1 Institute of Plant Biology, University of Zürich, Zollikerstraße
107, 8008 Zürich, Switzerland
2 Institute of Biologie III, University of Freiburg, Schänzlestraße
1, 79104 Freiburg, Germany
* Author for correspondence (e-mail: laux{at}biologie.uni-freiburg.de)
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Summary |
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Key words: Stem cells, Shoot meristem, Arabidopsis
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Introduction |
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|
The caveat of the above stem cell definition is, however, that it is based
on something the stem cell daughters do but tells us little about the nature
of a stem cell itself. Can we define a stem cell in molecular terms? In many
cases, molecular markers have been identified that allow enrichment for stem
cells (Blau et al., 2001;
Kornblum and Geschwind, 2001
;
Lagasse et al., 2000
).
However, it is often unclear whether such molecules are necessary components
of stem cell identity.
In plants, all postembryonically formed cells and organs are ultimately
derived from small stem cell populations in the apical shoot and root
meristems, which allow generation of new organs over a life span that can be
more than a thousand years. In addition, plants possess stem cells that have
more tissue-specific functions, such as to provide cells for gird growth. The
apical meristems are especially suitable for studies of stem cell biology. For
example, mutant sectors can be generated and the progeny of a single stem cell
can be followed. This has allowed determination of the numbers, potency and
proliferative properties of shoot meristem stem cells
(Furner and Pumfrey, 1992;
Irish and Sussex, 1992
;
Ruth et al., 1985
;
Stewart and Dermen, 1970
).
Here, we discuss our current knowledge of stem cell regulation in the shoot
meristem. For information on general shoot meristem development and function,
the reader is referred to several excellent reviews
(Barton, 1998
;
Bowman and Eshed, 2000
;
Clark, 1997
;
Meyerowitz, 1997
).
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Stem cells in the shoot apical meristem |
---|
|
Elegant clonal studies demonstrated that within a given layer all cells are
ultimately derived from 2-3 long-term stem cells
(Furner and Pumfrey, 1992;
Irish and Sussex, 1992
;
Schnittger et al., 1996
;
Stewart and Dermen, 1970
). In
addition, their immediate daughter cells can still act as transiently active
short-term stem cells, giving rise to a more restricted part of the plant
(Stewart and Dermen, 1970
). In
privet, it has been estimated that the short-term stem cells are replaced on
average every 14 days, whereas the long-term stem cells can be active
throughout the plants life (Stewart and
Dermen, 1970
). What could distinguish long-term from short-term
stem cells? It is possible that the only difference is their position: the
short-term cells at the rim of the stem cell pool are next to be `pushed out'
by divisions of central cells, whereas the central ones have a better chance
of staying for a longer time (Ball,
1960
). This division of labor might allow plants to reduce the
number of cell divisions of their long-term stem cells and thus maintain them
as a relatively error-free genetic blueprint.
The CZ is identified by its relatively weak cytoplasmic staining and low
rate of cell division. Although the stem cells cannot be recognized
histologically, on the basis of geometrical considerations one can predict
that they are located in the three outermost cell layers of the CZ. Thus, if
one assumes that the CZ in Arabidopsis it is about 5-6 cells high
(Fig. 2)
(Vaughan, 1955), the stem
cells occupy only about the upper half of it. Are the stem cells different
from surrounding cells in the shoot apex? The presumed stem cell region is
characterized by the expression of the CLAVATA3 (CLV3) gene, which is
thus used as an operational stem cell marker for the shoot meristem
(Fletcher et al., 1999
). This
indicates that the stem cells of the shoot meristem are distinct from the
other cells. Note, however, that mutants lacking CLV3 activity
possess stem cells, indicating that CLV3 is not essential for stem
cell identity (Clark et al.,
1995
).
Cells that exit the stem cell pool initiate differentiation and form
lateral organs (leaves, side shoots and flowers) in the ringshaped peripheral
zone surrounding the CZ, and central stem tissue from the rib zone underneath
the CZ. The earliest molecular changes known to occur are the downregulation
of CLV3 expression (Fletcher et
al., 1999) and the subsequent activation of several genes, such as
ZWILLE (ZLL)/PINHEAD (Lynn et
al., 1999
; Moussian et al.,
1998
). Eventually expression of the SHOOTMERISTEMLESS
(STM) gene is downregulated in organ anlagen, and organ development takes
place (Long et al., 1996
) (see
below).
In summary, the shoot meristem displays a succession of distinct cell states, from the central stem cells to the cells in organ primordia at the periphery, whose proper specification is essential for meristem function.
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Specification of stem cell identity in the shoot meristem |
---|
During shoot meristem initiation, the first organs appear to be formed
independently of the stem cells but subsequent organs are not
(Fig. 3)
(Sussex and Rosenthal, 1973).
One can therefore predict that mutants defective in stem cell specification
may form seedlings that have a normal pair of first, non-stem-cell-derived
`leaves' (the cotyledons) but no functional stem cells. This is the case in
Arabidopsis wuschel (wus) mutants, where the putative stem cells are
partially differentiated (Laux et al.,
1996
). WUS encodes a homeodomain protein and is expressed
in a group of
10 cells in the CZ of the meristem
(Fig. 4)
(Mayer et al., 1998
), which
are located underneath the three outermost cell layers that contain the stem
cells in the vegetative shoot meristem and one cell layer higher in embryonic
and floral meristems. Together with the finding that WUS is
sufficient to induce expression of CLV3
(Schoof et al., 2000
), these
observations suggest that the stem cells of the shoot meristem are specified
by signaling from the WUS-expressing cells, termed the organizing
center (OC; Fig. 4). Studies of
the function of the putative WUS orthologs in Petunia and
Antirrhinum support this model (M. Kieffer, H. Cook, Y. Stern et al.,
unpublished; Stuurman et al.,
2002
). Thus, the shoot meristem provides one of the few examples
where the presence of a stem cell niche can be shown genetically by the
requirement for non-cell-autonomous activities of neighboring cells to specify
stem cell identity.
|
|
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Feedback from the stem cells establishes a self-regulatory system |
---|
The results of surgical destruction of the shoot meristem apical cells
suggested that the stem cells inhibit stem cell fate in their daughters by
lateral suppression and thus themselves are involved in controlling the
boundaries of the stem cell pool (Loiseau,
1959; Pilkington,
1929
). Genetic analysis in Arabidopsis has verified this
and revealed that the size of the stem cell population is regulated through
size regulation of the OC. Mutations in the CLV genes result in
largely increased shoot and floral meristem sizes owing to accumulation of
CLV3-expressing stem cells (Fig.
3) (Clark, 1997
;
Fletcher et al., 1999
;
Laufs et al., 1998
). The
CLV3 gene encodes a small peptide that is secreted into the
extracellular space, where it presumably acts as a ligand for the CLV1
receptor-like kinase, which is expressed throughout most of the shoot meristem
(Clark et al., 1997
;
Fletcher et al., 1999
;
Rojo et al., 2002
;
Trotochaud et al., 1999
).
Besides CLV1 and CLV3, additional proteins and genetic loci that
participate in CLV-dependent signaling have been identified. CLV1 protein is
stabilized by CLV2, a receptorlike molecule lacking the intracellular kinase
domain that might form heterodimers with CLV1
(Jeong et al., 1999).
Furthermore, SHEPHERD, an HSP90-related protein that is thought to act as an
ER-localized chaperone (Ishiguro et al.,
2002
), is required for CLV signaling, which suggests that it is
either necessary for secretion of functional CLV3 protein or for assembly of a
functional CLV1-CLV2 receptor complex. Inside the cell, CLV1/CLV3 signaling is
negatively regulated by KAPP, a protein phosphatase
(Trotochaud et al., 1999
), and
antagonized by POLTERGEIST, which appears to act downstream of the
CLV loci (Yu et al.,
2000
).
What are the targets of CLV signaling? wus mutations are epistatic
to clv, mutations in any of the three CLV genes result in an
expanded WUS expression domain, and ectopic expression of
CLV3 is sufficient to repress WUS
(Brand et al., 2000;
Laux et al., 1996
;
Schoof et al., 2000
). These
results indicate that CLV3 signaling restricts the size of the stem cell pool
by restricting the size of the WUS expression domain. Thus, the
balance between stem cells and differentiating cells appears to be dynamically
regulated by a negative feedback loop between the OC and stem cells that
involves the WUS and CLV3 genes: signaling from the OC
confers stem cell identity to the cells in the three outermost layers, which
in turn signal back to limit the size of the OC
(Fig. 4)
(Schoof et al., 2000
). If, for
example, the number of stem cells is too small, a reduced amount of CLV3
signal will lead to an expanded WUS expression domain, which in turn
will result in the induction of more stem cells. This model for size
regulation of the stem cell population by the OC is in line with previous
findings from periclinal chimaeras in tomato, which showed that the floral
meristem size is determined by the genotype of the L3 cells
(Szymkowiak and Sussex,
1992
)
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Targeting the signals |
---|
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Turning meristem cells into organs |
---|
In addition to STM and WUS activities, maintaining the shoot meristem cells
in an undifferentiated state requires signaling from the organ primordia back
to the shoot apex (Waites et al.,
1998). In general, adaxial (upper) leaf identity appears to be
required for meristem maintenance, whereas abaxial leaf identity is
incompatible with it (Bowman and Eshed,
2000
; McConnell and Barton,
1998
).
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Making stem cells |
---|
|
Analysis of the zwille (zll, also named pinhead)
mutant has given some indication of how stem cell initiation is coordinated
with the rest of the embryo. In zll embryos, the expression pattern
of shoot meristem genes is randomized but still restricted to the shoot apex
(Lynn et al., 1999;
Moussian et al., 1998
). At
late stages, shoot meristem gene expression is shut off, and the cells at the
stem cell position differentiate (Endrizzi
et al., 1996
; McConnell and
Barton, 1995
; Moussian et al.,
1998
). During early embryo development, ZLL is expressed
in the precursor cells of the vasculature, directly underneath the shoot
meristem primordium, and later in the adaxial (upper) side of cotyledonary
primordia (Lynn et al., 1999
;
Moussian et al., 1998
).
Expression of ZLL in the abaxial (lower) instead of the abaxial side
of the cotyledonary primordia resulted in their transformation into
indeterminate axes with ectopic shoot meristems
(Newman et al., 2002
).
Together these observations indicate that stem cell formation requires
ZLL-dependent signals from neighboring embryonic cells. Similarly,
postembryonic ZLL activity in the vascular primordia and/or the
adaxial part of leaf primordia is important for the formation of axillary
meristems (Lynn et al.,
1999
).
ZLL encodes one of the name-giving members of a protein family
with a PAZ (PIWI ARGONAUTE ZWILLE) domain,
which is highly conserved throughout the animal and plant kingdom
(Cerutti et al., 2000). Recent
evidence shows that some PAZ proteins are members of complexes that bind micro
RNAs small RNA molecules of
20 nucleotides
(Hammond et al., 2001
;
Mourelatos et al., 2002
)
which in turn allow binding to homologous sequences of specific mRNA
species. Since one member of the PAZ family is the putative translation
initiation factor eIF2C from rabbit (Zou
et al., 1998
), and double mutants of zll and its relative
argonaute produce STM mRNA but no STM protein, an attractive
hypothesis is that ZLL functions in translational regulation of specific mRNA
species required for shoot meristem development
(Lynn et al., 1999
).
Formation of stem cells from differentiated cells
Plants can also form stem cells de novo from differentiated cells. For
example, the expression pattern of meristem genes suggests that floral
meristems that arise at the periphery of the inflorescence meristem are not
contiguous with the inflorescence meristem but are initiated de novo
(Mayer et al., 1998;
Otsuga et al., 2001
). While
the cells that give rise to floral meristems are still relatively
undifferentiated, plants clearly can also form meristems from fully
differentiated cells. For example, differentiated leaf epidermal cells can
give rise to leaf-borne embryos with apical meristems
(Taylor, 1967
). In the root,
lateral root meristems are initiated from differentiated pericycle cells
(Malamy and Benfey, 1997
). The
capacity of differentiated plant cells to dedifferentiate and to give rise to
stem cells, either through the induction of meristems or through somatic
embryo formation, provides an important tool for regenerative biology. It
should be noted, however, that in many cases the cells from which the stem
cells ultimately originate and their differentiation state are not precisely
known.
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Termination of stem cells |
---|
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Common principles in stem cell regulation |
---|
Traditionally plant stem cells have been considered to be fundamentally
different from animal stem cells. However, recent advances suggest that plant
and animal stem cells are functionally equivalent and regulated by common
principles. A major perceived difference is that plant stem cells are
regulated by positional information, whereas animal stem cells have been
viewed as cell lineages of a fixed fate. However, it now has become clear that
at least many animal stem cells are similarly specified by signals from their
neighborhood (Spradling et al.,
2001). For example, the germ line stem cells in the oviduct of
C. elegans are specified by signals from a single cell the distal tip
cell, that suppress differentiation (meiosis) and maintain mitotic divisions
(Berry et al., 1997
;
Henderson et al., 1994
).
A second apparent difference is that plant stem cells are considered to
have a much broader developmental program (they give rise to complete organs)
than their animal counterparts, which regenerate cells restricted to one
tissue type. However, recent findings have shown that in both cases the
developmental capacity of stem cells is not an inherent property of the stem
cell but instead dictated by the environment the daughter cells are exposed
to, and can be dramatically expanded if this environment is altered
(Blau et al., 2001;
Morrison, 2001
;
Steeves and Sussex, 1989
).
Are there also molecular similarities? This question is still difficult to
answer since we know too little of the molecules that are important for stem
cell generation and maintenance. Interestingly, one of the first
ZLL-related genes identified, PIWI, functions in the
regulation of stem cell maintenance in the Drosophila germarium
(Cox et al., 1999), which
suggests that there are at least some similarities. However, there are no
obvious candidates for the WUS or CLV3 genes in animals,
which could reflect the different cellular constitutions of plant and animal
stem cell niches, i.e. a dividing cell population versus a stable cavity.
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Conclusion and perspectives |
---|
Many of the regulatory principles appear to be common to a wide range of
stem cell systems in plants and animals. But still we do not know what a stem
cell is in molecular terms. What are the molecular factors that impart
pluripotency on a cell? Many hypotheses have implicated chromatin structure in
cell potency but, although this is an attractive possibility, robust
experimental data are not yet available. Do stem cells express specific genes
that confer `stemness' or is it sufficient to protect them against
differentiation signals? Is there a universal stem cell factor? Now that we
are able to mark and to purify stem cells, their molecular profiles can be
obtained that may allow answers to these questions
(Phillips et al., 2000;
Terskikh et al., 2001
).
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Acknowledgments |
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