Plant Stem Cell Niches

Plant Stem Cell Niches
Ernst Aichinger,1,2 Noortje Kornet,1

Thomas Friedrich,1 and Thomas Laux1,2
1
BIOSS Centre for Biological Signalling Studies, Faculty of Biology, University of Freiburg,
Annu. Rev. Plant Biol. 2012.63:615-636. Downloaded from www.annualreviews.org
79104 Freiburg, Germany; email: laux@biologie.uni-freiburg.de

2
by Universidad Autonoma de Queretaro on 10/24/13. For personal use only.
Freiburg Institute of Advanced Studies (FRIAS), D-79104 Freiburg, Germany
Annu. Rev. Plant Biol. 2012. 63:615–36 Keywords

First published online as a Review in Advance on cambium, organizing center, quiescent center, boundary formation,
February 9, 2012
signaling
The Annual Review of Plant Biology is online at
plant.annualreviews.org Abstract
This article’s doi:
Multicellular organisms possess pluripotent stem cells to form new or-
10.1146/annurev-arplant-042811-105555
gans, replenish the daily loss of cells, or regenerate organs after in-
Copyright c 2012 by Annual Reviews.
jury. Stem cells are maintained in specific environments, the stem cell
All rights reserved
niches, that provide signals to block differentiation. In plants, stem cell
1543-5008/12/0602-0615$20.00
niches are situated in the shoot, root, and vascular meristems—self-
perpetuating units of organ formation. Plants’ lifelong activity—which,
as in the case of trees, can extend over more than a thousand years—
requires that a robust regulatory network keep the balance between
pluripotent stem cells and differentiating descendants. In this review,
we focus on current models in plant stem cell research elaborated during
the past two decades, mainly in the model plant Arabidopsis thaliana. We
address the roles of mobile signals on transcriptional modules involved
in balancing cell fates. In addition, we discuss shared features of and
differences between the distinct stem cell niches of Arabidopsis.
615
year offer one of the most impressive examples
Contents of plant developmental capacity. The origin of
each new organ lies on the tip at each side of
INTRODUCTION . . . . . . . . . . . . . . . . . . 616
the plant body—the shoot apical meristem and
STRUCTURE AND FUNCTION
the root apical meristem. In addition, there are
OF THE SHOOT APICAL
two meristems involved in the thickening of the
MERISTEM . . . . . . . . . . . . . . . . . . . . . . 617
stem, which are most prominent in trees: the
Regulation of the Cytokinin/
ring-shaped cambium of the vasculature, which
Gibberellic Acid Balance by
provides transport and support, and the phel-
KNOX Genes . . . . . . . . . . . . . . . . . . . 617
logen/cork cambium, which replenishes the
Local Control of Stem Cells by
outer layer (bark) that is regularly shed. In all
WUS . . . . . . . . . . . . . . . . . . . . . . . . . . 619
cases, meristems have two functions: to produce
ZLL/AGO1 Balance Determines
new cells and to initiate organ formation.
Stem Cell Inhibitory MicroRNA
How new cells are produced has been

Levels . . . . . . . . . . . . . . . . . . . . . . . . . . 619
demonstrated by elegant cell-tracking experi-
Control of the Stem Cell Number . . 620

ments in the shoot meristem. In 1940, Satina
What Keeps the Stem Cell Niche at
and coworkers (113) induced polyploidy in sin-
the Tip of the Shoot? . . . . . . . . . . . 622
gle cells of Datura through colchicine treatment
THE ROOT STEM CELL NICHE . . 622
and found that the shoot meristem consists
The Quiescent Center Functions as
of clonally separate layers of cells: an outer
Organizer of the Root Stem Cell
L1 layer from which the epidermis is derived,
Niche . . . . . . . . . . . . . . . . . . . . . . . . . . 624
a subepidermal L2 layer, and an internal L3
WOX5 Expression in the Quiescent
layer. This three-layer organization is typical
Center Is Required to Maintain
of the shoot meristems of dicotyledonous seed
Stem Cells . . . . . . . . . . . . . . . . . . . . . . 624
plants, but varies in monocotyledons (two lay-
The Stele-Borne SHR Signal Is
ers), gymnosperms (one layer), and more basal
Required for Quiescent Center
species (mosses, ferns) where all cells originate
Function . . . . . . . . . . . . . . . . . . . . . . . 625
from a single apical cell. Thirty years later,
Long-Range Control of the Stem
Stewart & Dermen (125) provided elegant
Cell Niche via Auxin and PLT
evidence that the cells in approximately one-
Genes . . . . . . . . . . . . . . . . . . . . . . . . . . 625
third of the shoot circumference originated
Quiescence of the Quiescent
from a single stem cell in the shoot meristem,
Center . . . . . . . . . . . . . . . . . . . . . . . . . 626
indicating the presence of three stem cells in
THE VASCULAR STEM CELL
this layer. Because each clone derived from a
NICHE . . . . . . . . . . . . . . . . . . . . . . . . . . . 626
single cell comprised all cell types in this layer,
Stem Cell Maintenance in the
the shoot meristem stem cells can be viewed
Procambium . . . . . . . . . . . . . . . . . . . . 627
as pluripotent. Importantly, marked sectors
More Boundaries Within the
occasionally broadened from one-third to two-
Vascular Stem Cell Niche . . . . . . . 628
thirds and even to the entire circumference at
Coordination of Longitudinal and
the expense of the progeny of nonmarked stem
Lateral Growth . . . . . . . . . . . . . . . . . 629
cells and vice versa, indicating that stem cells
MOLECULAR SIGNATURE OF
can be replaced and act as stem cells only as
PLANT STEM CELLS . . . . . . . . . . . 629
long as they are in a specialized environment.
Finally, when an L1 stem cell was displaced
into the subepidermal layer by an occasional
INTRODUCTION periclinal division, it gave rise to L2 cell types,
Plants that are several hundred years old and suggesting that the fate of its progeny is not
yet generate whole new organs year after determined by the stem cell’s history but rather
616 Aichinger et al.

by the position of the differentiating offspring. been identified during the past two decades
In 1965, Newman (98) had already described by genetic studies, mainly in the model plant
shoot meristem stem cells as “temporary occu- Arabidopsis thaliana. For aspects not addressed
pants of a permanent office”—a good metaphor here, we refer readers to several excellent re-
for what we call stem cell niches today. views covering the initiation of meristems in the
How can plant stem cells exist for hun- embryo (9, 15, 72) and organ formation (18, 79).
dreds of years without accumulating mutations?
That stem cells divide relatively infrequently
has been recognized by histological studies and STRUCTURE AND FUNCTION OF
has been associated with the advantage of re- THE SHOOT APICAL MERISTEM
ducing the mutational load of DNA replica- The Arabidopsis shoot meristem is organized
tion (84). Immediate daughter cells of the stem into a central zone (CZ) of slowly dividing
cells might perform a finite number of division cells that contains the stem cells, a surrounding
rounds before they are replaced, thus increas- peripheral zone (PZ) of more rapidly dividing
ing the stem cell output as transit amplifying
cells from which lateral organs are derived,

cells (125). Fulcher & Sablowski (41) observed and an underlying rib zone where cells assume
that shoot and root meristem cells in Arabidopsis a flattened shape as the first indication of
are hypersensitive to DNA double strand breaks differentiation toward central stem tissue
and respond with cell death to DNA damage, (Figure 1a). Shoot meristem stem cells func-
allowing a quick clearing of compromised DNA tion in a population mode—that is, individual
from the stem cell system. divisions are not strictly asymmetric, generat-
On the basis of these studies, together with ing one new stem cell and one differentiating
studies in animals that rely largely on test- cell (73, 123). Rather, whether any given
ing stem cell potential in transplantation as- cell becomes a new stem cell or undergoes
says (114), a general stem cell niche concept differentiation depends on its position. Genetic
for multicellular organisms is apparent: (a) Cells studies of the past decade provided substantial
that are protected from differentiation by sig- insight into two questions: How is stem cell
nals from neighboring cells in specific niches identity determined? And how are boundaries
can divide and thus function as stem cells, and maintained in the dividing cellular context of
(b) the cells that leave a niche are bound to dif- the shoot meristem?
ferentiate. Differentiation of the daughter cells
leaving a niche appears to be dictated by the en-
vironment rather than by cell origin (128). In Regulation of the Cytokinin/
vitro, however, the potential of stem cells can Gibberellic Acid Balance
be expanded experimentally (101). by KNOX Genes
The excitement that the progress in animal The first plant stem cell regulator gene was
stem cell research has caused is mainly due to isolated from the maize leaf mutant knotted
its potential in regenerative medicine. Is there (kn) (50). KN encodes a homeodomain protein
a similar potential for plant stem cells in agri- that in the dominant active kn-1 mutant is
culture and breeding? Indeed, despite multiple ectopically expressed in leaf veins, resulting
examples of nonsexual propagation, regenera- in proliferating “knots.” KN is the founding
tion in many crop species has remained elusive member of the KNOTTED1-like homeobox
and inefficient. Triggering an excess of stem (KNOX) genes. Its normal expression is in
cells can overcome this problem, as exemplified undifferentiated cells of the shoot meristem
by the enhanced induction of somatic embryos dome, but notably, it is absent from the cells in
in Arabidopsis stem-cell-surplus mutants (94). leaf anlagen, consistent with a model in which
This review discusses current models and open KN promotes the undifferentiated cell state in
questions in plant stem cell research that have the shoot meristem (120).
www.annualreviews.org • Plant Stem Cell Niches 617

a CZ b
PZ
SC
LP
Auxin
OC LP
AS1
CK
RZ STM/
KNOX GA KNOX
CK AS1
c Expression of d
LOG key shoot apical
CK meristem regulators
? CKRp
HD-ZIPIII
CLV3 IPT7 AGO1
miR165/166
STM
CLV1 CK
AS1 GA CLV3
ARR7/15 ZLL
WUS/AHK4
WUS
Auxin CLV1
Figure 1
Organization and regulation of the shoot apical meristem. (a) Schematic representation of the structure of
the shoot meristem. Abbreviations: CZ, central zone; LP, leaf primordium; OC, organizing center; PZ,
peripheral zone; RZ, rib zone; SC, stem cells. (b) Regulation of organ boundaries. AS1 and auxin repress the
meristem-promoting activities of KNOX genes and cytokinin (CK) in the leaf primordium, whereas STM and
related KNOX genes repress AS1 in the meristem, activate CK biosynthesis, and repress gibberellic acid (GA)
biosynthesis. (c) A pool of pluripotent stem cells (blue) is maintained by a WUS/CLV3 negative-feedback
loop. STM activates IPT7, which catalyzes cytokinin biosynthesis. As has been shown in rice, L1-expressed
LOG might convert cytokinin riboside 5′ -monophosphates (CKRps) into active cytokinin. Higher
sensitivity to CK in the OC is achieved by localized expression of AHK4 and repression of ARR7/15. (d ) ZLL
is expressed in the vasculature underlying the shoot meristem, where it sequesters miR165/166 to prevent
downregulation of meristematic HD-ZIPIII genes in the shoot meristem primordium.
The Arabidopsis ortholog SHOOTMERIS- and exogenous application of cytokinins or

TEMLESS (STM) displays an expression expression of a cytokinin biosynthetic enzyme
pattern similar to that of KN (83). Seedlings from the STM promoter can rescue the stm
carrying the strong stm-1 mutation lack a shoot mutant phenotype. Conversely, overexpression
meristem and display fused cotyledons; stm-1 of STM induces cytokinin biosynthesis and the
mutants are also unable to initiate meristems formation of ectopic meristems (17, 58, 142).
postembryonically. Careful comparison of mu- Therefore, activation of cytokinin synthesis
tant defects and expression dynamics suggested by STM is crucial for meristem maintenance
two STM functions: to prevent differentiation (Figure 1b,c). Overexpression of the related
in the meristem dome and to repress cell KNOX gene KNAT1/BREVIPEDICELLUS
division between lateral organs, allowing their (BP) also results in higher cytokinin levels,
separation (35, 82, 83). STM directly activates raising the possibility that other KNOX genes
transcription of the cytokinin biosynthetic act similarly to STM (40, 58). STM also pre-
enzyme gene IPT7 in the shoot meristem, vents expression in the shoot meristem of the

ASYMMETRIC LEAVES1 (AS1) gene, which the OC variably overlaps with stem cells in the
represses the meristem-promoting factors third outermost cell layer. In addition to main-
KNAT1/BP and KNAT2 in lateral organ pri- taining the undifferentiated nature of the stem
mordia (20). Interestingly, the shoot meristem cells, WUS is required for expression of the
is recovered in as1 stm-1 double mutants, CLAVATA3 (CLV3; see below) gene in the stem
showing that meristem cells can be maintained cell region of shoot and floral meristems (17, 76,
without STM activity. It is plausible that, in 115). Because all three layers of stem cells are
this situation, KNAT genes can replace STM affected by WUS expression in the OC, a stem-
function. cell-promoting signal from the OC has been
STM (and related KNOX genes in other postulated (91). Yadav and colleagues (140)
species) furthermore downregulates gibberellic demonstrated that the WUS protein moves
acid (GA) levels in the shoot meristem through from the OC into the CZ, where it binds di-
direct repression of the GA-biosynthesis gene rectly to the CLV3 promoter, providing another
GA 20-oxidase and upregulation of the GA- example of moving plant transcription factors
degrading gene GA 2-oxidase (23, 58, 111). in cell-cell communication (97, 120). This in-
GAs promote differentiation and thus can be tercellular movement appears to be critical for
viewed as antagonists of meristem identity. GA stem cell maintenance, as decreasing WUS mo-
2-oxidase is expressed at the base of organ pri- bility results in loss of the shoot meristem.
mordia. One attractive model is that GA move- In OC cells, WUS directly downregulates
ment from the leaves into the shoot meristem the transcription of the type A ARABIDOPSIS
is thereby excluded (reviewed in 119). RESPONSE REGULATOR genes ARR7 and
ARR15 (Figure 1c), which encode inhibitors
of intracellular cytokinin signal transduction
Local Control of Stem Cells by WUS (75). Overexpression of a constitutively active
Seedlings of the wuschel (wus) mutant lack a form of ARR7 caused shoot meristem defects
shoot meristem and display partially differenti- similar to those in wus mutants, suggesting
ated cells at the position of the stem cells, sug- that promoting cytokinin signal transduction
gesting that WUS is required to prevent dif- in OC cells is an important part of how WUS
ferentiation of stem cells (74, 91). In contrast acts in stem cell maintenance. Chromatin
to stm mutants, wus mutants can initiate ad- immunoprecipitation experiments combined
ventitious shoot meristems postembryonically, with transcriptional profiling revealed that
although these terminate after the generation WUS acts on a larger set of genes involved in
of a few organs. Conversely, overexpression of meristem regulation, hormone pathways, and
WUS leads to enlarged meristems, suggesting cell division control (19). Notably, this study
that WUS is also sufficient to promote stem cell points to additional roles of WUS in regulating
identity (17, 76, 115, 141). Notably, this ability two phytohormones: jasmonate ( JA) through
appears to be limited to immature tissues, im- repression of the JA response factor JAZ5, and
plying that other factors are also required. WUS auxin (see below) through modulation of auxin
encodes a plant-specific homeodomain protein transport and response genes. In summary, the
and is the founding member of the WUSCHEL- OC-derived WUS protein must be present in
RELATED HOMEOBOX (WOX) gene family, both the OC and the stem cells to maintain the
which regulates diverse aspects of development stem cells in an undifferentiated state.
(130). WUS expression in the shoot meristem
defines the organizing center (OC), which in
seedlings is located in the fourth- and fifth- ZLL/AGO1 Balance Determines Stem
outermost cell layers, underneath the three Cell Inhibitory MicroRNA Levels
stem cell layers (Figure 1a,c); in the inflores- The ZWILLE/PINHEAD/AGO10 (ZLL) gene
cence meristem and floral meristem, however, has been identified in mutant screens for

meristem regulators and encodes an ARG- mRNA as efficiently as AGO1, suggesting that
ONAUTE (AGO) protein, implying a function ZLL sequesters miR165/166 away from the cat-
in RNA silencing. Mutant zll seedlings display alytically more active AGO1, and consequently
a range of phenotypes, from flat apices of differ- HD-ZIPIII expression is increased (151).
entiated cells to a terminal organ in place of the HD-ZIPIII activity also promotes adaxial leaf
shoot meristem (92, 95). However, WUS is still fate, which had previously been shown to
expressed in the OC of zll embryos, whereas positively affect shoot meristem maintenance
CLV3 expression is initiated in the presumptive (132), whereas abaxial identity genes, such
stem cells but is not maintained. In addition, as KANADI, antagonize it (reviewed in 9).
accumulation of stem cells by overexpression However, it has not yet been distinguished how
of WUS is suppressed in zll mutants (127). HD-ZIPIII expression in the shoot meristem
These findings suggest that ZLL is required to and in the leaf differ in their effects on shoot
potentiate WUS-dependent stem cell signal- meristem development.
ing. ZLL expression in the underlying vascular

primordium is sufficient for shoot meristem
development, indicating that the vasculature Control of the Stem Cell Number
plays a role in controlling the shoot meristem. Although all shoot meristem cells divide, the
The primary cause for the loss of the shoot shoot meristem keeps its shape and size (with
meristem in zll seedlings appears to be the ac- seasonal changes occurring) and its internal or-
cumulation of microRNA165/166 (miR165/166) ganization. How are boundaries in the shoot
and the consequent downregulation of their meristem controlled? Mutants with an ex-
target HOMEODOMAIN-LEUCINE ZIPPER panded stem cell pool have been the start-
III (HD-ZIPIII) messenger RNAs (mRNAs) ing point for some answers. Analysis of clavata
in the shoot meristem (Figure 1d ) (80). HD- (clv) mutants, which display gradually enlarg-
ZIPIII genes encode homeodomain proteins ing shoot meristems and floral meristems that
that act as key meristem regulators, among produce more organs than those of wild-type
other functions (9, 105). Multiple mutants plants (26, 27), led to the identification of a
of HD-ZIPIII genes such as PHABULOSA signal cascade central to stem cell regulation.
(PHB), PHAVOLUTA (PHV), and REVO- CLV3 (39) belongs to a family of 32
LUTA (REV ) or overexpression of miR166 small proteins called CLV3/EMBRYO SUR-
lead to shoot meristem termination (34, 136), ROUNDING REGION (CLE), which are
whereas upregulation of HD-ZIPIII genes posttranslationally processed into the active
leads to enlarged or ectopic meristems (93). signal peptides CLEp (29, 57). The expanded
How HD-ZIPIII proteins promote stem cell meristem of clv3 mutants is caused by an
maintenance is unclear. enlargement of the WUS expression domain
A puzzling question is how ZLL protein in (115). Conversely, overexpression of CLV3 re-
the vasculature can prevent miR165/166 accu- sulted in repression of WUS transcription and
mulation in the shoot meristem primordium. a phenocopy of the wus mutant (16, 77). CLV3
Surprisingly, molecular and genetic data is expressed in a wedge-shaped domain that
indicate that ZLL and its close homolog AGO1 roughly coincides with the position of the stem
have not only overlapping but also antagonistic cells. Notably, the number of cells in the L3
effects on gene silencing and development layer that express CLV3 appears smaller than
(88). One proposed model is that ZLL might the number of cells in the L1 layer, indicating
sequester miR165/166 and thus block its that CLV3 expression is not strictly linked to
accumulation in the shoot meristem (18, 24). stem cells, if there are the same number of
Biochemical evidence demonstrated that ZLL stem cells in each layer. CLV3 transcript levels
binds miR165/166 more efficiently than AGO1 are positively regulated by WUS, as CLV3
but does not seem to degrade HD-ZIPIII expression is lost in wus mutants and expanded

in WUS overexpressors (17, 115). This estab- overexpression in the L1 layer can completely
lishes a negative-feedback loop in which WUS repress WUS expression in the OC, causing
expression in the OC is required for CLV3 ex- a wus phenocopy (77). How is this prevented
pression in the stem cells, which in turn delimits under normal conditions? An active CLV3–
the WUS expression domain (Figure 1c). This green fluorescent protein (GFP) fusion protein
feedback loop provides a conceptual frame- spread away from the stem cells predominantly
work for how the size of the stem cell pool is in the lateral direction rather than into the
dynamically assessed and kept stable. Notably, underlying OC. Both effects were blocked by
however, the meristem appears able to tolerate the presence of a functional CLV1 receptor,
significant alterations of CLV3 levels without indicating that the CLV3-GFP fusion protein
phenotypic consequences, and initial down- remained uncleaved and that the observed
regulation of WUS expression can be reversed spread was not due to clipped off GFP. These
at later time points, suggesting additional reg- data suggest that binding of CLV3p to its re-
ulatory mechanisms that buffer stem cell main- ceptors in the overlying cells contributes to OC
tenance against incidental fluctuations (96). stability (77). However, recent findings are at
CLV3p is perceived by a multitude of recep- odds with such a mechanism: CLV3-dependent

tor complexes (reviewed in 61). CLV1 encodes internalization of a functional CLV1-2xGFP as
a leucine-rich repeat (LRR) receptor kinase a proxy for CLV3p binding was also detected
expressed in a central domain of the shoot in deeper cell layers of the shoot meristem,
meristem, including the OC and L3 layer of the irrespective of CLV1 levels, suggesting that
stem cells (25). CLV2 also codes for an LRR- ligand sequestering is not important (100).
receptor-like transmembrane protein that lacks Curiously, most of the CLV1 receptors appear
an intracellular kinase domain. CLV2 interacts already internalized in wild-type plants, sug-
with CORYNE (CRN)/SUPPRESSOR OF gesting a largely saturated response to CLV3,
LLP1 2 (SOL2) (which shares similarity which raises the question of how increased
with serine/threonine kinases but lacks an CLV3 levels can terminate the meristem and
extracellular LRR domain) to form a CLV3- WUS expression as previously shown (16, 77).
receptor complex independently of CLV1 (48). Notably, WUS was found to directly repress
Nimchuk et al. (99) recently provided evidence CLV1 expression, and thus might reduce the
that CRN is unable to autophosphorylate effect of CLV3p in the OC cells, thereby
and can mediate its function without a func- sustaining its own expression (19). Therefore,
tional kinase domain; the authors speculated a decrease in sensitivity to CLV3p in OC cells
that CRN could have scaffolding functions may also contribute to stability of the OC.
analogous to those of animal pseudokinases. Several decades ago, mechanical destruc-
Finally, a third important player in CLV3p tion of the meristem center in Impatiens roylei
perception is the recently identified receptor caused induction of new meristems from the
RECEPTOR-LIKE PROTEIN KINASE PZ, suggesting that this developmental option
2 (RPK2)/TOADSTOOL2 (TOAD2) (64). is normally repressed in the PZ by lateral
The clv1 clv2 rpk2 triple mutant phenocopies inhibition (81). By elegant laser ablation exper-
the clv3 mutant, suggesting that these three iments in tomato apices, Reinhardt et al. (108)
receptors constitute the three main pathways demonstrated that only ablation of the entire
of CLV3p perception in the shoot meristem. CZ, and not merely of the stem cell layers,
Where in the shoot meristem does CLV3 causes rapid activation of WUS in adjacent
activity repress WUS? In clv3 mutants, WUS PZ cells. Together, these results suggest that
expression is both shifted one layer up and the OC promotes stem cell fate in its apical
expanded laterally, suggesting that CLV3 neighbors but represses it in PZ cells, which
normally represses WUS at the distal and in turn implies the requirement of additional
lateral boundaries of the OC. Notably, CLV3 factors that modify cell responsiveness. In

Arabidopsis, Reddy & Meyerowitz (107) also to the underlying cells. Expression of the gene
reported lateral inhibition when manipulating encoding the cytokinin receptor ARABIDOP-
the stem cells. Using an inducible downregu- SIS HISTIDINE KINASE 4 (AHK4) overlaps
lation of CLV3 expression in the CZ by RNA with the OC and is required for induction of
interference (RNAi), they observed that cells WUS expression by cytokinin (44). Together
close to the CZ reverted back to stem cell with the finding that WUS promotes intracel-
fate (which potentially could be mediated by lular cytokinin signals (75), this suggests that
derepressed WUS expression), whereas cells OC cells are dedicated within the shoot meris-
more distant from the CZ displayed increased tem to perceiving and transducing cytokinin
cell division, separating independent functions signaling, and thus reinforce WUS expression.
of CLV3. In a different set of experiments by By contrast, in the stem cells, the cytokinin
Yadav et al. (141), downregulation of WUS in signaling inhibitors ARR7 and ARR15 are
the OC resulted in enlargement and a gradual required for high levels of CLV3 expression
shift of the auxin maxima marking lateral organ (149).

anlagen toward the CZ, implying that WUS Along the same lines, Yoshida et al. (144) as-
also has a non-cell-autonomous function in sociated downregulation of cytokinin response

controlling auxin responsiveness in the PZ. with strongly increased CLV3 expression in the
In summary, control of WUS gene ex- tomato shoot meristem. The surprising aspect
pression and multiple levels of lateral inhi- of this work is that light is required for nor-
bition contribute to robustly maintaining the mal cytokinin response in the shoot apex. Im-
boundaries between pluripotent stem cells and portantly, this requirement is independent of
differentiating descendants. photosynthesis and therefore suggests that light
acts as a signal to increase cytokinin response,
which in turn keeps the CLV signal pathway in
What Keeps the Stem Cell Niche check and thus promotes proliferation. At the
at the Tip of the Shoot? same time, light is also required for the forma-
If cells above the OC undergo periclinal tion of auxin maxima, involving PINFORMED
divisions, why is the OC not gradually dis- 1 (PIN1) localization. Notably, in this study,
placed away from the apex? Schoof et al. (115) light was able to trigger lateral primordia initi-
proposed that in addition to the repressive ation in the absence of leaves. Intuitively, one
CLV3 signal, stem cells also emanate a graded might not assume that the shoot apex is a place
signal that promotes WUS expression and thus for light perception, because in many cases it is
anchors the stem cell niche to the tip of the covered by developing leaves. Thus, either sen-
plant. Several recent observations are consis- sitive photoreceptors might enable the shoot
tent with a model in which cytokinin might be meristem to perceive light in a natural situa-
involved in this process. As said above, STM tion as well, or the leaves might take over this
promotes cytokinin synthesis throughout the function when the apex is covered.
meristem with the exception of incipient organ
primordia. In rice, the LONELY GUY (LOG)
gene, which encodes the enzyme catalyzing THE ROOT STEM CELL NICHE
the final step of cytokinin biosynthesis, is Longitudinal root growth originates at the tips
specifically expressed in the L1 layer, including of the roots where the root stem cells reside. In
the stem cell domain (69). Functional evidence the center of the root tip is the quiescent center
in Arabidopsis is still missing, but Yadav et al. (QC), which is mitotically relatively inactive in
(139) reported expression of LOG homologs Arabidopsis. The stem cells directly surround the
in the shoot meristem. It is thus tempting to QC and give rise to the different cell files of the
speculate that by producing active cytokinin, root, the stele, the ground tissue (consisting of
the L1 layer provides apical-basal information endodermis and cortex), the epidermis, and the

a b
SHR
SCR
SCR
SC R
R SC
WOX5
ACR4 ACR4
Quiescent center ACR4
Columella
ACR4 CLE40
Lateral root cap
Epidermis
CLE40
Cortex
Endodermis
Stele
CLE40
TPST RGF1/2/3 RGF PLT

expression expression protein protein
Figure 2
The root stem cell niche. (a) Schematic organization of the root stem cell niche. Intense colors represent the
stem cells of the corresponding cell file; intense green marks the cortex and endodermis stem cells, and
intense red marks the stem cells for the epidermis and lateral root cap. (b) Model for SHR/SCR and
CLE40/ACR4 action. SHR expressed in the stele moves to the surrounding endodermis and quiescent
center. There, SCR is required for nuclear localization of SHR, and SHR activates SCR expression. CLE40
is expressed in differentiated columella cells and acts via its putative receptor, ACR4, which is expressed in
columella stem cells and the first layer of differentiated columella cells. CLE40/ACR4 might function to
repress WOX5 expression in an indirect manner. (c) Schematic expression pattern of TPST and RGF1/2/3
according to in situ hybridization experiments, and protein abundance of RGF and PLT. The expression
maxima of TPST and RGF1/2/3 overlap with the PLT maxima and might help in creating the graded pattern
of PLT protein activity.
lateral root cap, as well as the columella (Figure the distal side of the QC are the columella stem
2a). Each stem cell division is asymmetric, cells (CSCs), whose daughter cells differentiate
generating one daughter cell that stays in without additional rounds of cell divisions into
contact with the QC and persists as a stem cell, starch-containing, gravity-sensing columella
and another cell that is located one cell away cells. Thus, the Arabidopsis root stem cells
from the QC, can undergo several rounds of operate in a lineage-based mechanism similar
cell divisions, and eventually differentiates. At to most animal stem cell niches and unlike

the shoot meristem (73). Notably, each stem state when the QC was ablated, indicating that
cell in the root meristem gives rise to only the stem-cell-promoting signals from the QC
one tissue, raising the question of whether the can work over several cell diameters but nor-
stem cell potential is limited. Elegant ablation mally are counteracted in cells without direct
studies have shown, however, that the daughter contact to the QC. Although the QC-borne
cells differentiate according to signals from signal molecules are still undiscovered, genetic
older differentiated cells and have the ability and molecular studies have identified pathways
to switch fates if displaced to a new position that are essential for stem cell maintenance in
(128). the Arabidopsis root.
The simple structure of the Arabidopsis root
makes it an ideal model for developmental stud-
ies, but compared with other species this is more WOX5 Expression in the Quiescent
an exception than the rule. For example, the QC Center Is Required to Maintain
Stem Cells
in maize root consists of up to 1,000 cells and

shows a gradient of quiescence with increasing The WUS homolog WOX5 is specifically ex-
mitotic activity toward the proximal meristem pressed in the QC, and loss of WOX5 function
(28, 37). Although species with similarly large leads to differentiation of the CSCs, similar
root meristems have been used for initial histo- to what was observed upon QC ablation (49,
logical studies, the stereotypic and simple orga- 112). Furthermore, overexpression of WOX5
nization of Arabidopsis roots has aided its use as a in the columella blocks differentiation and
model for stem cell research in plants. Here, we generates stem-cell-like cells. In contrast to
discuss how QC cells and stem cells are spec- the excessive undifferentiated cells caused by
ified and how the specific pattern of the root RBR downregulation, QC ablation does not
stem cell niche is regulated. suppress the effects of WOX5 overexpression,
consistent with the hypothesis that no QC
signal other than the one(s) generated by
The Quiescent Center Functions WOX5 is required for stem cell maintenance.
as Organizer of the Root Stem In addition to its effect on CSCs, WOX5 is also
Cell Niche required for maintaining proximal stem cells,
Direct evidence that the QC plays a role in but here WOX5 acts redundantly with the
controlling stem cells came from laser ablation SHORTROOT (SHR)/SCARECROW (SCR)
of individual Arabidopsis QC cells (129). CSCs and PLETHORA (PLT ) pathways (112).
abutting the ablated QC cells ceased prolifer- Several CLE peptides can cause differen-
ation and differentiated into starch-containing tiation of stem cells and/or reduce the size of
columella cells, whereas abutting cortex and en- the root meristem (16, 22, 54, 57, 124). The
dodermis initials (CEIs) differentiated into CEI CLE40 gene is expressed in the differentiated
daughter cells. The fact that only cells in direct columella cells and promotes differentiation
contact with the QC are maintained as stem via the receptor-like kinase ARABIDOPSIS
cells might suggest short-range or contact- CRINKLY 4 (ACR4) (124). Both acr4 and
based signaling. That this is not the case was cle40 loss-of-function mutants display an
shown in an elegant experiment by Wildwater additional layer of distal stem cells and a lateral
et al. (135) in which differentiation of stem expansion of WOX5 expression (31, 124).
cell daughters was blocked by RNAi-mediated Thus, the CLE40/ACR4 module provides a
downregulation of RETINOBLASTOMA- signal that counteracts stem-cell-promoting
RELATED (RBR) activity, resulting in several QC signals and allows distant columella cells
layers of undifferentiated cells next to the QC. to differentiate (Figure 2b). As the expression
These extra cells lost their undifferentiated pattern of the putative CLE40p receptor ACR4

does not overlap with the WOX5 expression reminiscent of animal morphogens. The high-
domain, the effect on WOX5 expression might est PLT levels are in the QC, and seem to be re-
be indirect, e.g., owing to misspecified CSCs. quired for specifying and maintaining the stem
cell niche; intermediate PLT levels in the prox-
imal meristem are required for mitotic activity;
The Stele-Borne SHR Signal and low levels correlate with differentiation
Is Required for Quiescent (Figure 2c). Because the response of PLT
Center Function expression to auxin occurs later than for
The GRAS (GAI, RGA, SCR) transcription other known auxin response genes, it has
factor SHR is expressed in the stele and moves been postulated to be rather indirect (3).
to the surrounding cells, including the QC, Tyrosylprotein sulfotransferase (TPST) and
where it activates expression of the related SCR the ROOT GROWTH FACTOR (RGF)
gene (Figure 2b) (51, 97). SCR itself is re- tyrosine-sulfated peptides might link auxin
quired for the nuclear localization of SHR, and to PLT protein levels (90, 150). The current
mutations in either SCR or SHR result in irreg- model holds that auxin induces the expression
ular morphology of the stem cell niche, lack of of TPST and several RGF genes. TPST in turn
QC-specific marker expression, and ultimately sulfates the RGF peptides, which by an un-
the collapse of the root meristem (30, 78, 110). known mechanism induce transcriptional and
QC-specific expression of SCR in the shr mu- posttranscriptional upregulation of the PLT
tant background cannot rescue the QC defects protein levels (Figure 2c). The direct targets
of shr, suggesting that both proteins must be of PLT proteins are still unknown. Notably,
present in the QC to maintain stem cell activity PLT activity enhances PIN expression, which
(110). might create a positive-feedback loop that
stabilizes the auxin maximum at the root tip
(14).
Long-Range Control of the Stem Cell As in many other examples, the readout of
Niche via Auxin and PLT Genes auxin in the root stem cell system depends on
The root stem cell niche is marked by an auxin the cellular context. Unlike in the QC, in the
maximum at the position of the QC (104, columella, auxin restricts stem cell identity and
109). Computer modeling and the discovery promotes differentiation. This occurs via the
of polar localization of PIN auxin transport AUXIN RESPONSE FACTOR 10 (ARF10)
facilitators to one side of a cell suggest that and ARF16, which are activated by auxin (133).
auxin accumulates in the QC region by a ARF16 is expressed in differentiated columella
rootward-directed auxin transport in the cells and CSCs, and in the double mutant arf10
vasculature and a shootward-directed transport arf16, the CSC daughter cells fail to undergo
in the lateral root cap and epidermis (46, 137). differentiation. Furthermore, increased ARF16
After excision of the root tip or ablation of activity reduces the levels of WOX5 expression
the QC, a new auxin maximum is established a (32). A similar repressive effect on WOX5 can be
few cell layers apically from the new tip and a obtained after application of auxin, which might
new stem cell niche is formed (109, 118, 138), act via auxin-mediated upregulation of ARF16.
suggesting that the auxin maximum and the As WOX5 and ARF16 do not have overlapping
stem cell niche are functionally linked. expression domains, ARF16 might be involved
Auxin function in the stem cell niche is in restricting the WOX5 domain to the QC and
mediated by PLT transcription factors (3, 42). thus allowing CSC daughter cells to differenti-
The activity of the different PLT proteins ate. In summary, the hormone auxin not only
is additive, and manipulating the expression promotes the root stem cell niche, but is also
levels suggests a dose-dependent readout, involved in restricting it.

Quiescence of the Quiescent Center THE VASCULAR STEM
The low mitotic activity of QC cells is caused CELL NICHE
by a prolonged G1 phase. For example, maize The plant vasculature is the main route for
QC cells divide every 180–200 h, compared long-distance transport of water and min-
with a 20-h cell cycle in the proximal meristem erals upward in the xylem and of organic
(7, 28). Recent reports provide insight into how compounds downward in the phloem; it also
the quiescence of QC cells is controlled. First, generates mechanical support for the growing
QC-specific knockout of RBR function indi- stem. Although the cell types are the same in
cates that RBR suppresses cell divisions in the all vascular plants, the architecture of the vas-
QC (131). Second, the oxidized redox status culature varies, even between organs. Despite
of the QC has been proposed to cause arrest its herbaceous nature, Arabidopsis has proven to
at the G1 /S transition (for a review, see 59). be an excellent model system for vascular de-
As this oxidized status is postulated to be due velopment (147). In the Arabidopsis root, the
to auxin degradation, how auxin, redox regula- xylem is located in a central row of cells, with
tion, and cell cycle control are linked will be an the protoxylem located on the marginal posi-
interesting question. tions and the metaxylem in a central position
The biological significance of a low cell (Figure 3a). On the perpendicular axis, two
division rate in the QC is unknown. Notably, poles of phloem are present and the intervening
under certain conditions, cell divisions of QC procambium consists of pluripotent stem cells.
cells do occur and QC derivatives can replace These tissues are surrounded by the pericy-
stem cells. In Arabidopsis thaliana, the QC is cle and together form the vasculature (or stele)
mitotically more active in older roots, and (Figure 3a). In the stem, a ring of vascular
mitosis is induced by stress conditions, altered bundles is present with phloem on the outside,
hormone levels, or a reduced redox status the procambium (or fascicular cambium) in the
(10, 32, 60, 63, 102, 146). In other species with middle and the xylem on the inside (Figure 3b).
larger stem cell niches, such as maize, there is During secondary growth, the fascicular cam-
no clear boundary between mitotically almost bium and the interfascicular cambium (IC) form
inactive QC cells and the dividing stem cells a closed cambium ring. The current opinion,
of the proximal meristem (28, 37). Therefore, supported by transcriptional profiling in Popu-
the QC can be seen as a flexible and responsive lus (116), is that the cambium contains stem cells
organizer that is competent to replenish stem with phloem mother cells on one side and xylem
cells when necessary. mother cells on the other (reviewed in 33).
−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 3
The vascular stem cell niche, with involved cell types shown in color. (a) Organization of vasculature in the Arabidopsis postembryonic
root. (b) Organization of vasculature in the Arabidopsis postembryonic stem. During secondary growth, the intervening procambial cells
(or fascicular cambium) and the interfascicular cambium files start to undergo periclinal divisions to initiate radial growth, continuously
producing the xylem (inward) and phloem (outward) in concentric rings. (c) The CLE–PXY/TDR–WOX4 pathway is involved in stem
cell proliferation and possibly cell division orientation. (d ) In the root, cytokinin (CK) and auxin determine boundary formation
between the procambium and protoxylem. CK is transported from the phloem and binds to hybrid histidine kinase receptors (CRE1/
WOL/AHK4, AHK2, AHK3), inducing autophosphorylation. The phosphate group is then transferred to Arabidopsis histidine
phosphotransfer proteins (AHP1–5), which move into the nucleus and phosphorylate Arabidopsis response regulators (ARRs). Type B
ARRs act as activators and directly induce type A ARRs, which act as repressors (reviewed in 4, 103, 126). The CK signal influences
localization of PIN3 and PIN7, creating an auxin maximum in the xylem. There, auxin induces pseudophosphotransfer protein AHP6,
which acts as an inhibitor of cytokinin signaling and promotes protoxylem formation. (e) In the root, positional information from the
endodermis specifies protoxylem and metaxylem differentiation through HD-ZIPIII protein-level regulation. The SHR gene is
expressed in the stele and the SHR protein moves to the endodermis (red arrow), where it activates SCR gene expression. SHR and SCR
directly activate miR165/166 gene expression, and miR165/166 subsequently moves toward the center of the vasculature.
Downregulation of HD-ZIPIII mRNA by miR165/166 in turn creates a reverse HD-ZIPIII gradient, which specifies dosage-dependent
xylem differentiation.

Stem Cell Maintenance The Arabidopsis TDIF homologs CLE41 and
in the Procambium CLE44 are expressed in the phloem and are
able to induce stem cell proliferation in the
Several key regulators of stem cell maintenance neighboring procambium of the hypocotyl
in the procambium have been identified and and shoot (36, 53, 134) (Figure 3c). The stem
revealed surprising similarities to the apical cells perceive CLE41p/44p via the CLV1-
meristems. Ito et al. (57) set the stage by like PHLOEM INTERCALATED WITH
purifying the CLE peptide TDIF (tracheary XYLEM/TDIF RECEPTOR (PXY/TDR)
element differentiation inhibitory factor), a re- receptor-like kinase (36, 38, 53). In the stems
pressor of xylem differentiation and promoter and petioles of pxy/tdr mutants, the phloem
of cell proliferation in Zinnia cell culture. and xylem are interspersed, the number of
a b
Procambium Procambium
Protoxylem Xylem
Metaxylem Phloem
Phloem Interfascicular
Pericycle cambium
Endodermis
Cortex
Epidermis
c CLE41p/44p d
PXY/TDR Phloem
Phospate group
Xylem Cambium Phloem Procambium
CK
Xylem Type A ARRs
differentiation (ARR5/6)
CK
CRE1/WOL/AHK4,
WOX4 AHK2, AHK3
High CK
AHP1–5
Proliferation
Type B ARRs
(ARR1/10/12) PIN7
PIN3
e High
auxin
SHR
SHR SCR Auxin
Proto- signaling
xylem
AHP6 CK
HD-ZIPIII
signaling
miR165/166
Metaxylem Protoxylem
Endodermis

procambium cells is reduced, and the orien- transcript profiling of Arabidopsis and Populus
tation of procambium cell division is lost (38, cambiums suggests that the known shoot
53). Thus, the differentiating phloem daughter meristem regulators CLV1 (expressed in the
cells provide stem-cell-promoting signals and phloem and cambium) and STM (expressed in
act like niche cells, similar to the OC and QC. the cambium) might also play a role in vascular
Ubiquitous overexpression of the ligand and stem cell maintenance (65, 116, 148). How
the receptor represses xylem differentiation and all these factors regulate vascular stem cells
causes more cells to accumulate in the vascular requires further investigation.
bundle and in the interfascicular region, rem-
iniscent of secondary growth initiation (36).
However, overexpression of CLE41 specifically More Boundaries Within the
in the phloem and ubiquitous overexpression Vascular Stem Cell Niche
of PXY/TDR do not repress xylem differenti- How do the cell types in the vasculature be-
ation, suggesting that the range of CLE41p is come organized within distinct boundaries? In
limited by an unknown mechanism (36). There- the root vasculature, cytokinin moves through
fore, the CLE41p–PXY/TDR module defines symplastic connections in the phloem from the
the boundary between vascular cell types and shoot to the root (13). Cytokinin depletion or
regulates the size of the vascular stem cell reduced cytokinin signaling results in fewer
population. Furthermore, the position of the cells in the vasculature and in all cells having
CLE-peptide-producing cells relative to the protoxylem identity (5, 56, 67, 70, 85–87, 89,
stem cells has been reported to correlate with 143) (Figure 3d ), suggesting that cytokinin
the orientation of stem cell divisions, because promotes proliferation and maintenance of the
ubiquitous and xylem-specific expression of procambium stem cells. Cytokinin signaling
CLE41 induces disoriented procambial cell di- is active in the intervening procambial cell
visions, whereas overexpression of CLE41 in the files adjacent to the xylem axis (12) and affects
phloem (where it is normally expressed) induces localization of PIN3 (expressed in the peri-
only correctly oriented cell divisions (36). cycle adjacent to the protoxylem) and PIN7
CLE41/44 signaling stimulates stem cell (expressed in the procambium and phloem) (12)
divisions in the procambium by promoting (Figure 3d ). This bisymmetric PIN localiza-
expression of the WOX4 gene there (52) tion could channel auxin to the central xylem
(Figure 3c). However, unlike in the pxy/tdr axis, where it would induce expression of the cy-
mutant, loss of WOX4 function does not tokinin signaling repressor gene ARABIDOP-
result in complete loss of the intervening SIS HISTIDINE PHOSPHOTRANSFER
procambial cell layer and does not suppress PROTEIN 6 (AHP6) at the protoxylem posi-
discontinuous xylem strand formation upon tion and consequently protoxylem formation
application of TDIF. This shows that WOX4 (12). Therefore, a mutually inhibitory interac-
mediates only stem cell divisions regulated by tion between cytokinin and auxin determines
PXY/TDR, whereas another still-unidentified boundary formation between procambium
pathway must mediate repression of xylem stem cells and the protoxylem (12).
differentiation by PXY/TDR (52) (Figure 3c). The HD-ZIPIII proteins have recently been
In addition to CLE41p/44p, treatment of shown to restrict the number of procambium
plants with combinations of CLE peptides cells by promoting xylem differentiation (6, 55).
results in cell proliferation in the vasculature SHR and SCR transcription factors directly
(134). Furthermore, the two receptor-like activate miR165a/166b gene expression in the
kinases [MORE LATERAL GROWTH1 endodermis, and miR165/166 moves toward
(MOL1) and REDUCED IN LATERAL the stele center and restricts expression of the
GROWTH1 (RUL1)] seem to affect cambium HD-ZIPIII genes [PHB, PHV, REV, CORONA
activity in an opposite manner (1). Finally, (CNA), ARABIDOPSIS HOMEOBOX GENE

8 (ATHB8)] (Figure 3e) (21). The resulting
HD-ZIPIII protein gradient determines xylem CHROMATIN STATES IN ANIMAL
development in a dosage-dependent manner: STEM CELLS
High levels specify metaxylem and lower
levels protoxylem (21). In conclusion, the In animals, the Oct4/POU5F1, Sox2, and Nanog transcription
neighboring endodermis provides positional factors are found in stem cells and are sufficient to reprogram
information for different cell fates along the differentiated cells into stem cells. This transcriptional program
xylem axis. is implemented in the context of a distinct chromatin state in
stem cells (reviewed in 43, 101, 145). Pluripotent stem cells
Coordination of Longitudinal contain open chromatin compared with differentiated cells: less
and Lateral Growth heterochromatin, more loosely bound (or hyperdynamic) archi-
tectural chromatin proteins, less H3K9 methylation, and global
With increasing height, plants must ensure that
transcriptional hyperactivity. Upon differentiation, the transcrip-
their stems can carry their weight. Interestingly,
tional program needs to be rapidly switched—possibly mediated

plant body weight can induce secondary growth
by the presence of both activating and repressive chromatin marks
in Arabidopsis stems (Figure 3b), because the ad-

(so-called bivalent domains) on lineage-specific developmental
dition of artificial weights (placing a 2.5-g tube
regulators—in a process whereby these regulators are silenced
on the top of an immature plant) can induce
and at the same time poised for activation. In addition, embry-
IC imitation, probably through auxin signaling
onic stem cells are sensitive to reduced levels of key structural
(66).
components of chromatin (cohesin and condensing complexes).
However, a recent study suggests that
there is no linear correlation between plant
height/weight and IC initiation (117). The au-
thors instead found that manipulation of JA
expression in the shoot and root, respectively,
signaling affects secondary growth. Because the
whereas CLE41p positively affects WOX4 ex-
touch-inducible JA signaling gene JAZ10 is ex-
pression in the vasculature (52, 91, 112, 115,
pressed at the base of the stem in the xylem
124). Second, the sources and sinks of the CLE
and IC, it was hypothesized that intratissue
peptides differ: In the shoot meristem, CLV3p
tension might play a role. This tension may
signals from the stem cells to the OC, whereas
arise from divisions in the fascicular cambium
in the root and in the vasculature, differenti-
or from xylem formation, which pushes the
ated stem cell daughters signal back to the niche
cambium outward, inducing JA signaling and
or stem cells (36, 96, 115, 124). Thus, without
thereby causing IC initiation (117). Thus, body
further studies, we cannot determine whether
weight and tension might provide input into the
the repeated use of CLE/WOX modules is co-
cambium stem cell niche.
incidental or reflects adaptations of an ancient
stem-cell-regulating mechanism.
MOLECULAR SIGNATURE There are more striking differences in the
OF PLANT STEM CELLS stem cell niches. Cytokinin signaling is required
The striking similarities between the shoot and in the shoot meristem and vascular stem cells,
root niches in both regulation and develop- whereas auxin is important for root stem cell
ment have been interpreted as an indication maintenance, as discussed above. In addition,
of an evolutionary relationship (112), in line HD-ZIPIII activity needs to be kept high in the
with paleobotanical views that the root evolved shoot meristem (34, 121, 136), but it promotes
from a shoot (106). CLE/WOX modules have vascular xylem differentiation (6, 21, 55) and
been identified for all three stem cell niches dis- represses root development (47).
cussed in this review, but each acts distinctly A yet unanswered question is whether
at the molecular level. First, CLE peptide sig- stem cells have specific stemness factors that
naling negatively regulates WUS and WOX5 make them pluripotent, or are simply any kind

of cell that divides and is blocked from the in Populus are characterized by signal trans-
next step of differentiation. Mutant analysis duction and transcriptional regulation factors
highlighted that chromatin factors and genome (116). The transcription profile of the root
organization factors are pivotal for stem cell cortex/endodermis stem cells shows high ex-
maintenance, and for most of them, it has been pression of the G2 /M-phase-specific genes, and
shown that they regulate key stem cell regula- it was shown that cyclinD6;1 has a role in the
tors (like WUS, WOX5, or PLT) (2, 8, 11, 45, asymmetric division of these stem cells (122).
62, 68, 71). Thus, shoot and root plant stem Shoot stem cells have an overrepresentation of
cells might contain a chromatin state distinct transcripts encoding factors involved in DNA
from that of differentiated cells, a situation metabolism, DNA replication and repair, chro-
that is similar to animal stem cells (see sidebar, mosome organization, and biogenesis (139). To
Chromatin States in Animal Stem Cells). In- elucidate whether there is a signature common
depth understanding of the molecular nature of to all plant stem cells, we will have to await
plant stem cells also profits from transcriptional a systematic comparison of transcriptional
profiling experiments. The cambial stem cells profiles.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
We thank Leron Katsir for critical comments on the manuscript. We apologize to colleagues
whose work could not be cited owing to space constraints. Work in our laboratory is supported
by grants from the DFG to T.L. as part of the SFB592 program, from the European Union as
part of the ERA-PG program, and from the BMBF as part of the FRISYS program, as well as an
EMBO postdoctoral fellowship to N.K.
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Annual Review of
Plant Biology
Contents Volume 63, 2012
There Ought to Be an Equation for That

Joseph A. Berry ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 1
Photorespiration and the Evolution of C4 Photosynthesis

Rowan F. Sage, Tammy L. Sage, and Ferit Kocacinar ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣19

The Evolution of Flavin-Binding Photoreceptors: An Ancient
Chromophore Serving Trendy Blue-Light Sensors
Aba Losi and Wolfgang Gärtner ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣49
The Shikimate Pathway and Aromatic Amino Acid Biosynthesis
in Plants
Hiroshi Maeda and Natalia Dudareva ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣73
Regulation of Seed Germination and Seedling Growth by Chemical
Signals from Burning Vegetation
David C. Nelson, Gavin R. Flematti, Emilio L. Ghisalberti, Kingsley W. Dixon,
and Steven M. Smith ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 107
Iron Uptake, Translocation, and Regulation in Higher Plants
Takanori Kobayashi and Naoko K. Nishizawa ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 131
Plant Nitrogen Assimilation and Use Efficiency
Guohua Xu, Xiaorong Fan, and Anthony J. Miller ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 153
Vacuolar Transporters in Their Physiological Context
Enrico Martinoia, Stefan Meyer, Alexis De Angeli, and Réka Nagy ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 183
Autophagy: Pathways for Self-Eating in Plant Cells
Yimo Liu and Diane C. Bassham ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 215
Plasmodesmata Paradigm Shift: Regulation from Without
Versus Within
Tessa M. Burch-Smith and Patricia C. Zambryski ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 239
Small Molecules Present Large Opportunities in Plant Biology
Glenn R. Hicks and Natasha V. Raikhel ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 261
Genome-Enabled Insights into Legume Biology
Nevin D. Young and Arvind K. Bharti ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 283
v
Synthetic Chromosome Platforms in Plants
Robert T. Gaeta, Rick E. Masonbrink, Lakshminarasimhan Krishnaswamy,
Changzeng Zhao, and James A. Birchler ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 307
Epigenetic Mechanisms Underlying Genomic Imprinting in Plants
Claudia Köhler, Philip Wolff, and Charles Spillane ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 331
Cytokinin Signaling Networks
Ildoo Hwang, Jen Sheen, and Bruno Müller ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 353
Growth Control and Cell Wall Signaling in Plants
Sebastian Wolf, Kian Hématy, and Herman Höfte ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 381
Phosphoinositide Signaling
Wendy F. Boss and Yang Ju Im ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 409
Plant Defense Against Herbivores: Chemical Aspects

Axel Mithöfer and Wilhelm Boland ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 431
Plant Innate Immunity: Perception of Conserved Microbial Signatures
Benjamin Schwessinger and Pamela C. Ronald ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 451
Early Embryogenesis in Flowering Plants: Setting Up
the Basic Body Pattern
Steffen Lau, Daniel Slane, Ole Herud, Jixiang Kong, and Gerd Jürgens ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 483
Seed Germination and Vigor
Loı̈c Rajjou, Manuel Duval, Karine Gallardo, Julie Catusse, Julia Bally,
Claudette Job, and Dominique Job ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 507
A New Development: Evolving Concepts in Leaf Ontogeny
Brad T. Townsley and Neelima R. Sinha ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 535
Control of Arabidopsis Root Development
Jalean J. Petricka, Cara M. Winter, and Philip N. Benfey ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 563
Mechanisms of Stomatal Development
Lynn Jo Pillitteri and Keiko U. Torii ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 591
Plant Stem Cell Niches
Ernst Aichinger, Noortje Kornet, Thomas Friedrich, and Thomas Laux ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 615
The Effects of Tropospheric Ozone on Net Primary Productivity
and Implications for Climate Change
Elizabeth A. Ainsworth, Craig R. Yendrek, Stephen Sitch, William J. Collins,
and Lisa D. Emberson ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 637
Quantitative Imaging with Fluorescent Biosensors
Sakiko Okumoto, Alexander Jones, and Wolf B. Frommer ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ 663
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Plant Stem Cell Niches

Ernst Aichinger,1,2 Noortje Kornet,1

79104 Freiburg, Germany; email: laux@biologie.uni-freiburg.de

Freiburg Institute of Advanced Studies (FRIAS), D-79104 Freiburg, Germany

Annu. Rev. Plant Biol. 2012. 63:615–36 Keywords

How new cells are produced has been

Control of the Stem Cell Number . . 620

616 Aichinger et al.

cells from which lateral organs are derived,

www.annualreviews.org • Plant Stem Cell Niches 617

The Arabidopsis ortholog SHOOTMERIS- and exogenous application of cytokinins or

618 Aichinger et al.

www.annualreviews.org • Plant Stem Cell Niches 619

ing. ZLL expression in the underlying vascular

620 Aichinger et al.

CLV3p is perceived by a multitude of recep- odds with such a mechanism: CLV3-dependent

www.annualreviews.org • Plant Stem Cell Niches 621

shift of the auxin maxima marking lateral organ (149).

also has a non-cell-autonomous function in sociated downregulation of cytokinin response

622 Aichinger et al.

TPST RGF1/2/3 RGF PLT

www.annualreviews.org • Plant Stem Cell Niches 623

in maize root consists of up to 1,000 cells and

624 Aichinger et al.

www.annualreviews.org • Plant Stem Cell Niches 625

626 Aichinger et al.

www.annualreviews.org • Plant Stem Cell Niches 627

628 Aichinger et al.

tional program needs to be rapidly switched—possibly mediated

in Arabidopsis stems (Figure 3b), because the ad-

www.annualreviews.org • Plant Stem Cell Niches 629

630 Aichinger et al.

network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

www.annualreviews.org • Plant Stem Cell Niches 631

of isopentenyl-type cytokinins. Plant Physiol. 126:1370–80

632 Aichinger et al.

www.annualreviews.org • Plant Stem Cell Niches 633

89. Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Vaclavikova K, et al. 2008.

634 Aichinger et al.

www.annualreviews.org • Plant Stem Cell Niches 635

flow in plants. Science 312:883

636 Aichinger et al.

Contents Volume 63, 2012

There Ought to Be an Equation for That

Photorespiration and the Evolution of C4 Photosynthesis

Rowan F. Sage, Tammy L. Sage, and Ferit Kocacinar ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣ ♣19

Plant Defense Against Herbivores: Chemical Aspects

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