Opinion

A quiescent path to plant longevity

Jefri Heyman, Robert P. Kumpf, and Lieven De Veylder
Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie (VIB), and Department of Plant Biotechnology and
Bioinformatics, Ghent University, 9052 Gent, Belgium

The giant sequoia and the bristlecone pine trees are

capable of living up to several hundreds or even thousands of years. Plants achieve this longevity by regenerating stem cells capable of giving rise to all
differentiated cells. Plant stem cells reside in specific
niches with high mitotic activity that are known as
meristems. Remarkably, at the center of the root stem
cell niche (SCN) resides a group of mitotically inactive
cells known as the quiescent center (QC). Recent studies
suggest that stress-related phytohormones and DNA
damage can initiate QC cell division, resulting in the
replenishment of stem cells surrounding the QC. We
therefore propose that the QC represents a pool of
backup cells that serve to replace damaged stem cells,
thereby contributing to plant longevity.
QC: the key to plant longevity
For humans, reaching the age of 100 years is considered to
be quite an achievement. However, many plant species,
including trees such as the bristlecone pine and the giant
sequoia, easily live up to several thousand years. Their
secret lies in the way they generate new cells. Plant cell
division is frequently confined to specialized regions called
meristems, of which the center contains stem cells capable
of self-renewal and differentiation into specific cell types.
The center of the root SCN contains a small group of cells
that exhibit a much lower proliferative activity compared
to that of their surrounding stem cells, marking a QC [1].
Indeed, the QC cell cycle length was found to exceed three
days [28], being three- to six-fold longer than that of its
surrounding stem cells [9]. These QC cells are considered
to preserve the SCN and hence the longevity of plants.
Animals also have quiescent cells that might contribute to
SCN longevity, such as in the hair follicle, gut, and the bone
marrow [10]. However, the relatively short lifespans of
mammals in relation to those of many plants suggests
that the role of the quiescent cells in stem cell maintenance
might be more robust in plants. A putative reason for this
higher robustness is the fact that plants have a sessile
lifestyle. They are unable to remove themselves from
particular stressful environments, in contrast to animals
that can easily escape harmful situations. Thus, compared
to animals, plants might have evolved more efficient SCN
rescue mechanisms. We review here the different regulatory pathways determining QC establishment, discuss the
Corresponding author: De Veylder, L. (livey@psb.vib-ugent.be).
Keywords: peptide signaling; quiescent center; root; stem cell niche; meristem.
0962-8924/
2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tcb.2014.03.004

need for stem cell quiescence, and put forward the hypothesis that stress-induced QC cell division might be the basis
of plant longevity.
The root SCN
At the tip of roots, new cells are continuously produced by
the apical SCN through oriented cell divisions, resulting in
a radial organization of different root cell types
(Figure 1A). The most distal stem cells produce the columella tissue, the most proximal cells produce the root
vasculature tissue, and the laterally situated cells give
rise to both cortical and endodermal cell files or the lateral
root cap and epidermis. At the center of these stem cells,
and in direct contact with them, are the QC cells [11]. The
number of QC cells can vary widely across plant species,
ranging from about four to eight in Arabidopsis thaliana
[1214] to up to 5001200 in maize (Zea mays) [4,15]. After
their ablation, neighboring stem cells differentiate, indicating the importance of direct cellcell contact between
the QC and surrounding stem cells, and illustrating that
QC cells are required to maintain stem cell fate [5]. Genetic
experiments revealed that both QC establishment and cell
division are determined by an interplay between phytohormones, transcriptional activators, small peptides, and
targeted protein turnover, which together constitute a
complex network determining QC and stem cell specification [1619].
An interplay between hormones and transcription
factors (TFs) controls SCN specification
The main force driving QC establishment is the phytohormone auxin. Auxin efflux carriers, such as PIN-FORMED 1
(PIN1), transport auxin through the vascular cells in a
polarized manner from the shoot toward the most distal
part of the root meristem [2022], where it is redistributed
in the columella cells. Auxin subsequently flows back to the
outer and more mature tissues in the root, where it is
recycled into vascular cells (Figure 1A). This reverse fountain establishes an auxin maximum at the root meristem,
thereby specifying QC cell identity [20]. Indeed, mutation
of the PIN genes that drive basal auxin transport results in
loss of QC specification. The auxin maximum triggers the
expression of the PLETHORA (PLT) genes, which are
members of the group of AP2 (APETALA 2)/ERF (ETHYLENE RESPONSE FACTOR)-type TFs. Matching the auxin
gradient, PLT transcription displays a graded pattern
within the root meristem, reaching maximum levels in
the QC. In turn, PLT proteins control PIN expression,
thereby providing a positive feedback loop that contributes
to a stable auxin maximum [19,23,24]. Therefore, similarly
Trends in Cell Biology, August 2014, Vol. 24, No. 8

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Trends in Cell Biology August 2014, Vol. 24, No. 8

Key:

(A)
Auxin

Quiescent center

Epidermis

Vascular ssue

Cortex

Pericycle

Lateral root cap

Endodermis

Columella

Ground ssue

Columella inials

SCR

SCR

xin
Au

Au
xin

(B)

SHR
WOX5
ACR4
CLE40
TRENDS in Cell Biology

Figure 1. Arabidopsis thaliana root meristem and stem cell niche (SCN) organization. The color codes indicate the respective root tissues, and the white encircled region in
B indicates the SCN. (A) Organization of the Arabidopsis thaliana root meristem. The large white arrow indicates the graded PIN-FORMED (PIN)-mediated auxin flow from
the stele toward the root tip. In the columella, auxin is transported upward, where it is funneled back into the center of the root. This reverse fountain auxin flow
establishes an auxin maximum in the SCN that defines the position of the quiescent center (QC). (B) Molecular control of SCN establishment. SHORTROOT (SHR) is
expressed in the root vascular cells but its gene product moves to the endodermal cell files, where it activates SCARECROW (SCR) expression. In combination with a
maximum in PLETHORA (PLT) levels (not shown), SCR defines the WUSCHEL-RELATED HOMEOBOX 5 (WOX5) expression domain, marking the QC cells. Expansion of this
expression domain to the columella stem cells is prohibited by the activity of the CLE40 (CLAVATA3/EMBRYO SURROUNDING REGION 40)ARABIDOPSIS CRINKLY 4
(ACR4) peptidereceptor signaling module.

to PIN loss, loss of PLT1/PLT2 gene function results in the

loss of QC cell identity. By contrast, overexpression of
PLT2 during embryogenesis leads to the establishment
of ectopic QCs and root stem cells throughout the seedling,
which can result in the formation of ectopic roots [19].
In parallel to the auxinPLT pathway, QC specification
involves the action of two GRAS [named from GIBBERELLIC-ACID INSENSITIVE (GAI), REPRESSOR of GAI
(RGA) and SCARECROW (SCR)]-type TFs SHORTROOT (SHR) and SCR (Figure 1B). SHR is expressed in
the root vasculature, and moves to the surrounding tissue
layer to activate SCR transcription [2528]. Expression of
SCR in turn initiates QC specification [29,30]. Mutant
analyses indicate that both SHR and SCR need to be
present to establish QC cell fate [31]. It is the combinatorial activity of PLT and SHR/SCR that provides the longitudinal and radial position of the QC, respectively [32].
Furthermore, the homeodomain TF WUSCHEL-RELATED HOMEOBOX 5 (WOX5), which is transcriptionally
regulated by SCR, is also required for QC functionality
[8] (Figure 1B). WOX5 is expressed exclusively in the QC,
and loss of WOX5 function results in the enlargement of
QC cells and accelerated differentiation of columella stem
cells [8].
Whereas a wealth of information is available on the
mechanisms that contribute to QC identity and maintenance, little is known regarding the factors that control QC
cell division. An important player working together with
SCR is the RETINOBLASTOMA-RELATED (RBR) protein [33,34] (Figure 2). RBR is the plant counterpart of the
444

mammalian RB protein, known for its role in blocking G1to-S entry through its association with and inhibition of
E2F TFs. Recent work shows that cell-specific RBR silencing triggers QC cell division, indicating that RBR inhibits
the proliferation of QC cells [35].
Peptide hormones in SCN establishment
Besides traditional hormones, peptide hormones are crucial for the organization of the root SCN. Different peptide
hormone families are present in Arabidopsis, all of which
are synthesized as precursor peptides requiring posttranslational modifications, such as proteolytic processing,
to release the mature peptide to the apoplast. The first
group comprises the CLE (CLAVATA 3/EMBRYO SURROUNDING REGION) peptides, which are similar to
CLAVATA peptides known for their role in cell homeostasis of shoot stem cells [36]. One particular member, CLE40,
plays a prominent role in the establishment of the root
SCN (Figure 1B). It is expressed in the columella and binds
the receptor-like kinase ARABIDOPSIS CRINKLY 4
(ACR4), which is present in columella stem cells and
controls stem cell maintenance as well as the number of
arising columella cells. Lack of a functional ACR4 receptor
results in an increased stem cell self-renewal and delayed
differentiation into columella cells [37]. Further evidence
suggests that the CLE40ACR4 signaling cascade negatively influences WOX5 expression because loss of CLE40
or ACR4 results in an expansion of the WOX5 expression
domain [38]. Therefore, the balance of QC cell identity and
the number of differentiated columella stem cells is

Opinion

Trends in Cell Biology August 2014, Vol. 24, No. 8

RGF/GLV

SCR
CCS52A2
APC/C
PLT

WOX5
QC cell
maintenance
RBR

Auxin

TPST

QC cell
proliferaon

SCR

ERF115

PSK5

TRENDS in Cell Biology

Figure 2. Pathways controlling the balance between quiescent center (QC) cell maintenance and division. PLETHORA (PLT) together with SCARECROW (SCR) determine QC
cell specification, as indicated by the occurrence of WUSCHEL-RELATED HOMEOBOX 5 (WOX5) expression (GFP-positive cells in the insets). CELL CYCLE SWITCH 52
(CCS52A2)-activated Anaphase Promoting Complex/Cyclosome (APC/C) maintains QC cell quiescence. By contrast, expression of the transcription factor (TF) ETHYLENE
RESPONSE FACTOR 115 (ERF115), an APC/CCCS52A2 target, triggers QC cell division through the transcriptional activation of the PHYTOSULFOKINE 5 (PSK5) peptide
precursor gene. Activation of the PSK5 peptide requires sulfation by TYROSYLPROTEIN SULFOTRANSFERASE (TPST). TPST is also required to activate the ROOT GROWTH
FACTOR (RGF)/GOLVEN (GLV) peptides, which are known to affect PLT levels, contributing to QC cell maintenance. Finally, RETINOBLASTOMA-RELATED (RBR) in complex
with SCR represses QC cell division. The key molecules that activate the cell cycle still need to be identified (indicated by question marks).

partially acquired through a peptidereceptor signaling

component in these columella stem cells.
A second group of peptide hormones consists of ROOT
GROWTH FACTORS (RGF)/GOLVEN (GLV) [17,39],
PLANT PEPTIDE CONTAINING SULFATED TYROSINE 1 (PSY1) and PHYTOSULFOKINE (PSK) [40,41]
that mediate different functions in SCN organization and
maintenance [17]. In contrast to other peptide hormones,
they require activation through tyrosine sulfation by TYROSYLPROTEIN SULFOTRANSFERASE (TPST) [42].
TPST is ubiquitously expressed throughout the plant,
although increased transcript levels can be found in the
root meristem, particularly in the SCN, which corresponds
with the high activity of the RGF/GLV, PSY, and PSK
peptides in this region. In addition, tpst mutants show an
increase in root QC cell number, together with a disorganized SCN. The mutation of TPST appears to have a
negative effect on PLT1 and PLT2 at both the transcriptional and post-translational level, suggesting a putative
link between sulfated peptide signaling and PLT-mediated
control of SCN establishment [43] (Figure 2).
The tpst mutant QC cell division and stem cell organization phenotypes can be partially restored through the
addition of RGF/GVL peptides [17], suggesting that RGF/
GLVs repress QC cell division. By contrast, recent work
indicates a positive effect of PSK peptides on QC cell

proliferation [44]. Therefore, it is likely that maintenance

of a functional SCN requires a tight balance of different
peptides, and that tipping the balance of (one of) these
peptides might favor division rather than quiescence, or
vice versa. Currently, only the receptors for the PSK and
PSY1 peptides have been characterized [41,45,46]. The
Arabidopsis genome encodes two PSK receptor genes,
PSKR1 and PSKR2, of which the former has been suggested to play a predominant role in PSK peptide signal
transduction [47], and whose expression can be found in
the root tip [40]. Identification of the currently unknown
RGF/GVL receptor will undoubtedly contribute to the
elucidation of putative crosstalk mechanisms between different peptide hormones.
Protein degradation and QC cell division
Next to the involvement of RBR and peptidereceptor
modules, protein degradation appears to be essential in
controlling QC cell division. A study of the CELL CYCLE
SWITCH 52 (CCS52) proteins, which are activators of the
highly conserved Anaphase Promoting Complex/Cyclosome (APC/C), revealed the necessity for APC/C activity
in QC cell maintenance [18]. APC/C is an E3 ubiquitin
ligase that controls cell division and differentiation by
targeting cell cycle proteins for proteasomal degradation.
The Arabidopsis genome encodes two different A-type
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Trends in Cell Biology August 2014, Vol. 24, No. 8

CCS52 isoforms, named CCS52A1 and CCS52A2 [48]. In

the Arabidopsis root, APC/CCCS52A1 accumulates in the
root transition zone, where it targets the mitotic cyclin
CYCA2;3 for destruction, pushing these cells toward differentiation [49]. By contrast, APC/CCCS52A2 activity in the
root meristem appears to be restricted to the QC cells.
Mutation of CCS52A2 activates QC cell division shortly
after germination, triggering a loss of QC cell identity [18].
Therefore, it seems that APC/CCCS52A2 activity is required
to repress QC cell division, thereby preventing exhaustion
of the SCN.
A screen for CCS52A2 copurifying proteins led to the
identification of ETHYLENE RESPONSE FACTOR 115
(ERF115) as the rate-limiting factor for QC cell division
that is targeted for destruction by APC/CCCS52A2 [44].
ERF115 belongs to the family of TFs that are involved
in the transduction of a wide variety of (a)biotic stresses,
including pathogens [5052], cold [53], drought [54,55],
water submergence [5658], and reactive oxygen species
signaling [59]. Chromatin immunoprecipitation of ERF115
combined with transcript profiling identified the gene
encoding the peptide growth hormone precursor PSK5 to
be a direct transcriptional target of ERF115 [44]. Thus,
APC/CCCS52A2 appears to control PSK-mediated QC cell
proliferation by regulating ERF115 abundance (Figure 2),
connecting APC/C activity with peptide hormone signaling.
To divide or not to divide?
When a QC cell divides it generates a new stem cell that
pushes an older one out of the SCN. Thus, as the source of
stem cells, the QC cells bear the genetic responsibility for
all arising root cells during the plant lifecycle. The low
proliferation rate of QC cells might represent a mechanism
to maintain an error-free genome because every round of
replication harbors the possibility of replication errors,
which in turn could alter the genomic integrity of the stem
cells. Interestingly, whereas proliferative plant stem cells
and their daughter cells appear to be hypersensitive to
DNA-damaging agents such as radiomimetic bleomycin
and zeocin, or genotoxic UV-B radiation, the QC cells
appear to be highly resistant [60,61]. The increased

Undamaged SCN

Stem cell death

expression of DNA repair genes in QC cells might account

for this increased tolerance to stress [44], as could the low
division rate, indicated by the observation that QC cell
proliferation, induced through depletion of RBR, renders
them sensitive to DNA damage [35]. It is likely that going
through the DNA replication process renders plants sensitive to DNA damage-inducing agents. Similarly, root
growth of RBR-depleted plants is impaired after treatment
with a DNA double-strand break-inducing drug [35].
Strikingly, although QC cells display a low proliferation
rate under normal growth conditions, they initiate cell
division after treatment by plant hormones such as ethylene, jasmonate, brassinosteroids, and cytokinins [6,6264].
Whereas increased levels of ethylene, jasmonate, and
brassinosteroids have been shown to transmit a stress
response signal [6,50,65,66], cytokinins might play an
indirect role in stress perception by altering the endogenous hormone balance [67]. Thus, although QC cells are
more resistant to DNA damage, they engage cell division
pathways after perceiving stress signals, and this may
render them susceptible to replication-associated DNA
mismatches or damage. A possible answer to this DNA
damage susceptibility of QC cells might be the mortal
strand hypothesis which proposes that during cell division the duplicated chromosomes segregate non-randomly
over the two daughter cells, resulting in one cell maintaining an original and intact DNA template, and the other
cell receiving a copy holding putative replication errors
[68]. Such non-random DNA template segregation has
been demonstrated in Escherichia coli and mammalian
cells [69,70]. Likewise, upon QC cell division, the stem cell
maintaining the QC cell fate might preferentially retain
the original DNA template, whereas the newly synthesized
DNA is passed on to the new stem cell initial. If this stem
cell accumulates genomic damage it might be pushed out of
the SCN through division of a QC cell harboring an undamaged DNA copy, keeping the SCN cells error-free.
Interestingly, the expression of the cell division ratelimiting ERF115 gene in the QC is induced by the DNA
double-strand break-inducing drug bleomycin. This induction results in the formation of new QC cells, and consequently the re-establishment of a normal SCN, allowing

QC cell division

Recovery

Recovered state
TRENDS in Cell Biology

Figure 3. Proposed model for stem cell replenishment through quiescent center (QC) cell division. At the left, an undamaged root meristem is shown with the QC cells
marked in dark green. Following exposure of the root to DNA damage-inducing agents, the stem cells surrounding the QC undergo cell death (depicted in red). Stem cell
niche (SCN) recovery is initiated by the activation of QC cell division. The newly generated cells with QC identity (shown in light green) replace the dead stem cells, thereby
replenishing the stem cell pool. As recovery advances, QC cell division diminishes and normal SCN organization is restored.

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Opinion
Box 1. Outstanding questions
 Which physiological factors refrain QC cells from frequent cell
division?
 Does loss of cell division quiescence of QC cells affect root
growth?
 What are the molecular components and signaling pathways that
link stem cell replacement with the cell cycle machinery?
 How do QC and non-QC stem cells communicate?
 Does the mechanism of stem cell replacement observed for the
root hold true for shoot tissue?
 Do the molecular components that control QC cell division also
account for de novo QC cell re-establishment?

the roots to resume growth after removal of the DNAdamaging agent. By contrast, plants harboring a dominant
negative ERF115 allele display impaired QC cell division
activity, experience a collapse of the root meristem after
bleomycin-induced stem cell death, and recover less efficiently after its removal [44]. These observations raise the
appealing hypothesis that stress-induced QC cell division
serves to replace damaged neighboring stem cells. In
agreement, pioneering work performed in maize has demonstrated that QC cells are more resistant to X-rays, likely
due to quiescence [71], and that damaged root meristem
cells are replaced by cells originating from QC cell division
[72]. It is thus possible that the QC cells serve as a pool of
highly protected backup cells that are tolerant to different
kinds of stress due to their quiescence, and that are called
upon when surrounding stem cells are in need of replacement (Figure 3). Replacing stem cells with a damaged
genome by cells harboring a perfect copy from the QC cells
could limit the propagation of deleterious mutations in the
organism, and therefore contribute to the longevity of
plants.
Concluding remarks
Taken together, it appears that QC cells might form a pool
of unspecialized immature cells that have the potential to
replenish damaged stem cells. Although many questions
remain, this mechanism of replacing damaged stem cells
by fresh ones might lie at the heart of the secret of plant
longevity (Box 1). Mammalian quiescent stem cells also
may contribute to SCN durability. Hematopoietic quiescent stem cells, for example, can remain dormant up to 145
days, retaining the ability to activate division under injury
or stress conditions [73]. Remarkably, after death of a
quiescent stem cell, mitotically active stem cells are capable of acquiring dormancy, replacing the lost quiescent cell
[10]. Again, these observations might be reminiscent of
plants because loss of QC cells results in a quick reestablishment of a new QC cell derived from the stele stem
cells [74]. Surprisingly, when all root stem cells are excised,
plants easily regenerate a completely new SCN within a
few days [75]. Therefore, the SCN regeneration mechanism
might be more potent in plants compared to animals.
Although PLT proteins are key regulators of SCN establishment, PLT mutants appear to maintain their regenerative capabilities when their root tips are excised [75].
Thus, the identity of the regulators that control QC cell
re-establishment and cell division remains unknown, but

Trends in Cell Biology August 2014, Vol. 24, No. 8

they might hold the key to unravel the mystery of the

thousand-year life expectancy of certain plants.
Acknowledgments
The authors thank Annick Bleys for help in preparing the manuscript. This
work was supported by grants from the Research Foundation-Flanders
(G.0C72.14N) and the Interuniversity Attraction Poles Programme (IUAP
P7/29 MARS), initiated by the Belgian Science Policy Office.

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