
and CK concentrations (Sieberer et al. 2003). Expression
of several other genes was found to be under control of
auxin and cytokinin. For example, transcription of the rootspecific
putative homeobox gene ATHB53 is differentially
regulated by auxin and CK (Son et al. 2005), and interestingly,
CK regulates also expression of genes of the auxin
signalling pathway (SHY2-2/IAA3, AXR3/IAA17 or SAURAC1)
(Rashotte et al. 2005).
Brassinosteroid: forget-me-not
Typically, effects of brassinosteroids (BRs) on root growth
strongly depend on the BR concentration used. Exogenous
BRs stimulate root growth at low concentrations, but have an
inhibitory effect at higher BR levels (Mussig et al. 2003).
BR-deficient mutants, such as dwarf1-6/(dwf1-6) and cabbage3/(cbb3)
(allelic to cpd), defective in brassinosteroid
biosynthesis (Kauschmann et al., 1996; Szekeres et al.,
1996), show shorter roots than wild-type plants (Mussig
et al. 2003). Root-specific BR-deficiency in brevis radix/
(brx) mutant causes reduced root growth due to reduction in
the meristem size, and mature cell size as well (Mouchel
et al. 2004). BRX, isolated as quantitative trait locus affecting
root growth in the Arabidopsis accession Umkirch-1
(Uk-1), is a member of a small gene family representing most
probably a novel class of transcriptional factors involved in
the regulation of expression of a rate-limiting enzyme in
brassinosteroid biosynthesis (Mouchel et al. 2006).
Transcriptome profile analyses in roots of two BR
mutants, dwf1-6 and (Mussig et al. 2003) and brx (Mouchel
et al. 2006), revealed a link between BR and the auxin
pathway in root development. Test of auxin response in brx
via microarray analysis showed that almost none of tested
auxin response genes responded normally to auxin in the
BR-deficient brx mutant, but this auxin responsiveness was
largely restored by brassinollide treatment. Accordingly,
expression of the auxin reporter DR5 (Sabatini et al. 1999;
Ulmasov et al. 1997) in brx was fully sensitized to auxin by
BR supply (Mouchel et al. 2006). Altogether, these results
suggested that optimal BR levels are rate limiting for
auxin-induced transcriptional responses. BR does not seem
to act through regulation of endogenous auxin content,
because as shown by Nakamura et al. (2003), BR did not
increase the endogenous auxin levels of either the control
plant or the BR-deficient mutant deetiolated2/det2. Furthermore,
the levels of AUX/IAA transcripts were lower in
the det2 mutant than in the control, even though endogenous
auxin levels were elevated in the det2 background
(Nakamura et al. 2003).
Accordingly, negative regulators of auxin signalling
IAA14 and IAA2 showed weaker expression in roots of
dwf1-6 (Fukaki et al. 2002; Mussig et al. 2003) and the
NIT3 gene, encoding enzyme involved in IAA biosynthesis
(Kutz et al. 2002) exhibited higher transcript level in the
dwf1-6 mutant background (Mussig et al. 2003).
Brassinosteroids are known to stimulate the production
of ethylene in shoots and roots (Arteca and Arteca 2001;
Schlagnhaufer and Arteca 1985; Yi et al. 1999). In line
with these observations, expression data point to a positive
BR effect on genes involved in ethylene biosynthesis and
ethylene response in roots (Mussig et al. 2003). Thus, part
of the BR inhibitory effect on root growth might be mediated
through ethylene. More detailed studies are needed to
dissect the ethylene effects in the context of BR action.
However, analysis of the auxin and ethylene resistant
mutants axr1 points to the existence of ethylene-independent
BR-regulated root growth (Clouse et al. 1993). A
direct BR-ethylene feedback loop might exist that specifically
interferes with BR transport, BR biosynthesis, or BR
responses.
Also another mutant in BR biosynthesis, sax1
(hypersensitive to abscisic acid and auxin), with roots
oversensitive to auxin and ABA suggests that BR interacts
with multiple hormonal pathways (Ephritikhine et al.
1999).
Gibberellins: you have to beat me
Although gibberellin (GA) has been recognized for a long
time mainly as a regulator of shoot growth, its important
role in the regulation of root growth has been demonstrated
as well. The GA-deficient mutant ga1-3 exhibits shorter
roots. Loss of DELLA proteins GAI and RGA, negative
inhibitors of GA signalling, suppress the ga1-3 root phenotype,
showing that GA pathway acts in the regulation of
root growth (Fu and Harberd 2003). An elegant set of
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123
experiments has recently been performed to map the site of
GA action for regulating root growth (Ubeda-Tomas et al.
2008). When gai, a mutant non-degradable DELLA protein,
was expressed in selected root tissues, the root growth was
retarded specifically when gai was expressed in endodermal
cells. These results demonstrated that the endodermis represents
the primary GA-responsive tissue and that
endodermal cell expansion is rate limiting for elongation of
other tissues and, therefore, of the root as a whole (UbedaTomas
et al. 2008). In work of Paquette and Benfey (2005)
also a role of GA in radial patterning of root meristem has
been revealed and GA shown to act as negative regulator of
the middle cortex formation—the third layer of the root
ground tissue rapidly differentiating to cortex.
GA stimulates growth by promoting the destruction of
DELLA proteins, a subfamily of the GRAS family of
putative transcriptional regulators (Dill et al. 2001; Fu and
Harberd 2003). Thus, DELLA proteins restrain the plant
growth, whereas GA relieves the DELLA-mediated growth
inhibition by targeting the DELLA proteins for destruction.
GA-mediated destabilization of DELLA proteins involves
GA-stimulated phosphorylation, polyubiquitination via a
specific SCF E3 ubiquitin ligase complex and subsequent
destruction in the 26S proteasome (Fu et al. 2002;
McGinnis et al. 2003; Sasaki et al. 2003).
As demonstrated by several laboratories, GA-regulated
root growth involves interaction with other hormonal
pathways, e.g. auxin (Fu and Harberd 2003), cytokinin
(Greenboim-Wainberg et al. 2005), ethylene (Achard et al.
2006) or ABA (Achard et al. 2006) and the regulation of
DELLA proteins stability might represent an important
cross-point.
GA and auxin pathways converge in roots to regulate
cell expansion and tissue differentiation. GA-induced root
elongation was inhibited by the removal of the shoot apex,
which is a major auxin source, and this effect was reversed
by auxin application suggesting that GA stimulation of root
elongation requires auxin. Moreover, application of the
auxin-transport inhibitor 1-N-naphthylphthalamic acid
(NPA), or a mutation in the auxin efflux carrier PIN1
attenuated the effect of GA on root elongation and on RGA
degradation in root cells. GA-induced RGA degradation
was also inhibited in the auxin resistant mutant axr1. These
observations indicate that auxin promotes the growth of
roots by enhancing the GA-induced destabilization of some
of the DELLA proteins (Fu and Harberd 2003). Thus, the
DELLA protein RGA seems to act as integrator of GA and
auxin signals in the root.
Positive regulation of GA biosynthesis by auxin might
be involved in these interactions. A stimulatory effect of
the auxin on GA biosynthesis was demonstrated and several
components of auxin signalling pathway seem to be
included in this regulation (Frigerio et al. 2006).
GA has been shown to antagonize ethylene inhibitory
effects on root growth (Achard et al. 2003). Ethylene
insensitive root growth of the gai rga GA-insensitive
mutant indicates that ethylene regulates root growth in a
DELLA-dependent manner. In agreement with this observation,
ethylene counteracted GA-induced destabilization
of the RGA protein in root cell nuclei. The effect of
ethylene on RGA stability was mimicked by the loss
of its signalling suppressor CONSTITUTIVE TRIPLE
RESPONSE1 (CTR1) (Guo and Ecker 2004), suggesting
that the ethylene’s RGA stabilizing signal is transduced via
a CTR1-dependent pathway (Achard et al. 2003).
Analysis of SPINDLY (SPY) gene revealed antagonistic
interaction of GA and CK in root growth (GreenboimWainberg
et al. 2005). Mutation of SPY results in phenotypes
resembling that of wild-type plants treated with
exogenous GA and overexpression of SPY produced phenotypes
consistent with a reduced GA action (Izhaki et al.
2001; Swain et al. 2001). This suggests that SPY functions
as a negative regulator of the GA-signal transduction.
Inhibition of root elongation by CK was greatly suppressed
in the spy mutant background, and accordingly, exogenous
application of GA antagonized the inhibitory effect of CK
on root growth. Both GA and spy interfered with the
induction of CK primary response gene ARR5. Thus, SPY
is a potential molecular component that integrates GA and
CK pathways in root growth and acts as a repressor of GA
responses and a positive regulator of CK signalling. Based
on the comparison of GA and CK sensitivities of spy
mutants, it seems that GA suppresses CK responses at least
partially via SPY (Greenboim-Wainberg et al. 2005).
In the shoot apical meristem KNOTTED-like homeobox
genes were shown to play an important role in the establishment
of the hormonal balance between CK and GA.
They activate CK biosynthesis and repress GA 20-oxidase
gene expression and, hence, GA biosynthesis, thus promoting
meristem activity (Jasinski et al. 2005; Yanai et al.
2005). Several members of this gene family were shown to
be expressed in distinct domains and cell types of the main
root (Truernit et al. 2006), but their role in the hormonal
interactions and its relevance for root growth regulation
remains to be examined in detail.
Abscisic acid: not only stress
The role of abscisic acid (ABA) in the regulation of root
growth is still not completely clear. However, recent
genetic and molecular studies started to unravel the
importance of ABA regulation in root meristem formation
and root growth. An example of genes involved in
ABA-mediated control of the root meristem is the TETRATRICOPEPTIDE-REPEAT
THIOREDOXIN-LIKE 1
(TTL1) gene. Mutation in TTL1 causes reduced root
Plant Mol Biol
123
elongation and disorganization of the root meristem. TTL1
mediates the sensitivity to ABA and to osmotic stress and
is supposed to participate in ABA signalling in Arabidopsis
(Rosado et al. 2006). ABA has been shown to rescue the
root meristem phenotype of Medicago mutant latd. latd
roots have disorganized root tip that is defective in meristem
organization, columella root cap formation and root
growth (Liang et al. 2007). latd mutants exhibit normal
ABA levels, but reduced sensitivity to ABA, suggesting
that LATD functions in the ABA signalling.
Multiple ABA effects are associated with ethylene action.
There are several hints that functional ethylene signalling is
necessary for root responses to ABA. The ABA effect on the
root growth was restrained by inhibitors of the ethylene
perception, but not by reduced ethylene biosynthesis, suggesting
that, in contrast to CK, ABA does not operate
through ethylene biosynthesis, as confirmed by the measurements
of ethylene production upon ABA treatment. Vice
versa, ethylene seems to inhibit root responsiveness to ABA
(Ghassemian et al. 2000). Close interplay of ABA and ethylene
in root development indicates era3 mutant identified in
a screen for ABA hypersensitive germination mutant. The
era3 mutation was found to be allelic to the ethylene
insensitive ein2 mutant (Beaudoin et al. 2000; Ghassemian
et al. 2000). Interestingly, the era3 roots are not only resistant
to CK and ethylene as previously shown for the ein2
mutant in ethylene signalling (Cary et al. 1995) but also to
ABA. Moreover, they are sensitive to auxin and accumulate
more ABA (Ghassemian et al. 2000). Thus, era3 represents
an important candidate to investigate ABA and ethylene
signalling interaction in the root development. The abi8/
eld1/kob1 mutant with altered ABA-responsive gene
expression was shown to be necessary for the meristematic
activity in the root (Brocard-Gifford et al. 2004). ABI8/
ELD1/KOB1 encodes a protein of unknown function and, in
contrast to most of the other ABA insensitive mutations, the
abi8 phenotype cannot be suppressed by inhibition of the
ethylene pathway. Thus, ABI8 might function in parallel or
downstream of the EIN2 and EIN3 components of the ethylene
signalling pathway (Brocard-Gifford et al. 2004).
The nhr1 mutation uncovers interaction between ABA
and auxin (Eapen et al. 2003). Semi-dominant nhr1
mutation was identified in a screen for lack of hydrotropic
root responses. NHR1 affects root meristem formation via
regulation of the QC, columella initials and root cap
specification and affects cell proliferation in the root
meristem. nhr1 shows reduced sensitivity to ABA, NAA
and to the auxin efflux inhibitor NPA. Authors hypothesize
that NHR1 is involved in the ABA-dependent mechanism
of efflux mediated auxin redistribution, allowing positive
hydrotropic response of the root (Eapen et al. 2003).
Similarly to ethylene, salt stress-induced ABA increases
the stability of DELLA negative regulators of the GA
pathway (Achard et al. 2006; Fu and Harberd 2003;
Vriezen et al. 2004). The quadruple DELLA mutant
gai,rga,rgl1,rgl2 is resistant to the growth-inhibitory
effects of ABA. Furthermore, EIN3, a negative regulator of
the ethylene signalling, was found to promote salt tolerance
via enhancement of the DELLA function (Achard et al.
2006). Thus, DELLA proteins integrate ABA and ethylene
signalling in the regulation of the root growth. As ABA and
ethylene signalling are involved in different abiotic and
biotic responses, this mechanism might mediate environmental
regulation of the root growth response (Achard
et al. 2006).
Recently, important connection between CK and ABA
signalling was described in Arabidopsis. Homologue of CK
receptors, sensory histidine kinase AHK1, was found to be
a positive regulator of drought and salt stress responses and
ABA signalling. In contrast, CK receptors AHK2, AHK3
and AHK4 were identified to be negative regulators of the
ABA signalling, acting in case of AHK2 and AHK3 via
negative regulation of many stress- and/or ABA-inducible
genes (Tran et al. 2007).
Conclusion
The current status of knowledge on root development
indisputably points out that a complex hormonal network
participates in the regulation of root formation and growth
from the moment of its initiation in the embryo. Essentially,
all hormonal pathways are involved and control
different developmental aspects of the root meristem formation.
Auxin seems to be the most universal factor acting
in all root developmental events (Dinneny and Benfey
2008; Galinha et al. 2007). CK has been shown to be a
critical factor in radial root patterning (Mahonen et al.
2006; Scheres et al. 1995), establishment of root stem cells
during early embryogenesis (Muller and Sheen 2008) and
establishment of the root meristem size by controlling the
balance between cell division and differentiation of cells
leaving the root meristem (Dello Ioio et al. 2007). Ethylene
and GA act primarily on the rapid elongation of cells
leaving the root meristem (Fu and Harberd 2003; Ruzicka
et al. 2007; Swarup et al. 2007; Ubeda-Tomas et al. 2008).
BR deficiency affects both the division activity of the root
meristem and rapid cell elongation (Mouchel et al. 2004),
and ABA mediates the environmental regulation of root
growth responses (Achard et al. 2006). Importantly, each
hormonal pathway functions in the context of the whole
hormonal network and they mutually modulate their
actions. Thus, for example, auxin regulated processes
require a minimal level of BR (Mouchel et al. 2006).
Maintenance of the root meristem size is balanced by
antagonistic activities of CK and auxin (Dello Ioio et al.
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123
2007), and the gibberellin pathway is differently modulated
by auxin and ethylene (Achard et al. 2003; Fu and Harberd
2003). Although our knowledge on the molecular components
and pathways that mediate developmental responses
to hormones has improved enormously in recent years,
molecular mechanisms standing behind their interactions
are poorly understood. However, from most of the recent
studies, it became obvious that diverse mechanisms of
hormonal interactions have evolved to coordinate activity
of hormonal pathways in certain developmental processes.
There are several examples of mutual regulations on the
level of hormone metabolism and distribution (Laplaze
et al. 2007; Stepanova et al. 2005; Stepanova et al. 2008;
Tsuchisaka and Theologis 2004). Transcriptional or posttranslational
control over the key molecular components of
signal transduction pathways by other hormonal signals is
another example of a cross-talk strategy (Fu and Harberd
2003; Chae et al. 2003; Muller and Sheen 2008). There are
rare cases in which activation of one hormonal pathway
might branch and stimulate transduction component of
another pathway (Hass et al. 2004). Hormonal signalling
pathways might also differentially regulate expression or
activity of common target gene (Chilley et al. 2006; Son
et al. 2005). Several other modes of hormonal interactions
could be predicted. Although we have no real evidence for
their existence today, they might be revealed in the future
years. In this context, we would like to note that although
sometimes experimental findings might lead to contradictory
conclusions on the mode of hormonal interactions
(Ferreira and Kieber 2005), these ‘‘inconsistencies’’ might
point to a very important feature of the hormone behaviour––its
action is extremely dependent on concentration
and developmental stage (Kuderova et al. 2008; Mussig
et al. 2003). It has been nicely demonstrated by Kuderova
et al. (2008) that the strength of the effects of temporal
pulses of endogenous CK via regulated expression of the
bacterial IPT depends on the developmental status of the
root. Consequently, the same hormone can, during one
developmental process, set up different interactions in
relation to the actual concentration and developmental
stage.
Recent investigations have created a good outline of
different possible modes of interactions between hormones,
which in combination with the fast progress in understanding
single hormonal pathways represents a promising
start to reveal concrete cross-talk molecular components,
which is the challenge of future research.
Acknowledgement We would like to thank Dr. Kamil Ruzicka and
Dr. Jiri Friml for critical reading of the manuscript and Martine De
Cock for help in preparing it. This work was supported by the Ministry
of Education, Youth and Sports of the Czech Republic (LC06034
and MSM0021622415) (JH).
References
Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003)
Ethylene regulates arabidopsis development via the modulation
of DELLA protein growth repressor function. Plant Cell
15:2816–2825. doi:10.1105/tpc.015685
Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T,
Van Der Straeten D, Peng J, Harberd NP (2006) Integration of
plant responses to environmentally activated phytohormonal
signals. Science 311:91–94. doi:10.1126/science.1118642
Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C,
Nussaume L, Noh YS, Amasino R, Scheres B (2004) The
PLETHORA genes mediate patterning of the Arabidopsis root
stem cell niche. Cell 119:109–120. doi:10.1016/j.cell.2004.
09.018
Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel
FM, Ecker JR (2003) Five components of the ethylene-response
pathway identified in a screen for weak ethylene-insensitive
mutants in Arabidopsis. Proc Natl Acad Sci USA 100:2992–
2997. doi:10.1073/pnas.0438070100
Arteca JM, Arteca RN (2001) Brassinosteroid-induced exaggerated
growth in hydroponically grown Arabidopsis plants. Physiol
Plant 112:104–112. doi:10.1034/j.1399-3054.2001.1120114.x
Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R, Bennett
M, Sandberg G, Bellini C (2000) The SUR2 gene of Arabidopsis
thaliana encodes the cytochrome P450 CYP83B1, a modulator of
auxin homeostasis. Proc Natl Acad Sci USA 97:14819–14824.
doi:10.1073/pnas.260502697
Beaudoin N, Serizet C, Gosti F, Giraudat J (2000) Interactions
between abscisic acid and ethylene signaling cascades. Plant Cell
12:1103–1115
Beemster GT, Baskin TI (2000) Stunted plant 1 mediates effects of
cytokinin, but not of auxin, on cell division and expansion in the
root of Arabidopsis. Plant Physiol 124:1718–1727. doi:10.1104/
pp.124.4.1718
Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT,
Aeschbacher RA (1993) Root development in Arabidopsis: four
mutants with dramatically altered root morphogenesis. Development
119:57–70
Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R (2001)
The PINOID protein kinase regulates organ development in
Arabidopsis by enhancing polar auxin transport. Development
128:4057–4067
Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D,
Jurgens G, Friml J (2003) Local, efflux-dependent auxin
gradients as a common module for plant organ formation. Cell
115:591–602. doi:10.1016/S0092-8674(03)00924-3
Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA,
Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1
gene: a permease-like regulator of root gravitropism. Science
273:948–950. doi:10.1126/science.273.5277.948
Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun
B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J,
Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer
WA, Murphy AS (2007) Interactions among PIN-FORMED and
P-glycoprotein auxin transporters in Arabidopsis. Plant Cell
19:131–147. doi:10.1105/tpc.106.040782
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in
plants. Annu Rev Cell Dev Biol 16:1–18. doi:10.1146/annurev.
cellbio.16.1.1
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J,
Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin
efflux facilitator network controls growth and patterning in
Arabidopsis roots. Nature 433:39–44. doi:10.1038/nature03184
Plant Mol Biol
123
Brocard-Gifford I, Lynch TJ, Garcia ME, Malhotra B, Finkelstein RR
(2004) The Arabidopsis thaliana ABSCISIC ACID-INSENSITIVE8
encodes a novel protein mediating abscisic acid and
sugar responses essential for growth. Plant Cell 16:406–421. doi:
10.1105/tpc.018077
Camilleri C, Azimzadeh J, Pastuglia M, Bellini C, Grandjean O,
Bouchez D (2002) The Arabidopsis TONNEAU2 gene encodes a
putative novel protein phosphatase 2A regulatory subunit
essential for the control of the cortical cytoskeleton. Plant Cell
14:833–845. doi:10.1105/tpc.010402
Cano-Delgado A, Yin Y, Yu C, Vafeados D, Mora-Garcia S, Cheng
JC, Nam KH, Li J, Chory J (2004) BRL1 and BRL3 are novel
brassinosteroid receptors that function in vascular differentiation
in Arabidopsis. Development 131:5341–5351. doi:10.1242/dev.
01403
Cary AJ, Liu W, Howell SH (1995) Cytokinin action is coupled to
ethylene in its effects on the inhibition of root and hypocotyl
elongation in Arabidopsis thaliana seedlings. Plant Physiol
107:1075–1082. doi:10.1104/pp.107.4.1075
Casson SA, Chilley PM, Topping JF, Evans IM, Souter MA, Lindsey
K (2002) The POLARIS gene of Arabidopsis encodes a
predicted peptide required for correct root growth and leaf
vascular patterning. Plant Cell 14:1705–1721. doi:10.1105/tpc.
002618
Clouse SD, Hall AF, Langford M, Mcmorris TC, Baker ME (1993)
Physiological and molecular effects of brassinosteroids on
Arabidopsis-Thaliana. J Plant Growth Regul 12:61–66. doi:
10.1007/BF00193234
Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher
KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An
evolutionarily conserved mechanism delimiting SHR movement
defines a single layer of endodermis in plants. Science 316:421–
425. doi:10.1126/science.1139531
Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E,
Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine
Arabidopsis root-meristem size by controlling cell
differentiation. Curr Biol 17:678–682. doi:10.1016/j.cub.2007.
02.047
Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein
TIR1 is an auxin receptor. Nature 435:441–445. doi:10.1038/
nature03543
Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y,
Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The
SCARECROW gene regulates an asymmetric cell division that
is essential for generating the radial organization of the
Arabidopsis root. Cell 86:423–433. doi:10.1016/S0092-8674(00)
80115-4
Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for
gibberellin-induced degradation of RGA. Proc Natl Acad Sci
USA 98:14162–14167. doi:10.1073/pnas.251534098
Dinneny JR, Benfey PN (2008) Plant stem cell niches: standing the
test of time. Cell 132:553–557. doi:10.1016/j.cell.2008.02.001
Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K,
Scheres B (1993) Cellular organisation of the Arabidopsis
thaliana root. Development 119:71–84
Eapen D, Barroso ML, Campos ME, Ponce G, Corkidi G, Dubrovsky
JG, Cassab GI (2003) A no hydrotropic response root mutant that
responds positively to gravitropism in Arabidopsis. Plant Physiol
131:536–546. doi:10.1104/pp.011841
Eklof S, Astot C, Blackwell J, Moritz T, Olsson O, Sandberg G
(1997) Auxin-cytokinin interactions in wild-type and transgenic
tobacco. Plant Cell Physiol 38:225–235
Ephritikhine G, Pagant S, Fujioka S, Takatsuto S, Lapous D, Caboche
M, Kendrick RE, Barbier-Brygoo H (1999) The sax1 mutation
defines a new locus involved in the brassinosteroid biosynthesis
pathway in Arabidopsis thaliana. Plant J 18:315–320. doi:
10.1046/j.1365-313X.1999.00455.x
Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant
Biol 8:518–525. doi:10.1016/j.pbi.2005.07.013
Fisher RH, Barton MK, Cohen JD, Cooke TJ (1996) Hormonal
studies of fass, an Arabidopsis mutant that is altered in organ
elongation. Plant Physiol 110:1109–1121
Frigerio M, Alabadi D, Perez-Gomez J, Garcia-Carcel L, Phillips AL,
Hedden P, Blazquez MA (2006) Transcriptional regulation of
gibberellin metabolism genes by auxin signaling in Arabidopsis.
Plant Physiol 142:553–563. doi:10.1104/pp.106.084871
Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K,
Woody S, Sandberg G, Scheres B, Jurgens G, Palme K (2002a)
AtPIN4 mediates sink-driven auxin gradients and root patterning
in Arabidopsis. Cell 108:661–673. doi:10.1016/S0092-8674(02)
00656-6
Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002b)
Lateral relocation of auxin efflux regulator PIN3 mediates
tropism in Arabidopsis. Nature 415:806–809
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T,
Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients
establish the apical–basal axis of Arabidopsis. Nature 426:147–
153. doi:10.1038/nature02085
Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by
modulating gibberellin response. Nature 421:740–743. doi:
10.1038/nature01387
Fu X, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng J,
Harberd NP (2002) Gibberellin-mediated proteasome-dependent
degradation of the barley DELLA protein SLN1 repressor. Plant
Cell 14:3191–3200. doi:10.1105/tpc.006197
Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root
formation is blocked by a gain-of-function mutation in the
SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–
168. doi:10.1046/j.0960-7412.2001.01201.x
Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R,
Scheres B (2007) PLETHORA proteins as dose-dependent
master regulators of Arabidopsis root development. Nature
449:1053–1057. doi:10.1038/nature06206
Galweiler L, Guan C, Muller A, Wisman E, Mendgen K, Yephremov
A, Palme K (1998) Regulation of polar auxin transport by
AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230.
doi:10.1126/science.282.5397.2226
Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y,
McCourt P (2000) Regulation of abscisic acid signaling by the
ethylene response pathway in Arabidopsis. Plant Cell 12:1117–
1126
Greenboim-Wainberg Y, Maymon I, Borochov R, Alvarez J,
Olszewski N, Ori N, Eshed Y, Weiss D (2005) Cross talk
between gibberellin and cytokinin: the Arabidopsis GA response
inhibitor SPINDLY plays a positive role in cytokinin signaling.
Plant Cell 17:92–102. doi:10.1105/tpc.104.028472
Guo H, Ecker JR (2004) The ethylene signaling pathway: new
insights. Curr Opin Plant Biol 7:40–49. doi:10.1016/j.pbi.2003.
11.011
Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The
Arabidopsis BODENLOS gene encodes an auxin response
protein inhibiting MONOPTEROS-mediated embryo patterning.
Genes Dev 16:1610–1615. doi:10.1101/gad.229402
Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS
encodes a transcription factor mediating embryo axis formation
and vascular development. EMBO J 17:1405–1411. doi:
10.1093/emboj/17.5.1405
Hass C, Lohrmann J, Albrecht V, Sweere U, Hummel F, Yoo SD,
Hwang I, Zhu T, Schafer E, Kudla J, Harter K (2004) The
response regulator 2 mediates ethylene signalling and hormone
Plant Mol Biol
123
signal integration in Arabidopsis. EMBO J 23:3290–3302. doi:
10.1038/sj.emboj.7600337
Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena
G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene
controls radial patterning of the Arabidopsis root through radial
signaling. Cell 101:555–567. doi:10.1016/S0092-8674(00)
80865-X
Helliwell CA, Sheldon CC, Olive MR, Walker AR, Zeevaart JA,
Peacock WJ, Dennis ES (1998) Cloning of the Arabidopsis entkaurene
oxidase gene GA3. Proc Natl Acad Sci USA 95:9019–
9024. doi:10.1073/pnas.95.15.9019
Hewelt A, Prinsen E, Schell J, Van Onckelen H, Schmulling T (1994)
Promoter tagging with a promoterless ipt gene leads to
cytokinin-induced phenotypic variability in transgenic tobacco
plants:implications of gene dosage effects. Plant J 6:879–891.
doi:10.1046/j.1365-313X.1994.6060879.x
Higuchi M, Pischke MS, Mahonen AP, Miyawaki K, Hashimoto Y,
Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta
Y, Sussman MR, Kakimoto T (2004) In planta functions of the
Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA
101:8821–8826. doi:10.1073/pnas.0402887101
Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW,
Maxwell BB, Perdue TD, Schaller GE, Alonso JM, Ecker JR,
Kieber JJ (2006) The Arabidopsis histidine phosphotransfer
proteins are redundant positive regulators of cytokinin signaling.
Plant Cell 18:3073–3087. doi:10.1105/tpc.106.045674
Chae HS, Faure F, Kieber JJ (2003) The eto1, eto2, and eto3
mutations and cytokinin treatment increase ethylene biosynthesis
in Arabidopsis by increasing the stability of ACS protein. Plant
Cell 15:545–559. doi:10.1105/tpc.006882
Chilley PM, Casson SA, Tarkowski P, Hawkins N, Wang KL, Hussey
PJ, Beale M, Ecker JR, Sandberg GK, Lindsey K (2006) The
POLARIS peptide of Arabidopsis regulates auxin transport and
root growth via effects on ethylene signaling. Plant Cell
18:3058–3072. doi:10.1105/tpc.106.040790
Izhaki A, Swain SM, Tseng TS, Borochov A, Olszewski NE, Weiss D
(2001) The role of SPY and its TPR domain in the regulation of
gibberellin action throughout the life cycle of Petunia hybrida
plants. Plant J 28:181–190. doi:10.1046/j.1365-313X.2001.
01144.x
Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A,
Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is
mediated by coordinate regulation of cytokinin and gibberellin
activities. Curr Biol 15:1560–1565. doi:10.1016/j.cub.2005.07.023
Kim GT, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S,
Tsukaya H (2005) CYP90C1 and CYP90D1 are involved in
different steps in the brassinosteroid biosynthesis pathway in
Arabidopsis thaliana. Plant J 41:710–721. doi:10.1111/
j.1365-313X.2004.02330.x
Knox K, Grierson CS, Leyser O (2003) AXR3 and SHY2 interact to
regulate root hair development. Development 130:5769–5777.
doi:10.1242/dev.00659
Kuderova A, Urbankova I, Valkova M, Malbeck J, Nemethova D and
Hejatko J (2008) Effects of conditional IPT-dependent cytokinin
overproduction on root architecture of Arabidopsis seedlings.
Plant Cell Physiol 49:570–582
Kutz A, Muller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW
(2002) A role for nitrilase 3 in the regulation of root morphology
in sulphur-starving Arabidopsis thaliana. Plant J 30:95–106. doi:
10.1046/j.1365-313X.2002.01271.x
Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R,
Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, Offringa
R, Graham N, Doumas P, Friml J, Bogusz D, Beeckman T,
Bennett M (2007) Cytokinins act directly on lateral root founder
cells to inhibit root initiation. Plant Cell 19:3889–3900. doi:
10.1105/tpc.107.055863
Le J, Vandenbussche F, Van Der Straeten D, Verbelen JP (2001) In
the early response of Arabidopsis roots to ethylene, cell
elongation is up- and down-regulated and uncoupled from
differentiation. Plant Physiol 125:519–522. doi:10.1104/pp.125.
2.519
Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd
NP, Peng J (2002) Gibberellin regulates Arabidopsis seed
germination via RGL2, a GAI/RGA-like gene whose expression
is up-regulated following imbibition. Genes Dev 16:646–658.
doi:10.1101/gad.969002
Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I,
Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B,
Benfey PN (2006) Whole-genome analysis of the SHORTROOT
developmental pathway in Arabidopsis. PLoS Biol
4:e143. doi:10.1371/journal.pbio.0040143
Leyser HM, Pickett FB, Dharmasiri S, Estelle M (1996) Mutations
in the AXR3 gene of Arabidopsis result in altered auxin
response including ectopic expression from the SAUR-AC1
promoter. Plant J 10:403–413. doi:10.1046/j.1365-313x.1996.
10030403.x
Li J, Dai X, Zhao Y (2006a) A role for auxin response factor 19 in
auxin and ethylene signaling in Arabidopsis. Plant Physiol
140:899–908. doi:10.1104/pp.105.070987
Li X, Mo X, Shou H, Wu P (2006b) Cytokinin-mediated cell cycling
arrest of pericycle founder cells in lateral root initiation of
Arabidopsis. Plant Cell Physiol 47:1112–1123. doi:10.1093/pcp/
pcj082
Liang X, Abel S, Keller JA, Shen NF, Theologis A (1992) The
1-aminocyclopropane–1-carboxylate synthase gene family of
Arabidopsis thaliana. Proc Natl Acad Sci USA 89:11046–11050.
doi:10.1073/pnas.89.22.11046
Liang Y, Mitchell DM, Harris JM (2007) Abscisic acid rescues the
root meristem defects of the Medicago truncatula latd mutant.
Dev Biol 304:297–307. doi:10.1016/j.ydbio.2006.12.037
Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a rootspecific
protein involved in auxin transport, is required for
gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187.
doi:10.1101/gad.12.14.2175
Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN,
Helariutta Y (2000) A novel two-component hybrid molecule
regulates vascular morphogenesis of the Arabidopsis root. Genes
Dev 14:2938–2943. doi:10.1101/gad.189200
Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K,
Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y
(2006) Cytokinin signaling and its inhibitor AHP6 regulate cell
fate during vascular development. Science 311:94–98. doi:
10.1126/science.1118875
McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP,
Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a
putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell
15:1120–1130. doi:10.1105/tpc.010827
Medford JI, Horgan R, El-Sawi Z, Klee HJ (1989) Alterations of
Endogenous Cytokinins in Transgenic Plants Using a Chimeric
Isopentenyl Transferase Gene. Plant Cell 1:403–413
Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression
of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis:
tissue specificity and regulation by auxin, cytokinin,
and nitrate. Plant J 37:128–138. doi:10.1046/j.1365-313X.
2003.01945.x
Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation
in Arabidopsis identifies BREVIS RADIX, a novel regulator of
cell proliferation and elongation in the root. Genes Dev 18:700–
714. doi:10.1101/gad.1187704
Mouchel CF, Osmont KS, Hardtke CS (2006) BRX mediates
feedback between brassinosteroid levels and auxin signalling
in root growth. Nature 443:458–461. doi:10.1038/nature05130
Plant Mol Biol
123
Muller B and Sheen J (2008) Cytokinin and auxin interaction in root
stem-cell specification during early embryogenesis. Nature
453:1094–1097
Mussig C, Shin GH, Altmann T (2003) Brassinosteroids promote root
growth in Arabidopsis. Plant Physiol 133:1261–1271. doi:
10.1104/pp.103.028662
Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M,
Reed JW (2000) AXR2 encodes a member of the Aux/IAA
protein family. Plant Physiol 123:563–574. doi:10.1104/pp.123.
2.563
Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular
movement of the putative transcription factor SHR in root
patterning. Nature 413:307–311. doi:10.1038/35095061
Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T,
Shimada Y, Yoshida S (2003) Brassinolide induces IAA5,
IAA19, and DR5, a synthetic auxin response element in
Arabidopsis, implying a cross talk point of brassinosteroid and
auxin signaling. Plant Physiol 133:1843–1853. doi:10.1104/
pp.103.030031
Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004)
Histidine kinase homologs that act as cytokinin receptors possess
overlapping functions in the regulation of shoot and root growth
in Arabidopsis. Plant Cell 16:1365–1377. doi:10.1105/tpc.
021477
Nordstrom A, Tarkowski P, Tarkowska D, Norbaek R, Astot C,
Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin
biosynthesis in Arabidopsis thaliana: a factor of potential
importance for auxin-cytokinin-regulated development. Proc
Natl Acad Sci USA 101:8039–8044. doi:10.1073/pnas.040
2504101
Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang
C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H,
Smith A, Yu G, Theologis A (2005) Functional genomic analysis
of the AUXIN RESPONSE FACTOR gene family members in
Arabidopsis thaliana: unique and overlapping functions of ARF7
and ARF19. Plant Cell 17:444–463. doi:10.1105/tpc.104.028316
Ortega-Martinez O, Pernas M, Carol RJ, Dolan L (2007) Ethylene
modulates stem cell division in the Arabidopsis thaliana root.
Science 317:507–510. doi:10.1126/science.1143409
Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR,
Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis
A (2005) Functional genomic analysis of the AUXIN/INDOLE–3ACETIC
ACID gene family members in Arabidopsis thaliana.
Plant Cell 17:3282–3300. doi:10.1105/tpc.105.036723
Palni LMS, Burch L, Horgan R (1988) The Effect of Auxin
Concentration on Cytokinin Stability and Metabolism. Planta
174:231–234. doi:10.1007/BF00394775
Paquette AJ, Benfey PN (2005) Maturation of the ground tissue of the
root is regulated by gibberellin and SCARECROW and requires
SHORT-ROOT. Plant Physiol 138:636–640. doi:10.1104/pp.104.
058362
Petra´sˇek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova´
D, Wisniewska J, Tadele Z, Kubes M, Covanova´ M, Dhonukshe
P, Skupa P, Benkova´ E, Perry L, Krecek P, Lee OR, Fink GR,
Geisler M, Murphy AS, Luschnig C, Zazı´malova´ E, Friml J
(2006) PIN proteins perform a rate-limiting function in cellular
auxin efflux Science 312:914–918. doi:10.1126/science.1123542
Pickett FB, Wilson AK, Estelle M (1990) The aux1 Mutation of
Arabidopsis Confers Both Auxin and Ethylene Resistance. Plant
Physiol 94:1462–1466
Rahman A, Amakawa T, Goto N, Tsurumi S (2001) Auxin is a
positive regulator for ethylene-mediated response in the growth
of arabidopsis roots. Plant and Cell Physiology 42:301–307. doi:
10.1093/pcp/pce035
Rahman A, Bannigan A, Sulaman W, Pechter P, Blancaflor EB,
Baskin TI (2007) Auxin, actin and growth of the Arabidopsis
thaliana primary root. Plant J 50:514–528. doi:10.1111/j.1365-
313X.2007.03068.x
Rashotte AM, Chae HS, Maxwell BB, Kieber JJ (2005) The
interaction of cytokinin with other signals. Physiologia Plantarum
123:184–194. doi:10.1111/j.1399-3054.2005.00445.x
Riefler M, Novak O, Strnad M, Schmulling T (2006) Arabidopsis
cytokinin receptor mutants reveal functions in shoot growth, leaf
senescence, seed size, germination, root development, and
cytokinin metabolism. Plant Cell 18:40–54. doi:10.1105/tpc.
105.037796
Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR (1995)
Genetic analysis of ethylene signal transduction in Arabidopsis
thaliana: five novel mutant loci integrated into a stress response
pathway. Genetics 139:1393–1409
Rosado A, Schapire AL, Bressan RA, Harfouche AL, Hasegawa PM,
Valpuesta V, Botella MA (2006) The Arabidopsis tetratricopeptide
repeat-containing protein TTL1 is required for osmotic
stress responses and abscisic acid sensitivity. Plant Physiol
142:1113–1126. doi:10.1104/pp.106.085191
Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J,
Benkova E (2007) Ethylene regulates root growth through
effects on auxin biosynthesis and transport-dependent auxin
distribution. Plant Cell 19:2197–2212. doi:10.1105/tpc.107.
052126
Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J,
Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999)
An auxin-dependent distal organizer of pattern and polarity in the
Arabidopsis root. Cell 99:463–472. doi:10.1016/S0092-8674(00)
81535-4
Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K,
Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M,
Matsuoka M (2003) Accumulation of phosphorylated repressor
for gibberellin signaling in an F-box mutant. Science 299:1896–
1898. doi:10.1126/science.1081077
Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S
(2003) Organ-specific expression of brassinosteroid-biosynthetic
genes and distribution of endogenous brassinosteroids in Arabidopsis.
Plant Physiol 131:287–297. doi:10.1104/pp.013029
Scheres B, Dilaurenzio L, Willemsen V, Hauser MT, Janmaat K,
Weisbeek P, Benfey PN (1995) Mutations Affecting the Radial
Organization of the Arabidopsis Root Display Specific Defects
Throughout the Embryonic Axis. Development 121:53–62
Schlagnhaufer CD, Arteca RN (1985) Brassinosteroid-Induced Epinasty
in Tomato Plants. Plant Physiol 78:300–303
Sieberer T, Hauser MT, Seifert GJ, Luschnig C (2003) PROPORZ1, a
putative Arabidopsis transcriptional adaptor protein, mediates
auxin and cytokinin signals in the control of cell proliferation.
Curr Biol 13:837–842. doi:10.1016/S0960-9822(03)00327-0
Smigocki AC (1991) Cytokinin content and tissue distribution in
plants transformed by a reconstructed isopentenyl transferase
gene. Plant Mol Biol 16:105–115. doi:10.1007/BF00017921
Son O, Cho HY, Kim MR, Lee H, Lee MS, Song E, Park JH, Nam
KH, Chun JY, Kim HJ, Hong SK, Chung YY, Hur CG, Cho HT,
Cheon CI (2005) Induction of a homeodomain-leucine zipper
gene by auxin is inhibited by cytokinin in Arabidopsis roots.
Biochem Biophys Res Commun 326:203–209. doi:10.1016/
j.bbrc.2004.11.014
Stepanova AN, Hoyt JM, Hamilton AA, Alonso JM (2005) A Link
between ethylene and auxin uncovered by the characterization of
two root-specific ethylene-insensitive mutants in Arabidopsis.
Plant Cell 17:2230–2242. doi:10.1105/tpc.105.033365
Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel
interactions between ethylene and auxin in Arabidopsis roots.
Plant Cell 19:2169–2185. doi:10.1105/tpc.107.052068
Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY,
Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1Plant
Mol Biol
123
mediated auxin biosynthesis is essential for hormone crosstalk
and plant development. Cell 133:177–191. doi:10.1016/j.cell.
2008.01.047
Swain SM, Tseng TS, Olszewski NE (2001) Altered expression of
SPINDLY affects gibberellin response and plant development.
Plant Physiol 126:1174–1185. doi:10.1104/pp.126.3.1174
Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT,
Sandberg G, Bhalerao R, Ljung K, Bennett MJ (2007) Ethylene
upregulates auxin biosynthesis in Arabidopsis seedlings to
enhance inhibition of root cell elongation. Plant Cell 19:2186–
2196. doi:10.1105/tpc.107.052100
Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno
JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballare
CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of
auxin via a new tryptophan-dependent pathway is required for
shade avoidance in plants. Cell 133:164–176. doi:10.1016/
j.cell.2008.01.049
Tian Q, Reed JW (1999) Control of auxin-regulated root development
by the Arabidopsis thaliana SHY2/IAA3 gene. Development
126:711–721
To JP, Haberer G, Ferreira FJ, Deruere J, Mason MG, Schaller GE,
Alonso JM, Ecker JR, Kieber JJ (2004) Type-A Arabidopsis
response regulators are partially redundant negative regulators of
cytokinin signaling. Plant Cell 16:658–671. doi:10.1105/tpc.
018978
Torres-Ruiz RA, Jurgens G (1994) Mutations in the FASS gene
uncouple pattern formation and morphogenesis in Arabidopsis
development. Development 120:2967–2978
Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K,
Yamaguchi-Shinozaki K (2007) Functional analysis of AHK1/
ATHK1 and cytokinin receptor histidine kinases in response to
abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl
Acad Sci USA 104:20623–20628. doi:10.1073/pnas.0706547105
Truernit E, Siemering KR, Hodge S, Grbic V, Haseloff J (2006) A
map of KNAT gene expression in the Arabidopsis root. Plant
Mol Biol 60:1–20. doi:10.1007/s11103-005-1673-9
Tsuchisaka A, Theologis A (2004) Unique and overlapping expression
patterns among the Arabidopsis 1-amino-cyclopropane–1carboxylate
synthase gene family members. Plant Physiol
136:2982–3000. doi:10.1104/pp.104.049999
Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster
GT, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in
Arabidopsis requires gibberellin/DELLA signalling in the endodermis.
Nat Cell Biol 10:625–628. doi:10.1038/ncb1726
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA
proteins repress expression of reporter genes containing natural
and highly active synthetic auxin response elements. Plant Cell
9:1963–1971
van den Berg C, Weisbeek P, Scheres B (1998) Cell fate and cell
differentiation status in the Arabidopsis root. Planta 205:483–
491. doi:10.1007/s004250050347
Vriezen WH, Achard P, Harberd NP, Van Der Straeten D (2004)
Ethylene-mediated enhancement of apical hook formation in
etiolated Arabidopsis thaliana seedlings is gibberellin dependent.
Plant J 37:505–516. doi:10.1046/j.1365-313X.2003.01975.x
Watt FM, Hogan BL (2000) Out of Eden: stem cells and their niches.
Science 287:1427–1430. doi:10.1126/science.287.5457.1427
Weijers D, Benkova E, Jager KE, Schlereth A, Hamann T, Kientz M,
Wilmoth JC, Reed JW, Jurgens G (2005) Developmental
specificity of auxin response by pairs of ARF and Aux/IAA
transcriptional regulators. EMBO J 24:1874–1885. doi:10.1038/
sj.emboj.7600659
Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M,
Jurgens G (2006) Auxin triggers transient local signaling for cell
specification in Arabidopsis embryogenesis. Dev Cell 10:265–
270. doi:10.1016/j.devcel.2005.12.001
Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B
(2007) Arabidopsis JACKDAW and MAGPIE zinc finger
proteins delimit asymmetric cell division and stabilize tissue
boundaries by restricting SHORT-ROOT action. Genes Dev
21:2196–2204. doi:10.1101/gad.440307
Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative
regulator of gibberellin responses. Plant Cell 14:87–100. doi:
10.1105/tpc.010325
Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H,
Schmulling T (2003) Cytokinin-deficient transgenic Arabidopsis
plants show multiple developmental alterations indicating
opposite functions of cytokinins in the regulation of shoot and
root meristem activity. Plant Cell 15:2532–2550. doi:10.1105/
tpc.014928
Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant
mutation in Arabidopsis confers resistance to auxin, ethylene and
abscisic acid. Mol Gen Genet 222:377–383. doi:10.1007/BF006
33843
Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G,
Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate
cytokinin biosynthesis. Curr Biol 15:1566–1571. doi:10.1016/
j.cub.2005.07.060
Yang SF, Hoffman NE (1984) Ethylene Biosynthesis and Its
Regulation in Higher-Plants. Annual Review of Plant Physiology
and Plant Molecular Biology 35:155–189. doi:10.1146/annurev.
arplant.35.1.155
Yang S, Yu H, Xu Y, Goh CJ (2003) Investigation of cytokinindeficient
phenotypes in Arabidopsis by ectopic expression of
orchid DSCKX1. FEBS Lett 555:291–296. doi:10.1016/S0014-
5793(03)01259-6
Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E (2006)
High-affinity auxin transport by the AUX1 influx carrier protein.
Curr Biol 16:1123–1127
Yi HC, Joo S, Nam KH, Lee JS, Kang BG, Kim WT (1999) Auxin
and brassinosteroid differentially regulate the expression of three
members of the 1-aminocyclopropane-1-carboxylate synthase
gene family in mung bean (Vigna radiata L.). Plant Mol Biol
41:443–454. doi:10.1023/A:1006372612574
Plant Mol Biol
123