Arabidopsis lateral root development:
an emerging story
Benjamin Pe´ret1*
, Bert De Rybel2,3*
, Ilda Casimiro4
, Eva Benkova´2,3
, Ranjan Swarup1
,
Laurent Laplaze5
, Tom Beeckman2,3
and Malcolm J. Bennett1
1
Plant Sciences Division and Centre for Plant Integrative Biology, School of Biosciences, University of Nottingham, Sutton
Bonington Campus, Loughborough LE12 5RD, UK
2
Department of Plant Systems Biology, VIB (the Flanders Institute for Biotechnology), Technologiepark 927, B-9052 Gent, Belgium
3
Department of Plant Biotechnology and Genetics, Ghent University, Technologiepark 927, B-9052 Gent, Belgium
4
Departamento de Anatomia, Biologia Celular y Zoologia. University of Extremadura, E-06071 Badajoz, Spain
5
Institut de Recherche pour le De´veloppement, UMR DIA-PC (Agro.M/INRA/IRD/UM2), Equipe Rhizogene`se, 911 Avenue Agropolis,
F-34394 Montpellier cedex 5, France
Lateral root formation is a major determinant of root
systems architecture. The degree of root branching
impacts the efﬁciency of water uptake, acquisition of
nutrients and anchorage by plants. Understanding the
regulation of lateral root development is therefore of
vital agronomic importance. The molecular and cellular
basis of lateral root formation has been most extensively
studied in the plant model Arabidopsis thaliana (Arabidopsis).
Signiﬁcant progress has recently been made in
identifying many new Arabidopsis genes that regulate
lateral root initiation, patterning and emergence processes.
We review how these studies have revealed that
the plant hormone auxin represents a common signal
that integrates these distinct yet interconnected developmental
processes.
Lateral root development
Higher plants exhibit an amazing diversity of root architectures
at both the system and anatomical levels [1].
Many dicotyledonous plants, such as Arabidopsis, have a
primary root that repeatedly branches to generate several
orders of lateral roots, whereas the root system of cereal
crops, such as rice (Oryza sativa) and maize (Zea mays), are
predominantly composed of adventitious roots [2,3].
Recent genetic studies have identiﬁed many genes that
are common to lateral, crown and adventitious root development
[4]. Although impressive progress has recently
been made in crops, Arabidopsis remains the best characterized
experimental system for studying lateral root development
and represents the focus for this review.
Arabidopsis lateral roots originate exclusively from
pericycle founder cells located opposite xylem poles [5]
(Figure 1). Lateral roots are initiated when either individual
[6] or pairs of pericycle founder cells undergo several
rounds of anticlinal divisions [6–8] to create a single
layered primordia composed of up to ten small cells of
equal length (termed stage I; Figure 1). Next, the
cells divide periclinally, forming an inner and an outer
layer (termed stage II; Figure 1). Further anticlinal and
periclinal divisions create a dome-shaped primordium
(spanning stages III–VII) that eventually emerges (at
stage VIII) from the parental root [7,8] (Figure 1).
In this review, we discuss Arabidopsis lateral root
development chronologically, starting from the initial
Review
Glossary
Recent advances in the study of lateral root formation have led to the
identification of new important regulatory processes. In order to
avoid any terminology confusion, we propose here a list of
definitions describing each of these processes in chronological order.
Xylem pole speciﬁcation: the differentiation between the phloem
pole and xylem pole pericycle cells giving rise to the diarch symmetry
of the Arabidopsis root. This distinction between the two cell
populations is apparent in the pericycle initial cells as early as the
heart stage embryo [15].
Basal meristem: zone situated between the apical meristem and the
elongation zone of the root characterized by both cell division and
cell elongation processes. The basal meristem has previously been
named ‘post-meristematic isodiametric growth zone’ or ‘distal
elongation zone’ [89].
Priming: xylem pole pericycle cells undergo a cyclic pre-initiation
event that is auxin dependent, occurs in the basal meristem and
marks the pericycle cells every 15 hours. These primed cells gain
pericycle founder cell identity and will become founder cells upon
auxin activation higher up in the parental root [21]. This founder cell
identity speciﬁcation can also occur outside the basal meristem by
auxin induction [23].
Pericycle founder cells: primed xylem pole pericycle cells that
undergo initiation by auxin activation, causing them to become
pericycle founder cells and undergo the ﬁrst anticlinal and asymmetric
division.
Pre-initiation events: all events occurring before the initiation process
and leading to pericycle cell speciﬁcation and priming.
Lateral root initiation: the start of the auxin-induced signalling processes
in two adjacent primed pericycle cells, including the ﬁrst
anticlinal and asymmetrical division of two adjacent pericycle founder
cells. This division creates two small daughter cells that will continue
to divide and create the primordium ﬂanked by two larger cells.
Lateral root patterning: the tightly controlled sequence of divisions
giving rise to a dome-shaped structure that will eventually give birth
to a new meristem.
Lateral root emergence: emergence is the continuous process by
which the primordium actively makes its way through the outer
tissues out to the rhizosphere. It includes the auxin-induced activation
of cell wall remodelling genes facilitating the emergence process [67].
Lateral root formation: the developmental process as a whole that
combines all steps from pre-initiation events up to initiation, emergence
and meristem activation of the lateral root primordium.Corresponding author: Pe´ret, B. (malcolm.bennett@nottingham.ac.uk)
*
These authors contributed equally to this work..
1360-1385/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2009.05.002 Available online 24 June 2009 399
speciﬁcation of pericycle cells opposite the xylem pole, then
covering lateral root initiation, patterning and emergence,
followed by activation of the new meristem and elongation
of the new lateral root (see Glossary). We focus on recent
advances in our understanding of the molecular and cellular
processes during lateral root development, highlighting
new insights into both pre- and post-initiation events,
including the previously overlooked issue of how a new
organ can emerge through overlaying tissues. Given the
space limitations of this article, readers might be interested
in several excellent reviews that focus in more detail
on speciﬁc aspects of lateral root formation, such as auxinregulated
initiation and cell cycle events [9,10], differences
between species [4,11] or regulation by nutrients [12–14].
Pre-initiation events: preparing xylem pole pericycle
cells to divide
The pericycle represents a heterogeneous tissue consisting
of quiescent cells at the phloem poles and cells competent
to form lateral root primordia (LRP) opposite each xylem
pole [15]. Speciﬁcation of xylem pole pericycle cell fate (see
Glossary) is controlled by the same genetic pathway determining
diarch patterning of the underlying root vascular
tissues [15,16]. Mutations, such as lonesome highway
(lhw), that disrupt the diarch patterning of xylem poles
also block the speciﬁcation of the overlaying pericycle cells
and their ability to form LRP [15]. Although three xylem
pole pericycle cell ﬁles are dividing during lateral root
formation, cell lineage experiments have revealed that
only the middle cell ﬁle contributes signiﬁcantly to the
establishment of the LRP [17].
After leaving the root apical meristem, pericycle cells at
the phloem poles remain in the G1 phase, whereas those at
the xylem poles advance to the G2 phase of the cell cycle
[18]. This sub-population of pericycle cells at the xylem pole
can be considered an ‘extended meristem’ [19] because,
unlike cells at the phloem pole or in other root tissues, they
maintain their ability to divide after exiting the root apical
meristem. The nuclear protein ALF4 (ABERRANT LATERAL
ROOT FORMATION4) is required to maintain
xylem pole pericycle cells in a mitosis-competent state
because the alf4 mutation blocks the induction of the
mitotic marker cyclin B1 (CycB1);1::GUS but causes
overexpression of the earlier cell cycle marker cyclin
dependent kinase B (CDKB);1:GUS in this tissue [20]
(Figure 2).
Pericycle cell division in Arabidopsis is ﬁrst detected
several millimetres distal to the primary root meristem [7].
However, it has recently been reported that the decision by
xylem pole pericycle cells to form a LRP is taken in a zone
termed the basal meristem, which is immediately behind
the primary root apical meristem [21] (Figure 2). The
authors demonstrated that xylem pole pericycle cells in
the basal meristem are primed to divide by auxin signalling.
Disrupting the auxin response of xylem pole pericycle
cells (except those in the apical and basal root meristem
zones; Figure 2) blocked the initial asymmetric division of
pairs of founder cells [21] (Figure 3). However, their nuclei
remained able to migrate to the common cell wall [21]
(Figure 3), implying that these pericycle founder cells must
have already been exposed to an inductive auxin signal.
Hence, priming of pairs of xylem pole pericycle cells to
become founder cells by auxin signalling normally occurs
close to the root apex in the basal meristem (Figure 2).
Auxin and mechanical signals regulate spacing of
pericycle founder cells
Every xylem pole pericycle cell has the ability to divide in
response to elevated auxin levels [22,23]. However, only
a limited number of xylem pole pericycle cells become
Figure 1. Morphological changes during lateral root development. Lateral roots originate deep within the primary root from the pericycle cells (a). The eight stages of
primordium development (roman numbers [6]) are shown (b) as well as establishment of the auxin signalling maximum as demonstrated with the DR5:GUS reporter (blue
gradient (c) [30]). The cartoons were drawn from aniline-blue-stained roots for each stage of lateral root development (d). The scale bars represent 20 mm.
Review Trends in Plant Science Vol.14 No.7
400
Figure 2. Lateral root priming occurs in the basal meristem. Schematic overview of the different root tissues (a) and the auxin signalling maximum present (b) as reported
by the DR5::GUS marker line [21]. The regularly spaced auxin accumulation sites in the protoxylem primes the adjacent pericycle cells to become pericycle founder cells.
Figure 3. Early events during lateral root initiation. Local auxin accumulation in primed xylem pole pericycle cells activates the auxin signalling cascade. Auxin causes the
degradation of IAA14, thereby de-repressing ARF7 and 19 and activating downstream gene expression. The receptor-like kinase ACR4 promotes formative divisions in the
primordium and represses cell divisions in surrounding pericycle cells [54]. Abbreviation: LOB, LATERAL ORGAN BOUNDARIES.
Review Trends in Plant Science Vol.14 No.7
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founder cells under normal conditions [8]. Intriguingly,
lateral root initiation occurs at a regular rhythm during
root growth [24]. Until very recently, the mechanism(s)
that patterns the regular spacing of LRP along the root has
proved elusive. It has been reported that priming of pericycle
founder cells is correlated with an oscillating auxin
response (visualized by the DR5::GUS marker) in adjacent
xylem cells [21] (Figure 2). The authors demonstrated that
these oscillations occurred at regular intervals of 15 h
and were associated with the induction of new LRP in
adjacent pericycle cells [21] (Figure 2). Arabidopsis roots
therefore seem to have an auxin-based oscillatory mechanism
that causes the periodic initiation of LRP along the
primary root.
The spacing of lateral roots along the Arabidopsis
primary root can also be inﬂuenced by tropic responses
and mechanical stimuli [21,25–27]. For example, it has
been reported that a gravitropic stimulus can induce LRP
to form on the outer side of bending roots [25]. Intuitively,
it is hard to reason how higher auxin levels might accumulate
in the pericycle on the outside of a root bend when a
gravity stimulus diverts the majority of auxin to the lower
side of the root [28,29]. Nevertheless, confocal imaging of
transgenic roots expressing a DR5::venusYFP (yellow
ﬂuorescent protein) reporter revealed dynamic changes
in auxin-responsive gene expression consistent with such
a redistribution of auxin between root tissues [26,27]. Via
in silico modelling, it was hypothesized that higher auxin
levels are created in the pericycle on the outside of the bend
by mechanically inﬂuenced changes in cell sizes. The
higher auxin levels trigger expression of the auxin inﬂux
carrier AUX1 (AUXIN RESISTANT1), resulting in the
creation of an auxin maximum before de novo organ formation
[26]. By contrast, it was proposed that mechanically
induced changes in auxin-responsive gene expression
at the site of lateral root initiation required the relocalization
of the auxin efﬂux transporter PIN1 (PIN-FORMED1)
in an adjacent protoxylem cell [27]. However, the mechanical
induction of LRP cannot be explained by either a
PIN1- or AUX1-based mechanism. First, the pin1 mutant
does not exhibit a lateral root defect [30]. Second, lateral
root initiation defects in auxin mutants, including aux1,
can be rescued by a mechanical stimulus [27]. This
suggests that a mechanical signalling mechanism must
exist independent of auxin to prime pericycle founder cells.
Hence, at least two mechanisms seem to be operating in
roots to inﬂuence positioning of LRP: a mechanical induction
pathway and an auxin-based oscillatory mechanism.
This makes perfect sense for a root because it enables the
spacing of LRP to be responsive to both environmental and
endogenous signals.
Although the molecular basis of the mechanical signalling
pathway remains to be elucidated, many of the transduction
components that mediate auxin-regulated lateral
root initiation have recently been identiﬁed and characterized
[10]. One of the most important auxin signalling
proteins regulating lateral root initiation is IAA14
(INDOLE ACETIC ACID14)/SLR1 (SOLITARYROOT1)
[31]. IAA14/SLR1 belongs to a family of labile Aux/IAA
proteins that function to repress auxin-regulated transcription
[31]. A key step in the lateral root initiation
pathway is the auxin-dependent degradation of Aux/IAA
proteins like IAA14/SLR1. Selected amino acid substitutions
in the IAA14 coding sequence have been reported
to stabilize the repressor protein [31]. The resulting gainof-function
slr-1 mutant does not form LRP as a result of
pericycle founder cells failing to undergo formative divisions
[31]. Nevertheless, the loss-of-function iaa14-1
mutant has no obvious phenotype [32], suggesting that
other members of the 29-strong Aux/IAA gene family
might also be involved. Although the gain-of-function
mutants iaa1/axr5 (auxin resistant 5) [33], iaa3/shy2
(short hypocotyl 2) [34], iaa18/crane [35], iaa19/msg2
(massugu2) [36] and iaa28-1 [37] are all impaired in lateral
root development (Table 1), none block lateral root
initiation completely, suggesting further redundancy in
the Aux/IAA gene family. This might be due to their
differential expression patterns or distinct functionality
between these proteins [38].
In the presence of auxin, the F-box proteins TIR1
(TRANSPORT INHIBITOR RESPONSE1) or AFB1–3
(AUXIN RECEPTOR F-BOX PROTEIN1–3) bind to Aux/
IAA proteins [39,40], which are then degraded after ubiquitin-dependent
targeting to the proteasome [41,42].
TIR1/AFB proteins seem to function redundantly during
lateral root development. Whereas single tir1 and afb
mutants have either a small or no difference in numbers
of LRP, the tir1 afb2 afb3 triple mutant exhibits a 90%
reduction [43,44]. However, it has recently been reported
that the tir1 mutation blocks the doubling in lateral root
number observed in wild-type seedlings grown in phosphate
(Pi)-poor media [44]. TIR1 expression in the pericycle
is induced by low Pi availability, whereas transgenic
lines overexpressing TIR1 phenocopy Pi-deprived seedlings
[44]. The authors propose that Pi availability modulates
LRP number by regulating the auxin sensitivity of
the pericycle in a TIR1-dependent manner.
Aux/IAA repressor proteins also dimerize with transcription
factors termed auxin response factors (ARFs)
that control auxin-responsive transcription [45]. IAA14/
SLR has been demonstrated to directly interact with ARF7
and ARF19 [46]. The targeted degradation of IAA14/SLR
by auxin and TIR1/AFB1–3 would therefore be expected to
cause the de-repression of the transcription factors ARF7
and ARF19 (Figure 3). Consistent with this model, the arf7
arf19 double mutant phenocopies many of the slr1 defects,
including the disruption of lateral root initiation [31,47].
Nevertheless, unlike slr1, the arf7 arf19 mutant still forms
a few lateral roots [10], suggesting that another ARF(s)
must also regulate organ initiation. The ARF gene family
is composed of 23 members [45]; ﬁve ARFs have been
demonstrated to function as transcriptional activators
(ARF4, 5, 6, 7 and 19) and the remaining ARFs seem to
behave like transcriptional repressors [48,49]. Several
members of the latter class of ARFs also seem to regulate
lateral root development [50–52].
Auxin regulates the patterning of new lateral root
primordia
Morphologically, lateral root initiation is usually ﬁrst
detected when pairs of pericycle founder cells undergo
several rounds of anticlinal divisions [6–8] (Figure 3).
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402
Characteristically, these formative cell divisions are asymmetric,
giving rise to shorter and longer daughter cells at
the centre and ﬂanks of the new LRP, respectively
(Figure 3). Asymmetric cell divisions are usually indicative
that daughter cells will adopt distinct developmental fates
[53]. Consistent with this conclusion, shorter (but not
longer) daughter cells express marker genes associated
with asymmetric division [54].
Researchers have recently attempted to identify the
genes that regulate these formative divisions by transcript
proﬁling arf7 arf19 and slr-1 mutants that fail to initiate
LRP [31,55]. It was observed that the slr-1 mutation
affected the expression of several cell cycle regulatory
genes, among others [55]. Overexpression of the cell cycle
regulator CycD3;1 (which promotes G1 to S phase transition)
in the slr-1 background induced a few rounds of
anticlinal divisions [55] but failed to activate the expression
of markers such as ACR4 (ARABIDOPSIS CRINKLY4) [54]
or lead to the formation of LRP [55]. The activation of cell
proliferation is therefore not sufﬁcient to rescue lateral root
development in slr-1. Instead, pericycle founder cells must
seemingly go through asymmetric cell division to express
genes such as ACR4 in their shorter daughter cells [54].
The GNOM protein seems to be required for these initial
asymmetric cell divisions [56,57]. Although pericycle cells
of weak alleles of gnom are still able to proliferate in
response to the addition of auxin, they fail to express
markers such as ACR4 [54] or form normally patterned
LRP [56]. GNOM encodes an ARF-GEF (ADP RIBOSYLATION
FACTOR-GUANIDINE EXCHANGE FACTOR)
that regulates the trafﬁcking of PIN auxin efﬂux carrier
proteins [57]. Mutants lacking several PIN genes (such as
PIN1, 3, 4 and 7) phenocopy the auxin-induced lateral root
phenotype observed in weak gnom alleles [58]. This is
because GNOM and PIN transporters are required to
establish an auxin gradient during primordium formation,
with a maximum initially in the central cells then later at
the tip of the multilayered LRP (Figure 1). This auxin
maximum is likely to pattern the new LRP in a manner
similar to a morphogen gradient during animal development
[59]. However, regulatory genes such as transcription
factors that are expressed at a particular threshold along
the auxin response gradient in LRP still wait to be ident-
iﬁed.
Auxin, initially accumulating in the central cells of the
LRP, then later at the tip of the LRP, will target the
degradation of Aux/IAA proteins, enabling ARF proteins
to transcribe genes that pattern the new LRP. Recently,
two ARF7- and ARF19-regulated genes capable of rescuing
the arf7 arf19 lateral root defect when overexpressed in the
Table 1. Overview of lateral root mutants involved in known molecular or cellular processes during lateral root formationa
Molecular/cellular processes Mutants Stage Lateral root phenotype Refs
Auxin homeostasis sur1 I Increased LR number [90]
sur2 I Increased LR number [91]
ilr2 I Reduced LR number [92]
arf8 I Increased LR number [52]
ilr1 iar3 ill2 I Reduced LR number [93]
ydk1 I Reduced LR number [94]
dﬂ1 I Reduced LR number [95]
Auxin signalling tir1 afb1 I Reduced LR number [43]
axr1 I Reduced LR number [96]
axr6/cul1 I Reduced LR number [97]
iaa1/axr5 I Reduced LR number on auxin [33]
iaa3/shy2-2 I & E Reduced LR number [34]
iaa14/slr I & E No LR [31]
iaa18/crane I Reduced LR number [35]
iaa19/msg2 I Reduced LR number [36]
iaa28 I Strongly reduced or no LR [37]
arf 7 arf19; mir160-resistant I & E No LR [32]
ARF10/16/17 I Reduced LR number [50,51]
Auxin transport aux1 I Reduced LR number [98]
lax3 E Reduced LR number [67]
pin1/3/4/7 and combinations I & P Reduced LR number [30]
pgp4 I Increased LR number [99]
Auxin transport protein addressing
and regulation
gnom I Reduced LR number [56]
axr4 I Reduced LR number [100]
pinoid I Reduced LR number [101]
big/tir3/doc1 I Reduced LR number [102]
Cell cycle 35S:KRP2 I Reduced LR number [103]
alf4 I No LR [20]
Cell-to-cell communication acr4; crr1/2/3/4 and combinations I More LR primordia and disturbed spacing [54]
Chromatin remodelling pickle I Increased LR number on auxin [104]
Cytokinin pathway brx-2 I Increased LR number on cytokinin [88]
F-box proteins 35S:SINAT5 I Reduced LR number [105]
cegenduo I Increased LR number [106]
xbat32-1 I Reduced LR number [107]
arabidillo1/2 I Reduced LR number [108]
Abbreviations: E, emergence; I, initiation; P, patterning.
a
This list is restricted to the small number of mutants for which the molecular/cellular process has been described amongst the high number of mutants with a lateral root
defect [9].
Review Trends in Plant Science Vol.14 No.7
403
double mutant background were identiﬁed [60]. LBD16/
ASL18 (LATERAL ORGAN BOUNDARIES-DOMAIN16/
ASYMMETRIC LEAVES2-LIKE18) and LBD29/ASL16
belong to a large family of plant-speciﬁc transcription
factors. LBD16/ASL18 and LBD29/ASL16 promoters
represent direct targets for ARF7 and ARF19 [60]. Hence,
these LBD proteins seem to function immediately downstream
to ARF7 and ARF19 and mediate auxin-regulated
lateral root patterning (Figure 3). Identifying which genes
are regulated by LBD16 and LBD29 is likely to prove
crucial to understanding how newly dividing pericycle
founder cells give rise to a correctly patterned LRP
(Figure 1).
In addition to auxin, cytokinins (CKs) also inﬂuence the
patterning of new LRP. Targeted expression of the CK
biosynthesis gene IPT (ISOPENTENYL TRANSFERASE)
in xylem pole pericycle (but not new LRP) cells was
observed to disrupt lateral root initiation and patterning
[61]. This result implies that CK interferes with very early
patterning events. CK seems to disrupt LRP patterning by
interfering with the expression of PIN genes, disrupting
the formation of an auxin gradient [61]. A similar mechanism
that involves auxin–CK crosstalk has been recently
described in the root apical meristem [62]. Consistent with
this model, addition of auxin to roots expressing IPT in
xylem pole pericycle cells caused them to proliferate but
fail to form patterned LRP [61]. Exogenous application of
CK leads to abnormal tangential and oblique divisions in
stage II LRP, followed by ectopic divisions in the inner
layer and rounds of periclinal divisions in the central cells
of the outer layer, giving rise to ﬂattened LRP [61]. Interestingly,
a similar deviation from the otherwise tightly
controlled cellular divisions during LRP organogenesis has
been observed in a mutant defective for the AP2 (APETALA2)/EREBP
(ETHYLENE RESPONSIVE ELEMENT
BINDING PROTEIN) transcription factor PUCHI [63].
In addition to auxin and cytokinin, signalling molecules
are likely to exist that regulate the asymmetric pericycle
cell divisions and thereby inﬂuence the patterning of newly
initiated LRP. Recently, over a dozen potential regulatory
genes that regulate asymmetric cell division and cell fate
speciﬁcation were identiﬁed by transcript proﬁling xylem
pole pericycle cells undergoing lateral root initiation [54].
One of these candidates, ACR4, was expressed in the small
daughter cells after the ﬁrst asymmetric division in the
xylem pole pericycle. Mutants lacking ACR4 and related
gene family member CRR4 (CRINKLY4 RELATED4) form
LRP that either fail to express, or exhibit aberrant expression
of, the boundary and auxin response markers
LBD5:GUS and DR5:GUS, respectively [54]. ACR4 therefore
seems to inﬂuence the speciﬁcation of cell fate during
lateral root initiation. ACR4 encodes a membrane-associated
receptor-like kinase [54], raising the intriguing
possibility that it regulates LRP patterning by recognizing
a novel class of signalling molecule, such as a peptide.
ACR4 and its related genes are also required to repress
divisions in nearby pericycle cells [54]. Mutants in ACR4
gene family members cause LRP to initiate close to one
another or at the normally excluded opposite poles [54].
Hence, ACR4 forms part of a novel patterning mechanism
that exists to repress proliferative divisions in adjacent
pericycle cells [54] (Figure 3). Given that ACR4 is
expressed exclusively in LRP, the receptor-like protein is
likely to regulate a non-cell-autonomous signal(s) that
represses division in nearby pericycle cells.
Auxin reprograms cells overlaying LRP to facilitate
organ emergence
To emerge, LRP must ﬁrst pass through several intervening
parental root tissues. In Arabidopsis, these comprise
single layers of endodermal, cortical and epidermal cells
(Figure 4). In other plant species, such as rice, LRP must
negotiate up to 15 intervening layers of cells [3]. Researchers
have speculated for over a century that lateral root
development and cell separation processes in adjacent root
tissues must be tightly coordinated to minimize tissue
damage and reduce the risk of infection (reviewed in
Ref. [1]). More recently, genes encoding several Arabidopsis
cell wall remodelling (CWR) enzymes have been
reported to be expressed in root cells next to new LRP,
presumably to cause cell separation in overlaying root
tissues and promote LRP emergence [64–66].
Figure 4. Lateral root emergence. In endodermal cells, the auxin-dependent degradation of the IAA3/SHY2 repressor triggers the expression of selected cell wall
remodelling (CWR) enzymes to initiate cell separation (a). Auxin derived from the primordium induces the expression of an auxin influx carrier, LAX3, in adjacent cortical
cells after the degradation of the IAA14/SLR repressor (b). The resulting LAX3-dependent accumulation of auxin causes the upregulation of expression of a distinct set of
CWR enzymes that initiate cortical cell separation (c). Auxin derived from later stage primordia in closer proximity to the overlaying epidermal cells induces the expression
of LAX3, and then CWR genes (d), causing cell separation and ultimately resulting in lateral root emergence. Hence, emergence of LRP through the outer root tissues is a
highly regulated process involving a complex transcellular auxin signalling network. Abbreviations: P, pericycle; End, endodermis; C, cortex; Epi, epidermis. Adapted from
Ref. [67].
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404
It was recently reported that auxin originating from
developing LRP acts as a local inductive signal that reprograms
adjacent cells, causing their cell walls to separate
[67]. LAX3 (LIKE AUX1-3) regulates the expression of
several CWR enzymes. These include a pectate lyase
(PLA2); polygalacturonase (PG); xyloglucan:xyloglucosyl
transferase (XTR6); expansin (EXP17); and glycosyl hydrolase
(GLH17) [68–72]. The PG and PLA2 enzymes are
likely to be particularly important for cell separation
during lateral root emergence because they cleave demethylated
pectin, a substrate that is enriched in the
middle lamella of root cells overlaying LRP. Intriguingly,
the endodermal-expressed IAA3/SHY2 protein regulates a
set of CWR enzymes that overlaps but is distinct from the
set of enzymes regulated by LAX3; this is likely to reﬂect
differences in cell wall composition between lateral and
endodermal root tissues.
The restricted pattern of LAX3 expression in outer root
tissues is important for the localized induction of CWR
genes such as PG and XTR6. This regulatory arrangement
ensures that the auxin-dependent induction of components
of the cell separation machinery is strictly controlled and
does not compromise the integrity of the parent root. High
levels of auxin are known to cause cell separation in
Arabidopsis roots [22,73]. However, the authors of these
studies observed that cells were sloughed off abnormally,
whereas under normal conditions cell separation is highly
localized. The model for lateral root emergence (Figure 4)
helps to explain how the activities of auxin-regulated CWR
enzymes are precisely targeted during lateral root emergence
without compromising the integrity of surrounding
root tissues.
This study also revealed that the developmental progression
and emergence of LRP are strictly coordinated.
Mutants that disrupt the lateral root emergence process
also impact the developmental progression of LRP, as
illustrated by the increased proportion of stage I primordia
in lax3 mutant roots [67]. The endodermis and cortex
tissues form concentric circles of cells around the pericycle
in which LRP initiate (Figure 1). Targeting cell separation
between endodermal and cortical cells overlaying the
stage I primordia would help to reduce the tissue tension
created by these encircling tissues, enabling meristematic
cells to divide periclinally and give rise to a new second
layer that will protrude out into the parental root (Figure
4).
The lax3 mutant, which displays disrupted lateral root
emergence, exhibits signiﬁcantly increased numbers of
LRP compared to the wild type [67]. The delay in developmental
progression of lateral roots in the lax3 mutant
background is likely to cause leaf-derived auxin (which
promotes lateral root emergence [74]) to accumulate to
supra-optimal levels in the root pericycle, stimulating
the ectopic initiation of new primordia. This hypothesis
is consistent with results obtained from stochastic
modelling of root branching that revealed feedback
regulation between lateral root initiation and emergence
[25]. We conclude that lateral root emergence is a highly
regulated process employing a common signal to synchronize
lateral root development and emergence pro-
cesses.
Lateral root meristem activation and elongation are
dependent on auxin
As the new lateral root protrudes through the epidermal
layer, activation of the meristem is thought to occur.
Although lateral root meristems have the ability to produce
auxin [75], it is not known at which stage the primordium
acquires independence from the primary root for
auxin supply. The arrest of post-emergence development in
the alf3 mutant can be rescued by exogenous application of
auxin or indole precursors [76]. It is therefore possible that
the ability to synthesize its own auxin could coincide with
or even trigger meristem activation. Nevertheless, acropetal
transport of auxin from the shoot and/or primary root
sources also seems to be necessary for the continued development
and elongation of the lateral root. Perturbation
of this acropetal auxin transport stream in the mdr1
(multiple drug resistance1) mutant leads to reduced
elongation or arrested lateral roots [77].
Future developments
Our understanding of lateral root development has
advanced considerably over the past ﬁve years. Recent
research has thrown new light on the regulation of lateral
root initiation and patterning and provided new insight
into the molecular basis of pre- and post-initiation processes,
such as priming of founder cells and organ emergence,
respectively.
Genetic studies have played, and will continue to play, a
vital role in the molecular dissection of lateral root development
in Arabidopsis. Although a great deal of our
current knowledge comes from forward genetics screens, it
is becoming increasingly difﬁcult to identify new mutants
using this approach because obvious phenotypes are being
exhausted from root architecture screens. By contrast,
thanks to the availability of high resolution spatiotemporal
transcript maps of individual cell types and developmental
zones in the root, reverse genetic screens are likely to
become much more important [78–80]. For example, the
catalogue of genes expressed in the xylem pole pericycle
cells [54] and in the outer tissues [66] will greatly aid
the identiﬁcation of new genes regulating lateral root
initiation and emergence processes, respectively. Conditional
approaches are likely to aid the discovery of novel
genes. For example, inducible RNA interference and
chemical genetic approaches [81] will aid identiﬁcation
and characterization of genes whose loss-of-function
mutations either exhibit embryo lethality or redundancy,
respectively. In addition to these new tools and approaches,
we need to take advantage of the existing resources for
studying primary root development. For example, welldescribed
primary root patterning genes like SCARECROW
[6], SHORTROOT [82], WOX [27,83] and PLETHORA [84]
are expressed during lateral root development, suggesting
that these genes might play important roles in patterning
LRP. Although over 70 Arabidopsis mutants with lateral
root defects have been described [9], only a small proportion
have been well characterized at the morphological level
(Table 1).
Impressive progress has been made in determining the
role of auxin during lateral root development. Progress has
also recently been made in studying the regulation of
Review Trends in Plant Science Vol.14 No.7
405
lateral root development by other hormones such as ethylene
and abscisic acid [85,86] and nutrient signals like
phosphate and nitrate [44,87]. A key challenge will be to
integrate these signalling pathways with auxin [88]. The
increasing knowledge of pre- and post-initiation events will
aid the construction of a regulatory network encompassing
all of these signals and their transduction pathways within
a multi-cellular context. Building and then validating
these regulatory networks will be greatly facilitated by
adopting an integrative systems biology approach. Recent
efforts to incorporate a modelling approach into Arabidopsis
root research illustrate the utility of this application
[24,26].
Acknowledgements
This work was supported by a Marie Curie Intra-European Fellowship
within the 7th
European Community Framework Programme (B.P.), the
Special Research Fund of Ghent University (pre-doctoral fellowship to
B.D.R.), the European Molecular Biology Organization Young
Investigator Program (E.B.), Junta de Extremadura (I.C.), Institut de
Recherche pour le De´veloppement (L.L.), Agropolis Fondation (n807024 to
L.L. and M.J.B.) and by grants from the Interuniversity Poles of
Attraction Program-Belgian Science Policy (P5/13 – M.J.B. and T.B.).
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1621–1626
Plant Science Conferences in 2009
International Conference on Retrograde Signalling in Plants
1–3 October, 2009
Berlin, Germany
http://www2.hu-berlin.de/dfg-forschergruppe804/international-conference/
Interdrought-III
11–16 October, 2009
Shanghai, China
http://www.interdrought.org
9th IPMB Congress
25–30 October, 2009
St Louis, MO, USA
http://www.ipmb2009.org.
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