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Apical Meristems
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Dennis Francis, Cardiff University, Cardiff, UK
. Apical Meristems
The cells in the meristem do not all divide at the same rate; the control of the cell cycle in
meristems is the subject of current research.
Apical Meristems
The true vegetative shoot apical meristem (SAM) comprises a relatively small population of cells above the
youngest primordium varying from as few as 50 cells in
Arabidopsis thaliana to over 1000 in Chrysanthemum
segetum. This cell population conforms to an apical dome,
which can be pronounced in some species (e.g. Lolium
temulentum) but flattened in others (e.g. Helianthus
annuus). Apical dome size varies between species (Table 1);
the basal diameter of the dome can vary from 50 to 3000 mm
(Mauseth, 1991). However, in the 250 000 angiosperms
worldwide, there will probably be some that exhibit larger
apical domes than indicated in Table 1.
A vegetative SAM changes size constantly. Through cell
division, it increases to a threshold size large enough to
partition itself into a smaller dome, primordia and
subapical tissue (Figure 1). The interval between the
initiation of successive primordia is defined as the
plastochron. The process will be repeated in a semiiterative fashion because, during vegetative growth, the
plastochron tends to lengthen; this, in turn, is reflected in
different growth rates between successive plastochrons
(Lyndon, 1977). Notably, the apical dome cells exhibit
exponential cell cycle kinetics so that dome growth during
successive plastochrons can be expressed as sawtooth plots
when temporal increases in cell number are plotted on a
loge scale.
Vegetative SAMs are described in at least three different
ways: according to planes of division (Tunica Corpus
theory), according to cell fates (L1, L2, L3) or according to
cell size/rates of cell division (zonation). The Tunica
Corpus theory (Schüepp, 1917) supports the partitioning
of cells into domains according to their plane of cell
division. In the tunica, cells divide with the plane of
chromosome separation at anaphase parallel to the surface
Table 1 Sample of vegetative apical domes ranked in order of
increasing size (for a review, see Francis, 1997)
Diameter of vegetative
apical dome (mm)
Plant
Arabidopsis thaliana
Helianthus annuus
Silene coeli-rosa
Chrysanthemum segetum
50
70
100
1400
. Cell Cycle Control in Meristems
(anticlinal). Typically the tunica is confined to the outer cell
layers. In the corpus, cells divide in any plane and this
domain is inside the tunica. Most dicotyledonous apical
domes exhibit a tunica of two to four layers. When there are
two tunica layers they are often described as L1 and L2,
with L3 representing the outermost layer of corpus. As
mentioned above, leaves are initiated from the apical
dome. Fate maps of leaves often indicate plasticity because
cells in a particular leaf tissue may be derived from all three
layers, but sometimes only from L1 and L2. In other words,
cell layers of the apical dome might be best regarded as
sources of cells, while fate is imposed on them through
positional controls during development (Lyndon, 1998).
On the basis of cell size and rates of cell division, different
regions of the dome can be classified in different zones: a
central zone (CZ) of large slowly dividing cells, a peripheral
zone (PZ) of smaller, faster dividing cells and a pith-rib
meristem (PRM) of cells with intermediate size and an
intermediate rate of cell division relative to the CZ and PZ
(Nougarède, 1967). Leaf primordia arise on the side of the
dome from cells of the PZ, which, as explained above, can
include L1, L2 and L3 layers. In the garden pea, the
primordium begins as a cohort of periclinal cell divisions
(plane of anaphase separation at 908 to the surface) within
the PZ occurring about one-third of the way through a
plastochron (Lyndon, 1970). In general terms, leaf initiation is a function of both the plane of cell division in the PZ
coupled with changes in the elasticity of the cell walls of the
epidermal cells at the point of primordium outgrowth
(Green, 1994). However, the primary signal for leaf
primordium initiation has yet to be discovered.
At the end of each plastochron, part of the PRM is
partitioned into the subapical region. Within this region
are the progenitor cells for both the internode and node
although it is impossible to resolve these tissues at this early
stage (Figure 1).
Recent studies of mutants of Arabidopsis, which are
deficient in normal SAM function, have led to the
discovery of genes that regulate vegetative development.
For example, the shootmeristemless (stm) mutant of
Arabidopsis is virtually unable to form a shoot meristem
and is regarded as a more severe mutation than the socalled topless (tpl) mutant, which is also unable to form a
shoot meristem (Evans and Barton, 1997). SHOOTMERISTEMLESS (STM) encodes a KNOTTED1-type of
homeodomain protein, which is first detected in one to two
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1
Apical Meristems
Figure 1 Median longitudinal section of a shoot apical meristem of the grass, Dactylis glomerata. A is the apical dome; B is the subapical region containing
the new leaf primordium as a bump on the left side adjacent to a central region in which the progenitor cells of the node and internode are located. Bar, 100
mm.
cells of the late globular stage of embryogenesis. First
discovered in maize, mutations in KN1 result in knots of
tissue forming around veins of the leaf blades (reviewed by
Evans and Barton, 1997). A consensus view is that STM is a
transcription factor regulating the expression of other
genes, including TPL. Another target gene is WUCHSEL,
which is required for cell identity in the centre of the SAM.
This gene cascade is essential for normal SAM morphogenesis (Evans and Barton, 1997). STM also has important
interactions with CLAVATA1(CLV1), the expression of
which can regulate the number of cell layers within the
meristem. One idea was that STM:CLV1 could regulate
cell fates in the meristem (Laux and Shoof, 1997).
Root apical meristems are located in the tips of roots and
can comprise between 125 000 and 250 000 cells spanning
approximately 2 mm of apical tissue. Root apical meristems exhibit specific tissue domains. At the centre is the
central stele, surrounded by the cortex, which is in turn
surrounded by the epidermal layer. Classically, these three
layers correspond to Hanstein’s (1870) histogens: the
periblem, plerome and dermatogen, which were perceived
as discrete domains of founder cells for each tissue. These
terms were originally applied to shoot apices but the
plerome and periblem are not easily distinguishable in
SAMs. Strictly speaking, the RAM is subapical in that it is
protected by a root cap, thus invoking Hanstein’s fourth
histogen, the calypterogen. Hence, the RAM gives rise to
cells of the various tissue domains, including the root cap.
The histogens were shown to be less specific in terms of
2
tissue-organizing ability by F. A. L. Clowes at Oxford, who
predicted, and subsequently discovered, a population of
cells at the pole of the various tissue domains that divided
much more slowly than surrounding cells (Clowes, 1954,
1956). This was the quiescent centre (QC), which led
Clowes to develop a theory of root growth based on apical
initials displaced from the QC by cell division, which then
surround the quiescent centre. Central to this theory was
that the apical initials themselves have no set fate but give
rise to descendants, which then establish the tissue domains
(Clowes, 1967). The cells of the QC are stimulated into
more rapid cell division by decapping, tissue damage or by
radiation leading to regeneration of the lost parts (Clowes,
1970). Hence, QC cells would conform to a population of
founder cells (Barlow, 1997). More recently, Scheres and
colleagues in Utrecht, using laser ablation on roots of
Arabidopsis, have demonstrated that QC cells exert a
negative regulation of cell differentiation on surface
contacting apical initials. These observations conformed
to a hypothesis whereby QC cells repress the differentiation
of contacting apical initials, enabling the latter to divide
(van den Berg et al., 1997).
Clearly, the frequency of cell division is highest in the
RAM and SAM of the plant. At the margins of the RAM,
cells are left behind to elongate and differentiate. Thus, at
this boundary region, the meristem is exhibiting steadystate cell cycle kinetics, where a cell division at the
periphery of the meristem results in one cell elongating
while the other remains part of the proliferative pool. This
ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net
Apical Meristems
helps to explain how the RAM remains fairly constant in
size during root growth, whereas the SAM is constantly
changing size (see above).
Cell Cycle Control in Meristems
Clearly, there are many cell divisions that occur in
meristems during the development of the plant. However,
not all meristem cells divide at the same time. Indeed, there
is evidence showing that substantial proportions of cells
are nondividing in RAMs (e.g. cells within the quiescent
centre – see above) and are scattered throughout SAMs
(Gonthier et al., 1987; Kinsman et al., 1997).
Cells achieve competence for cell division during the cell
cycle, which consists of four distinct phases: G1 (postmitotic interphase), S phase (period of DNA synthesis), G2
(postsynthetic interphase) and mitosis (M). Major checkpoints of the eukaryote cell cycle, at G1/S and G2/M, are
governed by the expression of cell division cycle (cdc) genes
or the closely related cyclin-dependent kinase (cdk) genes.
At G2/M a protein kinase encoded by cdc2 binds to a cyclin
(cyclins A/B), so called because its concentration reaches a
peak at a specific point in the cell cycle. This binding
contributes to the activation of the Cdc2 kinase, which
drives the cell into mitosis (Norbury and Nurse, 1992). In
vertebrates, another class of cyclins, the D types, are
critical for the entry of cells from a noncycling condition
(G0) into the cell cycle. In the presence of serum growth
factor, cyclin D1 is upregulated, which in turn leads to
transcriptional activation of cyclins D2 and D3 (Scherr,
1996). Homologues to these D cyclins have been cloned in
Arabidopsis. The so-called cycD2At is upregulated by
sucrose whereas cycD3At is activated by cytokinin,
provided that sucrose is present (Soni et al., 1995). It
seems likely that this is a major control regulating the
proportion of cycling cells in meristems. Remarkably, the
overexpression of cycD3At in tobacco led to a more rapid
growth rate in these transgenic plants, which is consistent
with the idea that the number of dividing cells in meristems
has an impact on plant growth (Cockcroft et al., 2000).
In Arabidopsis, cdc2b is expressed at the G2/M transition
together with cyclin B and cyclin A. The expression of all of
these genes is essential, but exactly what cyclin binds to
which Cdk is a subject of current research (Mironov et al.,
1999). Working on Arabidopsis, Inze and his colleagues at
Ghent spliced the promoter of cdc2 to the b-glucuronidase
(GUS) reporter gene and studied the spatial expression of
the gene during root development. The GUS staining
patterns obtained were consistent with high Cdk activity in
the RAM but also in the pericycle, the outermost layer of
the stele from which laterals arise (Hemerly et al., 1993).
These observations were consistent in revealing that cdc2
expression was indicative of division competence. Very
recent work from Inze’s laboratory has indicated that
lateral root initiation requires the expression of a newly
discovered cyclin, cycd4At (De Veylder et al., 1999).
SAMs exhibit gradients of cell division, slowest in the
CZ, fastest in the PZ and intermediate in the PRM. For
example, in Chrysanthemum at 208C, cell cycle times for the
CZ, PZ and PRM were 139, 48 and 70 h, respectively
(Rembur and Nougarède, 1977). Clearly, Cdk activity is
high in SAMs but the mechanism for spatial regulation of
cell division is unknown. However, it is anticipated that
there will be links between genes that regulate development
and those that control the cell cycle. One clue in this
direction was the finding that a gene that is essential for
megagametophyte and embryo development, PROLIFERA, encodes a minichromosome maintenance (MCM)like protein; MCMs are important regulators of DNA
replication (Springer et al., 1995). Integration of the data is
shedding light on the way that extracellular growth factors
impinge on the cell cycle. For example, gibberellic acid
treatment can lead to the upregulation of Cdc2 in rice and
cytokinins can influence the activation of Cdc2 in the
garden pea (for a review, see Francis and Sorrell, 2000).
Over the next few years it is anticipated that Cdk–cyclin
interactions will be verified in plants and that signal
transduction chains mediated by plant growth regulators
that interface with cell cycle control will be resolved, as will
some of the links between developmental genes and cell
cycle genes. Integration of the data on such interactions
will be important in understanding cell cycle regulation in
meristems during higher plant development.
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Further Reading
Francis D, Dudits D and Inze D (1998) Plant Cell Division. London:
Portland Press.
Lyndon RF (1998) The Shoot Apical Meristem. Cambridge: Cambridge
University Press.
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Plant Physiology, 2nd edn, chap. 16. Sunderland, MA: Sinauer
Associates.
Wolpert L (1998) Plant development. In: Principles of Development,
chap. 7. Oxford: Oxford University Press.
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