Article

Journal of Experimental Botany
doi:10.1093/jxb/eru534
Review Paper
Plant hormone cross-talk: the pivot of root growth
Elena Pacifici*, Laura Polverari* and Sabrina Sabatini†
Department of Biology and Biotechnology, Laboratory of Functional Genomics and Proteomics of Model Systems, University of Rome
Sapienza, P.le Aldo Moro 5, 00185 Rome, Italy
*
These authors contributed equally to this work
†
To whom correspondence should be addressed. E-mail: sabrina.sabatini@uniroma1.it
Received 13 November 2014; Revised 4 December 2014; Accepted 10 December 2014
Abstract
Root indeterminate growth and its outstanding ability to produce new tissues continuously make this organ a highly
dynamic structure able to respond promptly to external environmental stimuli. Developmental processes therefore
need to be finely tuned, and hormonal cross-talk plays a pivotal role in the regulation of root growth. In contrast to
what happens in animals, plant development is a post-embryonic process. A pool of stem cells, placed in a niche at
the apex of the meristem, is a source of self-renewing cells that provides cells for tissue formation. During the first
days post-germination, the meristem reaches its final size as a result of a balance between cell division and cell differ-
entiation. A complex network of interactions between hormonal pathways co-ordinates such developmental inputs. In
recent years, by means of molecular and computational approaches, many efforts have been made aiming to define
the molecular components of these networks. In this review, we focus our attention on the molecular mechanisms at
the basis of hormone cross-talk during root meristem size determination.
Key words: Auxin, cell differentiation, cell division, cytokinin, gibberellin, root meristem.
Introduction
Plants have the extraordinary capability of being potentially
‘immortal’. Indeed, there are plants which have been liv-
ing for several hundreds of years, and death occurs due to
external factors, such as environmental stresses, diseases, or
pathogen infection. This long life expectancy is mainly due
to their capacity to produce new tissues and organs through-
out their life thanks to the activities of long-lasting stem cells.
Plant indeterminate growth and development are predomi-
nantly post-embryonic processes taking place in the meris-
tems, where stem cells self-renew and produce daughter cells
that differentiate and give rise to different tissues and organ
structures (reviewed in Heidstra and Sabatini, 2014). As in
animals, plant stem cells are organized in stem cell niches
(SCNs). In the root of the Arabidopsis thaliana model plant,
the SCN is located at the apex of the meristem where stem
cells surround the organizer, the quiescence centre (QC), gen-
erating daughter cells (Heidstra and Sabatini, 2014). These
cells undergo additional division in the proximal meristem
(PM), and differentiate at the distal meristem transition zone
(TZ) that encompasses the boundary between dividing and
differentiating cells in the different cell files (Dello Ioio et al.,
2007). For meristem maintenance, and therefore for continu-
ous root growth, the rate of cell differentiation must equal
the rate of generation of new cells. The plant root is thus a
highly dynamic structure and the mechanisms that ensured
its activity need to be finely regulated. Hormones are among
the major endogenous regulators of root growth. Each hor-
mone such as auxin, cytokinin, gibberellin, brassinosteroids,
abscisic acid, and strigolactones has its specific biosynthetic
and signal transduction pathway, and much evidence has now
been collected showing that correct root growth depends on
their cross-talk. In the last few years many efforts have been
made to elucidate these complex networks. In this review,
we fist summarize current knowledge on the molecular
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of 9 | Pacifici et al.
mechanism at the basis of hormone biosynthesis, transport,
and signalling, and then discuss recent findings on hormo-
nal cross-talk, focusing our attention on primary root growth
and in particular on how hormonal cross-talk controls root
meristem size.
Auxin
‘Auxein’ is the word that the ancient Greeks used for ‘to
grow’, and in 1931 Kögl and Haagen-Smit coined the term
auxin for the substance they observed to be able to modulate
plant growth (Kögl and Haagen-Smit, 1931). Since then many
efforts have been made to try to elucidate the molecular play-
ers involved in auxin activity during plant development. The
bioactive auxin is indole-3-acetic acid (IAA) (Thimann, 1977).
IAA is a weak acid (pK=5.4) existing in a plant as a free form
or conjugated to a sugar or amino acid for degradation or
storage (Ljung et al., 2002). IAA biosynthesis is divided into
two different pathways: the trytophan-dependent and tryp-
tophan-independent pathways. The tryptophan-independent
pathway is poorly understood, but indole-3-glycerol phos-
phate (IGP) or indole are thought to be the primary precur-
sors of IAA biosynthesis (Zhang et al., 2008). On the other
hand, the biosynthetic pathway that has the amino acid tryp-
tophan as the IAA precursor has been widely investigated and
now the molecular players are clearly elucidated (reviewed in
Zhao, 2014). Tryptophan is converted into IAA through an
enzymatic cascade in a two-step pathway in which the inter-
mediate is indole-3-pyruvate (IPA) (Stepanova et al., 2008).
Local auxin biosynthesis is necessary to control different plant
developmental processes. Genes encoding the molecular com-
ponents of the IAA biosynthetic pathway are expressed in
the root and their activity is necessary to control root devel-
opment. For example, the quadruple yuc1yuc4yuc10yuc11
mutant in the YUCCA genes encoding a flavin monooxyge-
nase involved in tryptophan-dependent auxin biosynthesis
does not develop a root meristem, indicating the importance
of correct auxin biosynthesis in the root (Cheng et al., 2006).
From its site of biosynthesis auxin moves within the
Arabidopsis root through two types of transport. The proto-
nated form of the IAA (IAAH) passively diffuses across the
plasma membrane, while the anionic form (IAA–
) of the auxin
is transported outside and inside the cells through an active
transport that requires efflux and influx carriers, respectively.
Auxin influx is mediated by AUX1/LAX (AUXIN 1/LIKE
AUX1) carriers, in particular by the AUXIN PERMEASE1
(AUX1) (Swarup et al., 2001). Efflux transporters are PIN
FORMED (PIN) and ATP-BINDING CASSETTE GROUP
B (ABCB/MDRPGP) (Balzan et al., 2014). PIN proteins are
polarly localized in cell membranes through the cell endo-
membrane system and play a crucial role in polar auxin
transport (PAT) responsible for the formation of an auxin
gradient along the root (Blilou et al., 2005; Ljung et al., 2005;
Grieneisen et al., 2007). According to this gradient, a peak of
auxin is established at the root apex and provides positional
information essential for maintenance of correct cell division,
polarity, and fate (Sabatini et al., 1999).
In the cell, IAA molecules are perceived by specific recep-
tor proteins, the TIR1/AFB (TRANSPORT INHIBITOR
RESISTANT1/AUXIN SIGNALING F-BOX). TIR1 and
AFB1–AFB5 contain the F-box that takes part in the ubiq-
uitin ligase complex SCFTIR1
(Kepinski and Leyser, 2005).
More recently, ABP1 (AUXIN BINDING PROTEIN 1),
an extracellular localized protein able to bind IAA, has been
proposed as another auxin receptor involved in auxin inhi-
bition of clathrin-mediated endocytosis of the polar auxin
transporters PIN1 and PIN2 through the activation of a spe-
cific ROP-GTPase (Rho of plants) (Chen et al., 2012). Auxin
signal transduction strongly depends on the auxin intracel-
lular concentration. A high IAA concentration acts to sta-
bilize the binding of the TIR1/AFB receptors to repressor
auxin/IAA (Aux/IAA) proteins causing Aux/IAA ubiquitina-
tion and degradation via the proteasome. Aux/IAA proteins
work through heterodimerizing with AUXIN RESPONSE
FACTORs (ARFs), thus repressing their transcriptional
activity (reviewed in Wang and Estelle, 2014). Thus, Aux/
IAA degradation causes ARF activation that modulates
transcription of auxin-responsive target genes, binding the
AUXIN RESPONSIVE ELEMENT (ARE: 5′-TGTCTC-3′)
(Boer et al., 2014). At low IAA concentration, the ubiqui-
tin ligase complex SCFTIR1
displays less affinity for Aux/IAA
proteins, so the amount of stable Aux/IAA protein increases,
causing the formation of Aux/IAA–ARF heterodimers which
inhibit ARF-mediated regulation of target gene transcription
(reviewed in Peer, 2013).
Cytokinin
Cytokinins are plant hormones, known to be N6
-prenylated
adenine derivatives that control many aspects of plant growth
and development. In higher plants, bioactive cytokinins
are isoprenoid cytokinins such as isopentenyladenine (iP),
trans-zeatin (tZ), cis-zeatin, and dihydrozeatin (reviewed in
Del Bianco et al., 2013). The most abundant forms found
in Arabidopsis are iP and tZ (Sakakibara, 2006). Cytokinin
homeostasis is a multistep process regulated by the balance
between biosynthesis and catabolism (reviewed in Frébort
et al., 2011). The correct plant growth depends on spa-
tial and temporal co-ordination of this process (Miyawaky
et al., 2004; Sakakibara, 2006). The initial, rate-limiting
step in cytokinin biosynthesis is catalysed by the ATP/ADP-
ISOPENTENYLTRANSFERASE (IPT) gene family. In
Arabidopsis, there are seven IPT genes. Moreover, the expres-
sion domain of each IPT gene is tissue and organ specific
(Miyawaky et al., 2004). IPTs catalyse the transfer of an
isopentenyl group to an adenine nucleotide (iP nucleotide).
Two cytochrome P450 monooxygenases, CYP735A1 and
CYP735A2, convert the iP nucleotides to tZ nucleotides
(Takei et al., 2004). An additional step is necessary to con-
vert the cytokinin from its inactive to its active form. This
step is conducted by enzymes encoded by the LONELY GUY
(LOG) gene family (Kuroha et al., 2009). Analysis of the
expression pattern domain of AtLOG revealed that, like the
IPT genes, these genes are expressed throughout the plant

Hormone cross-talk and root growth | Page 3 of 9
during development, although with different and overlap-
ping expression domains (Kuroha et al., 2009). The final
step involves catabolic genes that ensure the maintenance
of a correct concentration of active cytokinin. Enzymes
encoded by the CYTOKININ OXIDASE (CKX) gene family
(Schmulling et al., 2003) mediate cytokinin degradation. The
CKX enzymes catalyse irreversible inactivation of cytokinin
through oxidative cleavage of its N6
side chain, resulting in
the formation of adenine (or its corresponding derivative for
N9
-substituted cytokinin) and a side chain-derived aldehyde
(Frebòrt et al., 2011).
How cytokinin is transported through the plant is still not
completely clear. Recently, it has been demonstrated that,
besides diffusion, long-distance (root to shoot) cytokinin
transport also occurs through the phloem (Bishopp et al.,
2011). Researchers identified members of the PURINE
PERMEASE (PUP) and EQUILIBRATE NUCLEOSIDE
TRANSPORT (ENT) families as putatively responsible for
cytokinin transport through the phloem (Gillissen et al., 2000;
Bürkle et al., 2003). Recently, another protein, the Arabidopsis
ATP-binding cassette (ABC) transporter G14 (AtABCG14),
has been demonstrated to be essential for cytokinin transport
through the xylem (Ko et al., 2014; Zhang et al., 2014).
Cytokinin signalling is mediated by a multistep phospho-
transfer cascade similar to the bacterial two-component
system (reviewed in El-Showk et al., 2013). In Arabidopsis,
cytokinins are perceived by transmembrane histidine
kinase receptors, named ARABIDOPSIS HIS KINASE
2 (AHK2), AHK3, and AHK4/WOODENLEG (WOL)/
CYTOKININ RESPONSE 1 (CRE1) (Hwang and Sheen,
2001; Inoue et al., 2001). Cytokinin–receptor binding acti-
vates a phosphorylation cascade ending with the transfer of
a phosphate group from members of the ARABIDOPSIS
HIS PHOSPHOTRANSFER PROTEIN (AHP) fam-
ily to the nuclear-localized ARABIDOPSIS RESPONSE
REGULATOR (ARR) protein family (Hwang and Sheen,
2001; Hutchison et al., 2006). The ARR proteins are classified
into two different types, type-A and type-B. Type-A ARRs
(ARR3–ARR9 and ARR15–ARR17) are negative regula-
tors of cytokinin responses and their mechanism of action
is poorly understood (Kim, 2008). In contrast, type-B ARRs
(ARR1, ARR2, ARR10–ARR14, and ARR18–ARR21) are
a family of transcription factors that act as positive regulators
of cytokinin-dependent gene expression (Muller, 2011). These
proteins are finely regulated by a family of F-box proteins,
called KISS ME DEADLY (KMD), that physically interact
with type-B ARRs, targeting these proteins for degradation
via the proteasome (Kim et al., 2013). The type-B cytokinin
transcription factors are believed to act together with another
family of cytokinin-dependent transcription factors, the
CYTOKININ RESPONSE FACTORs (CRFs), which posi-
tively control cytokinin response (Rashotte et al., 2006).
Gibberellin
Gibberellins (GAs) are a large family of tetracyclic diterpenoid
plant growth regulators. Biologically active GA forms, GA1,
GA3, GA4, and GA7, control different plant growth processes
including seed germination, stem elongation, leaf expansion,
and flower and seed development (Yamaguchi, 2008). Many
non-bioactive GAs exist in plants as precursors for the bioac-
tive forms or as deactivated metabolites (Yamaguchi, 2008).
The GA homeostasis is maintained by biosynthesis, forma-
tion of bioactive GAs, and deactivation pathways. GAs are
biosynthesized from geranylgeranyl diphosphate (GGDP), a
common C20 precursor of diterpenoids. Three different classes
of enzymes are required for the production of bioactive GAs
from GGDP: terpene synthases (TPSs), cytochrome P450
monooxygenases (P450s), and 2-oxoglutarate-dependent diox-
ygenases (2ODDs) (Yamaguchi, 2008). The final step of bio-
synthesis is catalysed by GA 20-oxidases (GA20oxs) and GA
3-oxidases (GA3oxs) (Chiang et al., 1995; Phillips et al., 1995).
These enzymes, by a series of oxidation steps, synthesize the
bioactive GAs, in particular GA4 and GA1. The bioactive GA
homeostasis is sustained by feedback mechanisms that also
depend on catabolic genes. One of these genes encodes the GA
2-oxidase (GA2ox) which mediates the deactivation of bioac-
tive GAs by 2β-hydroxylation (Schomburg et al., 2003; Rieu
et al., 2008). GAs are synthesized in the root meristem; in fact
the activity of biosynthetic genes is higher in the meristem and
lower in other cell types (Silverstone, 1997; Birnbaum et al.,
2003). GAs accumulate in the endodermis of the root elon-
gation zone (Shani et al., 2013), but the mechanism through
which GAs move along the root is poorly understood.
GAs are perceived in the cell through a simple circuit, which
is regulated by the nuclear-localized growth-repressing DELLA
proteins (DELLAs), a subgroup of the GRAS family of puta-
tive transcription regulators (Bolle, 2004; reviewed in Davière
and Achard, 2013). In Arabidopsis, there are five DELLAs:
GA-INSENSITIVE (GAI), REPRESSOR OF GA (RGA),
RGA-LIKE1 (RGL1), RGL2, and RGL3. These proteins
are the intracellular negative regulators of the GA response
(Peng et al., 1997; Silverstone et al., 1998). The GA signalling
pathway starts when GA molecules are perceived by a solu-
ble GA receptor with homology to human-sensitive lipase,
GA-INSENSITIVE DWARF1 (GID1) (Ueguchi-Tanaka
et al., 2005). The direct binding between GAs and GID1 induces
the interaction between GID1 and the DELLA-domain of
DELLAs (Willige et al., 2007), allowing the formation of the
GA–GID1–DELLA complex. Consequently, the GA–GID1–
DELLA complex is targeted by a specific SCF (SK1, CULLIN,
F-BOX) E3 ubiquitin-ligase complex, through the binding
between DELLA protein and the F-BOX protein SLEEPY
(SLY). In turn, SCFSLY
promotes the ubiquitinylation and sub-
sequent degradation of DELLA by the 26S proteasome, trig-
gering the GA response (Fu et al., 2004). In the root, the tissue
committed to GA response is the endodermis where it has been
shown that it is sufficient to manipulate GAI degradation to
control root meristem size (Ubeda-Tomas et al., 2008, 2009).
Brassinosteroids
Brassinosteroids (BRs) are involved in the regulation of cell
elongation and division during plant organ formation and are

implicated in abiotic and biotic stresses responses. Moreover
BRs are also involved in the control of photomorphogenesis,
bending, development of reproductive organs, and vascular
development. The most bioactive form of BR, brassinolide
(BL), is synthesized from campesterol as a primary precursor
upstream of different biosynthetic pathways named early and
late C-6 oxidation, C-22, and C-23 oxidation pathways con-
verging on castesterone production which is finally converted
to BL (Noguchi et al., 2000).
It has been suggested that BRs are inactivated by different
reactions, such as hydroxylation, glycosylation, demethyla-
tionm and side chain cleavage at multiple positions (Bajguz
et al., 2007).
The BR signal cascade is activated when BR binds to
the BRASSINOSTEROID INSENSITIVE1 (BRI1) recep-
tor, a leucine-rich repeat (LRR)-receptor kinase located
at the plasma membrane (She et al., 2011). From the cell
surface, BR signal reaches the nucleus following a multi-
step process in which degradation of the GSK3-like kinase
BRASSINOSTEROID INSENSITIVE2 (BIN2) determines
the activation of the two key transcription factor homologues,
BRASSINAZOLE RESISTANT1 (BZR1) and BRI1-EMS-
SUPPRESSOR1 (BES1)/BZR2, by a dephosphorylation step
mediated by PP2A phosphatase (Clouse, 2011; Tang et al.,
2011). BZR1 and BES1 are consequently stable and accumu-
late in the nucleus where they form homo- and heterodimers
that bind DNA of specific target genes recognizing brassi-
nosteroid-responsive elements (BRREs) (Sun et al., 2010; Yu
et al., 2011). In this way, the BR signalling pathway generates
a homeostatic feedback loop also controlling its own biosyn-
thesis. However, despite recent progress in our comprehen-
sion of BRs signalling, many aspects of BR homeostasis,
transport, and functions need to be elucidated.
Abscisic acid
Plants, which are sessile organisms, evolved highly efficient
environmental adaptive strategies. External environmental
stresses are perceived by plants and translated into internal
signals activating specific stress-responsive genes. A phy-
tohormone playing a crucial rule in this process is the iso-
prenoid hormone abscisic acid (ABA). ABA was originally
identified in the 1960s as a hormone involved in seed dor-
mancy regulation and organ abscission (Liu and Carns, 1961).
It has been shown that exogenous ABA application induces
the expression of specific stress-related genes, the same genes
that are up-regulated under environmental stress conditions
(Shinozaki and Yamaguchi-Shinozaki, 2000). Therefore,
plants respond to environmental stresses by overproduc-
ing ABA and activating the ABA signalling pathway. ABA
biosynthesis occurs in plastids of all cell types, but predomi-
nantly in the vascular tissues. It is characterized by a series
of oxidation and isomerization of carotenoids leading to the
cleavage of C40 carotenoid that causes the production of
xanthoxin that is then converted in ABA aldehyde and finally
oxidized to ABA. There is also a parallel pathway starting
from ABA aldehyde that is converted to ABA alcohol and
transformed into ABA after oxidization by a P450 monooxy-
genase (Nambara and Marion-Poll, 2005). ABA homeostasis
involves catabolic processes including oxidative and con-
jugative reactions. Hydroxylation of three different methyl
groups of ABA (7′, 8′, and 9′) leads to different oxidation
pathways. The hydroxylation reaction results in the produc-
tion of phaseic acid (PA) that is transformed to dihydropha-
seic acid (DPA) which is a biologically inactive form of ABA.
On the other hand, a conjugative reaction is responsible for
the production of the ABA-glucose ester (ABA-GE) derived
from ABA upon covalent conjugation with glucose (Jiang
and Hartung, 2008). ABA-GE is a long-distance transported
form and a storage form of ABA, as demonstrated by the fact
that cleavage of the conjugate, by β-glucosidases, releases free
ABA (Lee et al., 2006).
ABA perception starts when this hormone is perceived
by the PYRABACTIN RESISTANCE (PYR)/PYR1-
LIKE (PYL)/REGULATORY COMPONENTS OF ABA
RECEPTORS (RCAR) family of ABA receptors (Santiago
et al.,2009;Mosqunaet al.,2011).ABAbindingtoPYR/PYL/
RCAR receptors blocks the phosphatase activity of type 2C
protein phosphatases (PP2Cs). These are negative regulators
of ABA signalling that activate the transcription of specific
ABA-responsive genes, containing ABA-responsive elements
(ABREs; PyACGTGGC) in the promoter (Giraudat et al.,
1994; Busk and Pages, 1998).
As ABA is the major hormone involved in stress responses,
such as salinity, drought, and temperature stresses, a full com-
prehension of ABA signalling and perception would be use-
ful to increase crop productivity.
Strigolactones
Recent studies identified a class of terpenoid lactones called
strigolactones (SLs) as new plant hormone (Gomez-Roldan
et al., 2008). The first data collected assigned a role for SLs in
parasitic and symbiotic interaction responses. Subsequently,
in 2008, two groups discovered a fundamental role for SLs
in shoot branching regulation (Gomez-Roldan et al., 2008;
Umehara et al., 2008). Recent work identified SLs as positive
regulators of primary root elongation and negative regula-
tors of adventitious root formation (Ruyter-Spira et al., 2011;
Rasmussen et al., 2012). Thus, SLs are new important com-
ponents involved in plant growth and development. Little is
known about the SL biosynthetic pathway, but recent data
suggested a possible involvement of carotenoid as a precursor
of SLs. Indeed, carotenoid-deficient mutants show absence of
SLs and, in plants treated with fluridone, a carotenoid bio-
synthesis inhibitor, SL levels are reduced (Matusova et al.,
2005). Alder et al. (2012) identified carlactone as a possible
SL biosynthetic intermediate. Some genes involved in SL
biosynthesis have been identified, and among them there are
two carotenoid cleavage dioxygenases (CCD7 and CCD8)
and one cytochrome P450, MORE AXILLARY GROWTH1
(MAX1) (Gomez-Roldan et al., 2008; Umehara et al., 2008).
Localization of biosynthetic gene expression patterns is
useful to obtain preliminary information about sites of SL

biosynthesis in the plant. In rice root, CCD7 (HTD1) and
CCD8 (D10) are expressed throughout the vascular paren-
chyma cells, while in Arabidopsis MAX1 is active in root
vascular tissue and CCD8 (MAX4) is expressed in primary
and lateral roots in the columella root cap (Bainbridge et al.,
2005; Booker et al., 2005; Arite et al., 2007). SL receptors
have not been identified yet, but some proteins have been
proposed as possible candidates. One of them is the MAX2
protein which is a member of the SCF-type ubiquitin ligase
complex (Stirnberg et al., 2007). More recently, evidence has
been collected showing that DWARF 14 (D14), an α/β hydro-
lase protein, connects SL perception and signalling through
protein–protein interactions with MAX2-type proteins (Arite
et al., 2009; Waters et al., 2012; Kagiyama et al., 2013).
Plant hormones: the importance of cross-
talk in controlling root meristem size
Data collected in the last few years demonstrate that coherent
root growth is a finely regulated process requiring that each
hormone communicates with the others, giving rise to a com-
plex network of hormone interactions.
Root meristem development starts post-embryonically
when the root SCN is activated, leading to radicle protru-
sion during seed germination processes. In this phase of
root development, the division rate of stem cell daughters
overcomes their differentiation, allowing meristem building
(Moubayidin et al., 2010). At 5 days post-germination (dpg),
the meristem sets its final size, establishing a dynamic equilib-
rium between cell division and cell differentiation. Meristem
size is then maintained constant over time (Dello Ioio et al.,
2007). The overall events ensuring meristem building and
maintenance need to be finely regulated, and a pivotal role
in this process is played by plant hormones and their cross-
talk. The Aux/IAA SHORT HYPOCOTYL2 (SHY2) gene,
a repressor of auxin signalling, has a crucial role in control-
ling meristem size and development. Indeed, the loss-of-
function shy2-31 mutant displays an enlarged root meristem
due to a delay in cell differentiation that causes loss of the
balance between cell division and cell differentiation, while
high levels of SHY2 during the root meristem growth phase
are sufficient to stop root growth and reduce meristem size
(Dello Ioio et al., 2008; Moubayidin et al., 2010). It has been
shown that SHY2 specifically acts at the vascular tissue tran-
sition zone to regulate PIN expression and auxin distribu-
tion. Cross-talk of many hormones converges on this gene,
fine-tuning its level and thus controlling SHY2 abundance in
a time-dependent manner during root development (Fig. 1).
The optimal SHY2 level is reached only when both the ARR1
and ARR12 cytokinin-dependent genes activate SHY2 tran-
scription (Moubayidin et al., 2010) (Fig. 1B). During the
meristem growth phase, a high amount of GA causes ARR1
repression through degradation of the DELLA protein
REPRESSOR OF GA (RGA) (Moubayidin et al., 2010)
(Fig. 1A). In this way SHY2 levels are kept low because its
activation depends only on ARR12. A low SHY2 level results
in auxin signalling activation that positively regulates the
auxin transport facilitator PIN genes promoting auxin distri-
bution and cell division (Dello Ioio et al., 2008; Moubayidin
et al., 2010) (Fig. 1A). At the same time, BREVIS RADIX
(BRX), a protein implicated in the BR pathway, also controls
polar auxin transport, specifically inducing PIN3 expression
(Scacchi et al., 2010) (Fig. 1A). Recently, it has been shown
that ARR12 controls root growth by activating the transcrip-
tion of a member of the ARF family, AUXIN RESPONSE
FACTOR19 (ARF19), together with SHY2, promoting cell
differentiation of meristematic cells at the TZ (Perilli et al.,
2013).
At 5 dpg, the level of RGA increases, probably because
of a decrease in amount of GA, inducing ARR1 activation.
ARR1 activates SHY2 together with ARR12, increasing its
level of expression, repressing PIN activity, and enhancing
cell differentiation (Moubayidin et al., 2010) (Fig. 1B). The
increase in SHY2 level also depends on SL activity. Indeed,
it has been shown that SLs induce SHY2 expression, thus
interfering with auxin flux (Koren et al., 2013) (Fig. 1B). It
has been demonstrated that BRX expression is controlled
by auxin; thus, a reduction in auxin distribution, caused by
PIN repression, determines a decrease in BRX level and a
consequent PIN3 inhibition. This inhibition limits auxin
transport and distribution, thus contributing to the increase
of the cell differentiation rate (Scacchi et al., 2010) (Fig. 1B).
Modulation of auxin flux also depends on the activity of
the BR receptor, BRASSINOSTEROID INSENSITIVE 1
(BRI1), which is expressed in the epidermis and from this tis-
sue post-transcriptionally regulates PIN proteins (Hacham
et al., 2011, 2012).
Another hormone involved in polar auxin transport regu-
lation is ABA. Indeed, ABSCISIC ACID INSENSITIVE4
(ABI4), a protein encoding an ABA-regulated AP2 domain
transcription factor whose expression is induced by ABA and
cytokinin, represses PIN1 expression (Shkolnik-Inbar and
Bar-Zvi, 2011) (Fig. 1B). Recently, it has been demonstrated
that another gene involved in ABA signalling, ABSCISIC
ACID INSENSITIVE5 (ABI5), which encodes a transcrip-
tion factor belonging to the basic leucine zipper (bZIP) fam-
ily, represses polar auxin flux through the inhibition of PIN1,
thereby controlling root growth (Yuan et al., 2014) (Fig. 1B).
All the hormonal pathways described co-operate to keep
polar auxin transport low, while at the same time auxin coun-
teracts this repression, directing SHY2 degradation, and thus
allowing the maintenance of PIN activity and the consequent
induction of cell division (Dello Ioio et al., 2008).
This complex network of hormone interactions allows cell
differentiation to balance cell division, consequently setting
the final root meristem size.
To ensure coherent root growth, cell differentiation at the
TZ needs to be co-ordinated not only with cell division of
meristematic cells, but also with the activity of stem cells.
Recently the molecular mechanism involved in the spatial co-
ordination between the TZ activity and the SCN has been
partially clarified. Co-ordination between these two zones is
regulated by the SCARECROW (SCR) gene (Sabatini et al.,
2003; Moubayidin et al., 2013). In the QC, SCR directly binds
to and negatively regulates ARR1, which in turn, controls

auxin production by modulating the expression of the auxin
biosynthesis gene ASB1. SCR, by controlling the level of
auxin production in the QC, exerts a long-distance control
of ARR1 in the TZ. The auxin produced by ASB1 in the QC
and distributed along the meristem by PINs is sufficient to
activate ARR1 expression in the TZ, thus sustaining cell dif-
ferentiation via SHY2 (Dello Ioio et al., 2008; Moubayidin
et al., 2013).
Conclusions and perspectives
In this review, we provide an overview on the plant hormones
involved in the regulation of root meristem size. In particu-
lar, we integrated recent data showing molecular details of
hormonal interaction. The emerging picture is that auxin is
the pivot of the dynamic regulation of root meristem size.
A lot of data indicate that auxin is not a common plant hor-
mone, but it acts as a morphogen instructing cell fate in a
dose-dependent manner (reviewed in Benkova et al., 2009).
Hormonal cross-talk converges on the regulation of genes
involved in auxin signalling and/or transport to ensure a cor-
rect auxin graded distribution, allowing, in this case, correct
root meristem size determination. Therefore, the finely regu-
lated spatio-temporal interactions between hormones ulti-
mately modulate the distribution and the perception of auxin.
The increasing amount of molecular data contributes to
broaden our knowledge, at the same time introducing an
additional level of complexity, as the outputs of such net-
works are non-intuitive. Mathematical modelling has already
proved to be a powerful tool to integrate data at multiples
levels, allowing for the dissection of hormonal cross-talk
involved in the control of a particular system. For example,
a computational approach has been used to demonstrate that
auxin–cytokinin interaction is responsible for the formation
of a stable pattern within a growing vascular tissue (De Rybel
et al., 2014).
We are confident that further modelling development will
provide insights into the role of the complex hormonal circuit
Fig. 1. Hormonal cross-talk involved in root meristem size determination. (A, B) Confocal microscope images of the Arabidopsis root tip with different
developmental zones indicated, stem cell niche (SCN), proximal meristem (PM), transition zone (TZ), and elongation and differentiation zone (EDZ),
flanked by a schematic model of hormonal interaction at 3 days post-germination (dpg) (A) and at 5 dpg (B). At the bottom a schematic picture of
communicating vessels is used to represent the ratio between cell division and cell differentiation at 3 dpg (A) and at 5 dpg (B). (A) At 3 dpg, hormonal
cross-talk guarantees a low level of cell differentiation, allowing meristem growth. (B) At 5 dpg, a complex network of hormonal interactions balances cell
differentiation with cell division, setting the meristem size. In both cases, hormone cross-talk converges on the SHY2 gene whose levels are kept low at
3dpg (A) and higher at 5 dpg (B). Red arrowheads indicate the TZ of the cortex tissue, placed at the boundary between the last meristematic cell and the
first differentiating cell. A colour code has been used to indicate different pathways: in blue pathways under the control of auxin (IAA), in red those under
the control of cytokinin (CK), in yellow that controlled by gibberellin (GA), in orange those controlled by brassinosteroid (BR), in green those controlled by
abscisic acid (ABA), and in grey that controlled by strigolactones (SLs).

responsible for pattern formation and growth in the root
meristem, predicting emerging properties that could not be
observed solely by means of ‘wet’ biology.
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