Available online at www.sciencedirect.
com
Plant primary meristems: shared functions and regulatory
mechanisms
Yvonne Stahl and Rüdiger Simon
Primary plant meristems are the shoot and root meristems that
are initiated at opposite poles of the plant embryo. They contain
stem cells, which remain undifferentiated, and supply new cells
for growth and the formation of tissues. The maintenance of a
long-lasting stem cell population in meristems is achieved by
signal exchange between organizing regions and the stem
cells, and also by feedback signals emanating from
differentiating cells. Related peptide signals that make use of
different receptor classes were found to control the stem cell
populations in both meristem types by regulating evolutionarily
conserved homeodomain transcription factors. The precise
interplay of auxin and cytokinin signaling pathways is central to
keep cells in the meristem, or direct them toward
differentiation.
Address
Institut für Genetik, Heinrich-Heine Universität, Universitätsstr. 1,
D-40225 Düsseldorf, Germany
Corresponding author: Stahl, Yvonne (yvonne.stahl@uni-duesseldorf.de)
and Simon, Rüdiger (ruediger.simon@uni-duesseldorf.de)
Current Opinion in Plant Biology 2010, 13:53–58
This review comes from a themed issue on
Growth and Development
Edited by Dominique C. Bergmann and Andrew J. Fleming
Available online 15th October 2009
1369-5266/$ – see front matter
# 2009 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2009.09.008
Introduction
The shoot and root meristems of higher plants are the
microenvironments that allow stem cells to prosper. Stem
cell divisions generate new cells that are displaced from
the stem cell niche, undergo several additional rounds of
cell divisions as transit-amplifying cells (TA cells), and
are then permitted to differentiate into specific cell types
(Figure 1) [1]. The past two years have brought new
insights into the roles of genes controlling cell behavior in
the two primary meristems, and have unveiled sim-
ilarities between the molecules and mechanisms, hinting
at their shared evolutionary origin. Attention will be
focused on recent advances in understanding peptide
signaling pathways that restrict stem cell populations,
and on the crosstalk between phytohormone pathways
that affect meristem cell proliferation and the exit into
differentiation.
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Making the shoot niche
The shoot apex harbors stem cells at the meristem tip in
the central zone (CZ). The surrounding peripheral zone
carries more rapidly dividing TA cells that can enter a
differentiation pathway. Only a limited number of stem
cells are maintained, and their daughters are shifted
toward the periphery during development. In Arabidopsis,
niche function is provided by underlying cells that form
the organizing centre (OC) and express the homeodomain
transcription factor WUSCHEL (WUS) (Figure 1A,B) [2].
Known target genes directly regulated by WUS are ARA-
BIDOPSIS RESPONSE REGULATORS (ARRs) that cre-
ate a negative feedback loop for cytokinin signaling [3].
The importance of cytokinins for the stem cell niche was
recently re-emphasized by the discovery of lonely guy (log)
mutants from rice, which arrest shoot meristem growth
[4], comparable to wus mutants. LOG is expressed in the
CZ and converts inactive cytokinin nucleotides into the
active hormone. However, why WUS induces stem cell
fate only at the distal meristem tip, but not directly in the
OC is not yet understood. New misexpression exper-
iments now revealed that the ARGONAUTE related
protein ZWILLE (ZLL) is required for WUS function
[5]. Only ZLL expression in the vascular domain (under-
neath the OC) rescues the meristem defects of zll
mutants, suggesting that ZLL may contribute to the
generation of a mobile signal in the vasculature that
interacts with the stem cell inducing activity of WUS.
miRNAs are obvious candidates, and both zll and ago1
mutants show increased miRNA165/166 levels in the CZ
of the meristem, which could target HD-ZIPIII family
members for cleavage [6]. Still, only cells at the distal tip
of the meristem appear to be responsive to these com-
bined signals, and auxin may have a role in defining this
position. Although shoot stem cells appeared auxin-insen-
sitive using the DR5::GFP reporter, auxin was found
enriched in the central zone using biochemical methods
[7], and the auxin biosynthetic gene TRYPTOPHAN
AMINOTRANSFERASE OF ARABIDOPSIS1 (TAA1) is
highly expressed in the stem cell domain [8,9].
Feedback regulation of stem cell fate in the
shoot
The shoot stem cells deliver a negative feedback signal to
WUS by secretion of the 13 amino acid CLAVATA3
(CLV3) glycopeptide [10,11], which was shown to bind
to the extracellular leucin-rich repeat (LRR) domains of
the CLAVATA1 (CLV1) receptor kinase [12]. A second
pathway for CLV3 signaling comprises the LRR carrying
receptor-like protein CLAVATA2 (CLV2) [13] and the
Current Opinion in Plant Biology 2010, 13:53–58
54 Growth and Development

Figure 1

Regulation of stem cell fate in the shoot and root meristem. (A and C) Schematic representation of the shoot apical meristem (A) and root meristem (C).
Stem cells are outlined in bold. Gene expression domains are color coded. TA = transit-amplifying cells; Diff. = cell differentiation. (B, D and E)
Regulatory networks of proteins and phytohormones (italicized) involved in controlling stem cell fate and differentiation (boxes) in the shoot (B) and root
(D and E) meristem. Arrows indicate positive regulation; barred lines indicate negative regulation.

receptor-like kinase CORYNE (CRN) [14], which may
interact via their transmembrane domains to reconstitute
a functional receptor. Genetic dissection of CLV3 sig-
naling indicates that the CLV1 and the CLV2/CRN
receptors can act in parallel [14]. That CLV2 and
CRN (but not CLV1) also function in root meristem
development supports the idea of functional indepen-
dence [14,15]. Furthermore, CLV1-like receptor
kinases were identified in many species, reaching from
higher plants to pteridophytes and moss [16], whereas
CLV2 and CRN seem to be specific for higher plants with
complex stem cell systems. Both pathways later converge
again to repress the activity of POLTERGEIST (POL)
and POLTERGEIST-LIKE (PLL1), two related
protein phosphatases 2C that positively regulate WUS
expression [17], but are also essential to initiate the
embryonic root meristem [18]. This feedback regulation
of the stem cell domain tolerates a wide range of CLV3
levels [19], and allows to vary meristem sizes [20] in
response to environmental triggers, such as flowering
signals.
Terminating the stem cell niche
Floral meristems lose WUS expression due to AGAMOUS
(AG) activity, and stem cells are consumed for carpel
formation. Surprisingly, AG is expressed in the center
of the flower from stage 3 onwards where it promotes the
formation of both stamen and carpel, but overlaps with
WUS expression until stage 6, before WUS RNA disap-
pears from the floral meristem [21]. A recent study now
solved this apparent enigma by showing that the AG
protein binds to the promoter region of KNUCKLES
(KNU), encoding a zinc-finger type transcriptional repres-
sor [22], and activates KNU expression [23]. KNU is then
able to switch off WUS transcription by an unknown
mechanism, because direct interaction of KNU with
the WUS promoter has not been shown. Interestingly,
AG is already present for two days before KNU transcrip-
tion increases. This temporal delay is explained by the
requirement for removal of repressive H3K27me3 marks
from the KNU promoter region to allow KNU transcrip-
tion. Cell divisions could be essential to allow the removal
of these marks, which would elegantly link the timing of

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 Functions and regulatory mechanisms of meristems Stahl and Simon 55
WUS downregulation and stem cell loss to growth and
proliferation of the floral meristem.
Integrating the shoot stem cell niche with
organ development
Several HD-ZIPIII proteins, homeodomain transcription
factors carrying a leucine zipper, have dual functions not
only to maintain the niche and the SAM, but also to
promote adaxial identity in lateral organs [24]. At the
abaxial organ domain, HD-ZIPIII proteins are then
titrated by LITTLE ZIPPER (ZPR), which interferes
with their DNA binding activity [25]. This could suggest
a stepwise process of cell fate acquisition, reaching from
the meristem center to lateral positions, that depends on
HD-ZIPIII downregulation. Conversely, organ primordia
were now shown to signal back to the meristem center
and restrict stem cell fate [26]. FILAMENTOUS
FLOWER (FIL) and related YABBY transcription factors
promote abaxial organ identity, but FIL was also found to
confine meristem size non-cell-autonomously. Interest-
ingly, this requires expression of the transcription factor
LATERAL SUPPRESSOR (LAS) in the boundary be-
tween organs and the meristem, which may act there to
interpret a FIL-dependent signal, or generate a secondary
mobile molecule.
The root stem cell niche
It is hypothesized that the angiosperm root apical mer-
istem (RAM) has evolved from the shoot apical meristem
(SAM) probably as a consequence of the plants adap-
tation to changing environmental requirements, for
example nutrient and water uptake and anchorage
[27]. Therefore key regulational themes present in the
shoot are also expected and found important in the de-
velopment and regulation of the primary root meristem,
such as phytohormones, peptide ligands, and their recep-
tors as well as transcription factors. In the Arabidopsis
root, all cell layers are organized in a simple radial pattern
of clonal cell files. The root meristem can be divided into
three main regions: the meristematic zone, the
elongation zone, and the differentiation zone. The mer-
istematic zone contains the stem cell niche, comprising
the rarely dividing quiescent centre (QC) cells, which
control the surrounding stem cells (also called initial
cells) (Figure 1C–E). After division of an initial cell,
the daughter cell still in contact with the QC keeps its
stem cell fate, whereas the other cell becomes a transit-
amplifying cell (TA cell), and after further divisions and
expansion in the elongation zone acquires its destined
cell fate in the differentiation zone [28]. The transcrip-
tion factors SCARECROW (SCR), SHORTROOT (SHR),
and PLETHORA1 (PLT1) and 2, have essential roles in
QC establishment and stem cell maintenance [29].
Role of phytohormones in the root meristem
The phytohormones auxin, cytokinin, ethylene, and gib-
berellin are the major regulators of cell specification,
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proliferation, and expansion in the Arabidopsis root, and
extensive crosstalk between them can ensure rapid
responses to external and internal cues. Auxin controls
not only the initiation, stem cell niche formation, and
proliferation of cells in the proximal meristem but also
cell elongation and the differentiation of cells leaving the
meristem. The auxin maximum and gradient in the root
tip is self-organizing, and can be maintained by PIN auxin
efflux facilitators, which exhibit cell type specific polar
localization. This was nicely demonstrated by marker
gene and mutant analyses, and elaborated into a math-
ematical model [30]. The importance of organized auxin
transport is further highlighted by root regeneration stu-
dies [31]. Arabidopsis roots were able to restore excised
root tips, as long as auxin transport was uninhibited.
Notably, SCR, SHR, and PLT functions were only
required for indeterminate root growth, but not for organ
regeneration, indicating that pluripotent cells are also
found outside of the stem cell niche.
The established auxin gradient is interpreted by differ-
ential expression of PLT genes, where high PLT activity
promotes stem cell fate, low activity induces mitotic
activity of stem cell daughters, and lowest PLT levels
allow differentiation [32,33]. Besides auxin, expression of
PLT2 also requires GCN5 activity, a histone acetyltrans-
ferase that was previously shown to repress WUS and AG
transcription in floral meristems [34]. Mutants in GCN5
fail to maintain a QC and have shorter root meristems, but
these defects can be rescued by increased PLT2 expres-
sion. One possible target gene for PLT2 (and GCN5?) is
CYCLIN B1;1, which acts at the G2/M transition of the
cell cycle and could promote TA cell amplification [33].
Recessive mutations in the HIGH PLOIDY2 (HPY2)
gene, which encodes a SUMO E3 ligase, reduce root
meristem size and stimulate endoreduplication due to
reduced CDKB1 and 2 levels [35]. HPY2 expression is
activated by PLT1 and PLT2, and hpy2-1 mutants sup-
press PLT2 misexpression phenotypes. Together, this
suggests that auxin maintains the root meristem by acting
through PLT1/2 on HPY2 and CYCB1;1 to inhibit endo-
cycles and promote mitotic cell divisions.
BREVIS RADIX (BRX) was identified as a transcription
factor that controls a rate-limiting step in brassinosteroid
synthesis, and is strongly induced by auxin [36], thus
allowing for crosstalk between these two phytohormones.
brx mutants are impaired in meristem growth, but not in
organ initiation or tropisms. The BRX protein was now
found to colocalize with PIN1 at the plasma membrane,
and shuttle to the nucleus upon auxin treatment, where it
may execute a transcriptional response [37].
Cytokinins were found to promote cell differentiation at
the transition zone [38], and increasing cytokinin levels
reduce root meristem size and inhibit root growth. These
effects are due to the modulation of auxin distribution
Current Opinion in Plant Biology 2010, 13:53–58
56 Growth and Development
through regulation of PIN expression [39]. This crosstalk
between cytokinin and auxin is mediated by SHORT
HYPOCOTYL2 (SHY2), an IAA-class repressor of auxin
signaling [40]. ARR1, a primary cytokinin response
factor, was shown to bind the SHY2 promoter and activate
SHY2 transcription, which then represses PIN1 expres-
sion, causing auxin redistribution. Auxin, in turn, will
induce SHY2 degradation and thereby stabilize PIN
expression levels.
Ethylene promotes QC divisions and the production of
more columella cell layers independently of auxin [41]. In
the proximal meristem, ethylene reduces root meristem
size by inhibiting cell elongation — this effect is
mediated by the stimulation of auxin biosynthesis.
ACS proteins are rate limiting for ethylene synthesis,
and CULLIN3 (CUL3), a member of the Cullin–RING–
ubiquitin ligases, modulates ethylene production by tar-
geting them for degradation. cul3 hypomorphic mutants
show a reduced primary root meristem size and cell
number [42]. Recently, mutants in TAA1 and the close
homolog TAR2 were found to show root-specific ethylene
insensitivity and reduction in local auxin concentration,
thereby providing a further link between local auxin
synthesis and ethylene responses [8].
Gibberellin (GA) is known to control cell elongation in
the Arabidopsis root by the degradation of the growth
repressing DELLA proteins, and ethylene was pre-
viously shown to delay DELLA degradation [43].
DELLA proteins were now found to restrain meriste-
matic cell proliferation and cell division rate (without
influencing the stem cell niche) by increasing the levels
of cell cycle inhibitors [44]. Interestingly, only a subset
of the meristematic cells, namely the endodermal
cells, seem to dictate cell division and expansion also
in the adjacent root tissues and thereby control root
meristem size [45].
Feedback regulation of stem cell fate in the
root
Stem cell fate in the root is subject to feedback regulation
by gene functions related to those acting in the shoot. The
WUS-RELATED HOMEOBOX 5 transcription factor
(WOX5) is expressed exclusively in the QC cells and
maintains distal stem cell fate [46]. WOX5 and WUS
are close homologs and can substitute for each other if
expressed in the shoot or root niche, respectively [46]. In
contrast to angiosperms, gymnosperms carry only one
WUS/WOX5 ortholog, indicating that separate WUS and
WOX5 genes are a recent invention of the angiosperm
lineage [47]. Homologs of CLV3 in Arabidopsis are the 31
members of the CLV3/ENDOSPERM SURROUND-
ING REGION (CLE) family that carry a 14 amino acid
conserved region, the CLE motif, at their C-terminus
[48]. Two classes of peptides can be distinguished by
their effect upon application of synthetic peptides or their
Current Opinion in Plant Biology 2010, 13:53–58
overexpression on the root meristem size. Class A pep-
tides like CLV3, CLE19, and CLE40 reduce root mer-
istem size, whereas class B peptides, like CLE41 (TDIF),
have no effects on root meristem size, but instead
promote proliferation of vascular cells [49–52]. CLV2
was shown to be essential for CLE peptide induced root
restriction, but clv2 mutants exhibit no mutant phenotype
in the root, and the role of CLE peptides in root de-
velopment remained enigmatic.
Recently, CLE40 was shown to control stem cell prolifer-
ation in the distal root meristem. CLE40 is thought to be
secreted from differentiated columella cells (CCs) and to
repress WOX5 in the QC via its putative receptor ARABI-
DOPSIS CRINKLY4 (ACR4). ACR4 is expressed in the
distal meristem mainly in columella stem cells, and cle40
and acr4 mutants accumulate this stem cell type [53,54].
This root-specific CLE40/WOX5 pathway parallels the
activity of the CLV3/WUS signaling pathway in the shoot,
with the notable difference that the stem cell limiting signal
in roots, CLE40, originates from differentiated cells and not
from the stem cells like CLV3 in the shoot.
Conclusions
The past years have revealed how hormones can act
context dependent and exert location-specific effects
in both root and shoot meristems. One example is the
establishment of a stable auxin gradient in the root that
translates into differential expression of PLT genes [30].
More peptide signals have been discovered that control
not only stem cell behavior, but also cell differentiation.
Further, cell type specific gene expression analysis, first
pioneered for the dissection of transcriptional networks
in the root [55], has now been successfully employed also
for the shoot meristem [9]. We expect that a precise
picture for differential gene expression and transcrip-
tional hierarchies, linked up with signaling pathways, will
be drawn for both meristem types in the near future. One
of the challenges still lying ahead is to integrate these
numerous interactions and crosstalk mechanisms into
comprehensive models for shoot and root meristem
development.
Acknowledgement
We would like to acknowledge the support by the Deutsche
Forschungsgemeinschaft through SFB590.
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