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Plant stem cells: divergent pathways and common themes
in shoots and roots
Mary E Byrne, Catherine A Kidner and Robert A Martienssen
Stem cells in plant shoot and root meristems are maintained
throughout the life of the plant and produce somatic daughter
cells that make up the body of the plant. Plant stem cells can also
be derived from somatic cells in vivo and in vitro. Recent findings
are refining our knowledge of signaling pathways that define
stem cell fate and specify either shoot or root stem cell function.
New evidence also highlights a role for epigenetic mechanisms in
controlling stem cell fate.
Addresses
Cold Spring Harbor Laboratory, 1 Bungtown Rd, Cold Spring Harbor,
New York 11724, USA
e-mail: [email protected]
Current Opinion in Genetics & Development 2003, 13:551–557
This review comes from a themed issue on
Differentiation and gene regulation
Edited by Azim Surani and Austin Smith
0959-437X/$ – see front matter
ß 2003 Elsevier Ltd. All rights reserved.
daughter cell following division is not restricted but the
population of stem cells as a whole is maintained.
In plants, two populations of cells, one comprising the
shoot apical meristem and the other the root apical
meristem, give rise to the plant body. These meristems
are established early in embryogenesis, at opposite poles
of the embryo, and are maintained throughout the life of
the plant. Superficially, shoot and root meristems appear
dissimilar. Shoot meristems are located at the extreme tip
of the shoot and cell divisions contribute laterally and
basally to terminally differentiated tissue including
organs such as leaves. Root meristems, on the other hand,
are subterminal to a protective root cap. Most cell divisions contribute apically and basally to mature root tissues. Despite these differences, shoot and root meristems
each comprise a stepwise progression from totipotent to
determined cell fate. Different genetic pathways operate
to establish and maintain stem cell function in shoots and
roots, but common mechanisms may guide maintenance
of stem cells and acquisition of daughter cell fate.
DOI 10.1016/j.gde.2003.08.008
Abbreviations
AGO1 ARGONAUTE1
AS1
ASYMMETRIC LEAVES1
AS2
ASYMMETRIC LEAVES2
BLR
BELLRINGER
BOP
BLADE ON PETIOLE
BP
BREVIPEDICELLUS
CLV
CLAVATA
GAI
GIBBERELLIN-ACID INSENSITIVE
GRAS GAI, RGA, SCR
QC
quiescent center
RGA
REPRESSOR OF GAI
RNAi
RNA interference
SCR
SCARECROW
SHR
SHORTROOT
STM
SHOOT MERISTEMLESS
WUS
WUSCHEL
Introduction
Stem cells are defined both by self-renewal and by their
potential to differentiate to multiple cell types. Unicellular stem cell lineages occur in yeast: following division,
the mother cell attains the ability to switch mating type,
while the daughter cell does not. As in multicellular
organisms, this difference is specified, at least in part,
by asymmetric distribution of intracellular factors. In
multicellular organisms, stem cells can be maintained
as populations. External and internal influences establish
a specialized niche where the fate of any one individual
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Regulation of stem cell fate in the shoot
apical meristem
The organization of the shoot apical meristem in higher
plants has been defined classically by histology and more
recently by gene-expression patterns. Typically, discrete
cell layers can be distinguished. The outer layer (L1)
gives rise to outermost epidermal tissues. Either one or
two inner cell layers (L2 and L3) contribute to internal
ground tissue and vasculature of mature organs. Superimposed on this organization is a central zone of highly
vacuolated and slowly dividing cells that are readily
distinguished from more rapidly dividing, cytoplasmically
dense peripheral zone cells (Figure 1). Cells on the
margins of the peripheral zone are recruited into differentiating structures. Clonal analysis provides evidence
that a small number of stem cells persist for some time at
the apex contributing to many nodes through plant development. Other, presumably more peripheral, cells retain
some stem-cell capability in that they contribute to multiple but fewer nodes [1].
The homeobox gene WUSCHEL (WUS) is expressed very
early in embryogenesis and is rapidly confined to a few
cells in the inner layers of the central zone (Figure 2) [2].
Mutations in WUS result in termination of the shoot
meristem and loss of stem cell function whereas overexpression results in proliferation of stem cells [3,4]. WUS
acts in concert with a signaling complex comprising the
CLAVATA (CLV) genes. CLV1 encodes a leucine-rich
Current Opinion in Genetics & Development 2003, 13:551–557
552 Differentiation and gene regulation
Figure 1
(a)
(b)
Current Opinion in Genetics & Development
The shoot and root apical meristems. (a) The layered structure of the
shoot meristem. The outermost layer (L1) is shown in red, the second
(L2), in yellow. Blue marks the slowly dividing central zone. (b) The
root apical meristem is subterminal, but like the shoot apical meristem
has a layered structure and a center of slowly dividing cells (the QC,
shown in blue) surrounded by the initials for individual tissue (shown
in green).
repeat transmembrane kinase expressed in a small group
of cells immediately above the region of WUS expression
[5]. CLV1 interacts directly with another transmembrane
leucine-rich repeat protein, CLV2 [6]. A third member of
this pathway is CLV3, which encodes a secreted protein
expressed in outer layers of the meristem in a domain
partly overlapping that of CLV1 (Figure 2) [7]. CLV3 acts
non-cell autonomously to regulate WUS expression and
this is likely via interaction with CLV1 [8,9]. Mutations
in CLV genes result in an enlarged meristem and an
Figure 2
(a)
(b)
Current Opinion in Genetics & Development
The gene expression patterns underlying meristem organization.
(a) In the shoot CLV3 (green) is expressed in the central zone in the
upper layers. CLV1 is expressed subterminally (yellow) and overlaps
with WUS expression (red). WUS promotes CLV3 function in the cells
above it (arrow) and CLV3 signals through CLV1 to repress spreading of
WUS (bars). (b) in the root apical meristem SCR (yellow) is expressed
in the QC, adjacent ground tissue initials and the endodermis, SHR
(blue) is expressed in the stele and is trafficked into the adjacent cell
layer, the endodermis, where it directs cell fate (arrows).
Current Opinion in Genetics & Development 2003, 13:551–557
expanded domain of WUS expression. Conversely, constitutive CLV3 expression leads to loss of meristem function and WUS expression. The CLV complex, therefore,
negatively regulates WUS. Furthermore, WUS is required
for CLV1 expression. The interactions between WUS and
CLV form a positive feedback loop to maintain a balanced
population of stem cells in the central zone [4,10].
Additional components of the CLV1 complex includes a
protein phosphatase (KAPP) and a Rho GTPase [11,12]
whereas the protein phophatase POLTERGEIST acts
downstream of CLV1 [13,14]. poltergeist mutants suppress
clv and also enhance wus, but this is dependent on CLV1
function. Thus, POLTERGEIST appears to function
downstream of CLV in both a WUS-dependent and
WUS-independent pathway. Mutations in SHEPHERD
result in expansion of the shoot meristem [15], like clv,
and SHEPHERD encodes a HSP90-like protein predicted to be required for correct folding of CLV proteins.
A second pathway required for maintenance of stem cell
fate in the shoot meristem involves KNOX and BELL
class genes both of which belong to a larger group of
TALE class homeodomain transcription factors. Class 1
KNOX genes are expressed in the shoot apical meristem
and downregulated in differentiating cells [16–18]. Mutations in the Arabidopsis KNOX gene SHOOT MERISTEMLESS (STM) result in loss of meristem function
[17,19,20]. One means by which STM maintains stem cell
function is via repression of differentiation program genes
ASYMMETRIC LEAVES1 (AS1) and ASYMMETRIC
LEAVES2 (AS2) [21,22]. A closely related KNOX gene
BREVIPEDICELLUS (BP) is able to promote meristem
function in the absence of STM [22–24] but this is
apparent only in the absence of either AS1 or AS2,
indicating that KNOX genes function redundantly to
maintain stem cell fate. STM and BP depend on a more
distantly related BELL class homoeobox gene, BELLRINGER (BLR) [25], also called PENNYWISE [26].
Alone, blr mutants have a defect in organ positioning
(phyllotaxy) indicative of respecification of peripheral
zone cell fate. However, blr enhances the meristem
defect in weak alleles of stm and in backgrounds where
BP acts in meristem function. Consistent with these
observations, BLR interacts directly with KNOX proteins
and the expression domain of BLR in the shoot meristem
overlaps with that of STM and BP.
Induction of ectopic shoot meristems
Misexpression of KNOX genes alone can induce ectopic
meristems, suggesting that this class of genes has the
potential to establish stem cell fate in differentiated cells.
Furthermore, an increasing number of genes are now
known to maintain cells in a differentiated state by
repression of KNOX genes. One such gene is AS1, which
encodes a myb domain transcription factor [21,27,28].
Undifferentiated outgrowths and ectopic meristems
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Plant stem cells Byrne, Kidner and Martienssen 553
Figure 3
(a)
(b)
Current Opinion in Genetics & Development
Reprogramming cell fate: ectopic shoot meristems on as1 mutant
leaves. (a) Changes in cell-division patterns mark initial sites of ectopic
meristem formation. (b) Later in development, ectopic shoot meristems
give rise to lateral organs.
appear on as1 mutant leaves (Figure 3). AS1 likely acts
together with AS2, a member of the LATERAL ORGAN
BOUNDARIES family predicted to be transcription factors [22,28–31]. BLADE ON PETIOLE (BOP) also
represses KNOX genes in lateral organs [32]. As with
as1, mutations in bop result in lobed leaves and ectopic
outgrowths appear on leaves, although in this case organized meristems are not observed. KNOX gene repressors
include members of the YABBY family of potential
transcription factors. The YABBY genes FILAMENTOUS
FLOWER and YABBY3 are required for correct patterning
of lateral organs [33]. However, filamentous flower yabby3
double mutants also generate shoots on cotyledons and
leaves [34]. Genetic interactions between as1 and bop, as
well as as1 and yabby mutants, point to multiple independent pathways for suppression of stem cell fate by regulation of KNOX gene expression [33,34].
WUS can also re-establish stem cell fate in differentiated organs. Overexpression of WUS can result in dedifferentiation and subsequent somatic embryogenesis
from unspecialized callus cells [35]. In other cases, particularly when WUS is induced post-embryonically, only
small outgrowths are formed from differentiated tissue
[36,37]. The different affects of ectopic WUS are possibly
a result of WUS expression levels, timing of misexpression, tissue-specific effects or a combination of these
parameters. Likewise, overexpression of STM in some
but not all instances results in ectopic meristems [35–38].
However, combined post-embryonic ectopic induction of
STM and WUS can promote ectopic expression of CLV
genes and production of ectopic meristems. This is consistent with genetic interactions whereby STM and WUS–
CLV pathways converge to establish and maintain the
shoot apical meristem.
Stem cells of the root
Like the shoot apical meristem, the root meristem has a
central group of slowly dividing cells: the quiescent
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center (QC) (Figure 1). The QC is established early in
embryogenesis and is derived not from the embryoproper but from the uppermost cell of the suspensor.
Clonal analysis has demonstrated that asymmetric division of QC cells generates daughter cells, which either
retain QC cell function or replace an adjacent cell [39].
Immediate derivatives of the QC are themselves stem
cells, or initials, each of which gives rise to specific tissue
types within the root (Figure 1). After damage by laser
ablation or radiation, stem cells of the root divide to
repopulate the meristem. In maize, cultured root stem
cells can regenerate the root [40]. Studies on root development in Arabidopsis, where patterns of cell division
are particularly clear, have revealed that stem cells of
the root meristem are maintained by positional information. When the QC is ablated, a new functional QC
develops from proximal cells [41]. The QC also signals
to adjacent initial cells to maintain meristem function
[42]. Furthermore, when an initial cell is ablated an
adjacent cell divides to produce a new initial. Specification of the new initial requires contact with adjacent
initials indicating that these cells also respond to positional information [41].
One signal important for initiation and maintenance of
the root meristem is auxin. Inhibitors of auxin transport
result in expression of QC-specific markers in cells above
the QC, indicating a role for auxin in longitudinal positioning of the QC [43]. Furthermore, the root is a sink for
auxin and a maxima of auxin exists in the cells below the
QC [43,44]. Additional evidence supporting the role of
auxin in establishing and patterning the root meristem
comes from analysis of mutants that disrupt auxin signaling. For example, AtPIN4, which encodes a putative auxin
efflux carrier, is necessary for root meristem patterning
[45]. The auxin response factor MONOPTEROS effects
apical–basal patterning of the embryo. MONOPTEROS is
required for initiation of the root meristem as monopteros
mutants fail to specify QC cells and do not form a root
[46]. Another gene, BODENLOS, encodes an auxin
response regulator. Dominant gain-of-function mutations
in BODENLOS result in loss of the root meristem in a
manner similar to that of monopteros mutants. BODENLOS may act via inhibition of MONOPTEROS as these
two proteins directly interact [47,48].
SCARECROW (SCR), a GRAS family transcription factor,
is required for maintenance of the root meristem [49]. In
the root, SCR is expressed in the QC, adjacent endodermis/cortex initials and in differentiated endodermis
(Figure 2). Loss of SCR function leads to disruption of
stem cell identity in the initials as well as the QC. The
cell division that typically differentiates endodermal and
cortical cells does not occur in scr mutants and derivatives
of this initial assume a mixed fate of the two cell types.
This defect is restored by cell-autonomous expression of
SCR in the initial cells [50]. However, stem cell activity
Current Opinion in Genetics & Development 2003, 13:551–557
554 Differentiation and gene regulation
requires SCR expression in the QC, which is sufficient for
QC cell identity and root growth. SCR, therefore, acts cell
autonomously to maintain identity of initials and the QC,
whereas non-cell autonomous signaling from the QC
maintains adjacent stem cell divisions. SCR is also
expressed in the L1 layer of the shoot meristem, but
scr has no shoot meristem defects, although patterning in
mature shoot tissues is disrupted [51].
It is possible that gating of protein movement between
cells establishes a niche for maintaining stem cell function. In addition to proteins, RNA movement is well
documented in plant cells. Viral RNA and RNA encoding
regulatory genes such as KNOX genes are transported
systemically [58–61]. The role of RNA in maintaining
stem cells is discussed below.
Epigenetic control of stem cell fate
A related GRAS gene, SHORTROOT (SHR), is also
required for patterning the root meristem [52]. shr
mutants have irregular QC anatomy, loss of QC-specific
markers and their roots cease growing. SHR is expressed
in the stele (Figure 2) and the protein traffics to adjacent
cell layers, including the QC [53]. In the endodermis/
cortex initial, SHR activates SCR, which promotes the
asymmetric division characteristic of this cell type
[52,53]. Both SCR and SHR are required for QC function as the QC defect in shr is not rescued by SCR expression in the QC [50]. Another potential component is
SCHIZORIZA. In schizorizia mutants, additional internal
cell layers are formed and internal tissue is mis-specified
as epidermis. Double mutant analysis suggests that at
least one function of SCHIZORIZA is suppression of SCR
in the cortex/endodermis initial [54].
Genetic pathways required for shoot and root meristem
function in general do not overlap, but the same classes of
genes are likely to operate in each system. For example,
in petunia HAIRY MERISTEM, a GRAS family gene
related to SCR and SHR, acts non-cell autonomously to
maintain stem cell fate in the shoot apical meristem [55].
Furthermore, the temperature-sensitive topless mutant
converts shoots into roots [56]. This effect can be
induced relatively late in embryogenesis implying loss
of the shoot meristem program as well as gain of a root
meristem program. The similar organization between
shoot and root structures may represent a readily adopted
solution to the problem of maintaining a balance between
undifferentiated stem cells and differentiating derivatives in a growing tip.
Genetic evidence suggests that stem cells in plants, as in
animals, have a specialized chromatin structure. This may
reflect their capacity for a variety of gene-expression
programs, as well as their ability to divide repeatedly
without either differentiation or senescence. Components of the chromatin assembly factor complex are
encoded by the FASCIATA genes FAS1 and FAS2, which
restrict WUS and SCR activity [62]. The SWI2/SNF2
chromatin remodeling gene PICKLE represses embryonic genes in germinating seedlings [63,64]. Furthermore
pickle interacts synergistically with as1 indicating a role for
chromatin remodeling in stem cell fate [27]. Orthologs of
AS1 in other plants include PHANTASTICA from Antirrhinum and ROUGH SHEATH 2 from maize [65,66].
These genes share a SANT-class myb domain found in
the SWI3 family of proteins in yeast, which interact with
SWI2/SNF2 chromatin remodelers [67].
Autonomy and non-autonomy
ARGONAUTE1 (AGO1) and the closely related gene
PINHEAD/ZWILLE are also involved in Arabidopsis stem
cell fate. In ago1 and pinhead single mutants shoot meristem function is frequently lost, although penetrance is
variable [68–71]. Both genes are also required for organ
polarity, but loss of shoot meristem function is severe
and consistent in ago1 pinhead double mutants [68,70].
AGO1 expression is ubiquitous whereas expression of
PINHEAD is confined to the shoot meristem, the adaxial
(dorsal) side of lateral organs and shoot vasculature [70].
Ectopic expression of PINHEAD on the abaxial (ventral)
side of lateral organs results in additional cotyledons that
are occasionally fused as well as ectopic meristems along
the zone of fusion [72]. PINHEAD may be required for
specification of the plant apical–basal axis in that ectopic
expression establishes novel growth axes.
At least one common mechanistic theme in shoot and root
meristem patterning is the use of positional cues to
modulate cell fate. How plant cells specify positional
information is poorly understood but is likely to involve
movement of proteins via conduits, superficially resembling gap-junctions, known as plasmodesmata. Intercellular movement has been reported for several
transcription factors. For example, in the shoot movement
of KNOX genes from the L1 to inner layers of the
meristem partially rescues meristem defects of stm
[57]. Likewise in the root, movement of SHR from
internal stele cell layers to the adjacent cell layer is
required for activation of the downstream target SCR
and specification of endodermal and QC cell fate [53].
AGO1, along with homologs in animals and yeast, is
required for RNA interference (RNAi). One possible role
for RNAi is regulating microRNA interaction with target
genes, which frequently encode transcription factors in
plants [73]. miRNA targets include the CUC2 gene, which
is required redundantly with CUC1 for STM expression
[74]. These transcription factors are unique to plants,
however, and both plant and animal stem cells depend
on RNAi for persistence and propagation. That is, AGO/
PIWI homologs in Drosophila, Caenorhabditis elegans and
mouse are required to maintain stem cells in the germline
[75]. This may point to a more universal mechanism.
RNAi in the fission yeast Schizosaccharomyces pombe is
Current Opinion in Genetics & Development 2003, 13:551–557
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Plant stem cells Byrne, Kidner and Martienssen 555
involved in turnover of pericentromeric repeat transcripts
and this promotes chromosome disjunction at mitosis by
recruiting cohesin via histone lysine-9 methylation
[76,77]. Similar mechanisms in Drosophila [78] and
Arabidopsis (L Lippman et al., unpublished data) point
to a conserved role for RNAi in chromosome segregation.
Such a role could influence symmetric and asymmetric
cell divisions that underlie stem cell fate.
Conclusions
Stem cells occupy a niche in both shoot and root meristems that is specified by cell–cell signaling. Maintenance of stem cell fate requires several homeodomain
transcription factors, components of the RNAi machinery
and chromatin remodeling factors that may promote
pluripotency and stem cell proliferation. Although most
of the components controlling these functions have
diverged in roots and shoots, ancestral pathways controlling stem cell function in early eukaryotes may be shared
with animal and fungal lineages.
Update
In a situation analogous to loss of root QC cells, ablation of
central zone cells in the shoot meristem leads to WUS
expression in peripheral zone cells and respecification as
central zone cells [79].
Acknowledgements
We apologize to those whose work was not cited for lack of space. We thank
members of the Martienssen laboratory for useful discussions. The
preparation of this manuscript was supported by USDA-NRI grant
2003-00967.
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Current Opinion in Genetics & Development 2003, 13:551–557