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Review
Blackwell Publishing Ltd.
Tansley review
Models of shoot apical meristem
function
Author for correspondence:
Fiona Tooke
Email: [email protected]
Received: 16 January 2003
Accepted: 3 April 2003
Fiona Tooke† and Nick Battey
†Department of Plant Sciences, Cambridge University, Cambridge, CB2 3EA, UK; School of Plant
Sciences, The University of Reading, Whiteknights, Reading, RG6 6AS, UK
doi: 10.1046/j.1469-8137.2003.00803.x
Contents
Summary
37
V. Developmental genetics
44
I.
37
VI. Conclusions
49
II. How things began
38
Acknowledgements
50
III. Cytology
39
References
50
IV. Morphology
41
Introduction
Summary
Key words: shoot apical meristem,
models, flower initiation, leaf
initiation, growth, developmental
genetics.
In this review we describe how concepts of shoot apical meristem function have
developed over time. The role of the scientist is emphasized, as proposer, receiver
and evaluator of ideas about the shoot apical meristem. Models have become
increasingly popular over the last 250 years, and we consider their role. They provide
valuable grounding for the development of hypotheses, but in addition they have a
strong human element and their uptake relies on various degrees of persuasion. The
most influential models are probably those that most data support, consolidating them
as an insight into reality; but they also work by altering how we see meristems, redirecting us to influence the data we collect and the questions we consider meaningful.
© New Phytologist (2003) 159: 37–52
I. Introduction
During embryogenesis certain cells gain the potential to produce
the roots and shoots of a plant. These zones of cells have
become known as the root and shoot apical meristems. The
latter, often after a period of dormancy in the seed, functions to
produce the entire above-ground structure of the plant. What
we know about this process, and how we now perceive the shoot
© New Phytologist (2003) 159: 37 – 52 www.newphytologist.com
apical meristem is a consequence of a long history of research,
through which has emerged a number of key models, influential to many but traceable back to a dominant few.
The many facets of the shoot apical meristem provide
tremendous scope for different interpretations. Below, in Fig. 1,
are four views of the shoot apical meristem. Notice what
aspects each view emphasizes: in the transverse section, the clear
phyllotactic arrangement and the organ initiation function
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Fig. 1 Views of the shoot apical meristem. (a) Transverse section of the terminal bud of Ligustrum vulgare (1, shoot apex; 2, youngest leaf
primordia; 3, older leaves). (b) Longitudinal section of the shoot apical meristem of Zea mays (1, shoot apex; 2, new leaf; 3, previous leaf; 4,
primary thickening meristem; 5, procambial strand). (c) Transmission electron microscope image of Linum usitatissimum (1, stoma; 2, bud).
(d) Top view of the shoot tip of Aeonium. Reprinted from Bowes (1996), with permission from T. Norman Tait.
are of apparent; in the longitudinal section, the cellular organization and outgrowth of primordia at the periphery can be
seen; by scanning electron microscopy the shoot architecture
is visible; and in the living plant, the lateral outgrowths from the
meristem and the integration of growth and development
over time is shown. How would you describe how this system
works? What or who influences you in your description?
In nearly 250 years of shoot apical meristem research,
many would probably agree with the experience of being
‘thrilled by the translucent, glistening beauty of the apical
meristem and surrounding leaf primordia’ described by Sussex
(1998). From this perspective, driven by an enthusiasm to
find out how the shoot apical meristem works, it is perhaps
hard to conceive that very different perceptions of it could
exist. Indeed, it might be assumed that progress to today’s
understanding of the genetic principles underlying shoot apical meristem structure and function would have been quicker,
but for technological or resource constraints. Yet this is only
partly correct. The recognition that the paths we are now on
were not always taken at the first opportunity shows the
importance of individual judgements, and that arrival at
today’s models of genetic determinism was perhaps not
inevitable. Goebel (1926) commented that, ‘it is not the facts
thereby attained but the conclusions drawn from them that
determine the progress of science. These conclusions are influenced not only by each particular investigator’s individuality
but by the general posture of science in his day.’
The purpose of this review is to chart the prominent people,
from Wolff in the 1700s to Weigel now, who have influenced
the way we view meristems, and to describe their approaches
and contributions to current understanding of the shoot
apical meristem. We have had to be somewhat selective in our
treatment of the topic; for comprehensive reviews of various
aspects of the shoot apical meristem readers are referred to
Adler et al. (1997), Jean (1994) and Lyndon (1994, 1998).
II. How things began
In 1759, in his mid 20s, at a time when the microscope
was still relatively underdeveloped and plant anatomy was
failing to command great attention, Caspar Wolff published
Fig. 2 The punctum vegetationis. Diagram by Caspar Wolff ( Wolff,
1896), which he described as follows, ‘The tip was peeled and all
leaves were removed from the front view, so that it is possible to see
the vegetation point. Leaves were not removed from the back to
demonstrate their attachment to the vegetation surface. (v) The
convex, juicy and translucent vegetation surface. (p) The first leaf to
appear, with its concave inner surface adjacent to the vegetation
surface. The consistency of this leaf is barely more substantial than a
viscous fluid. (a) A different leaf, which is larger and more substantial
than the previous. (c) A leaf which has already developed a
surrounding edge. (e) Half a leaf. (d) Complete leaf.’
‘Theoria Generationis’ (Wolff, 1896). The work had little
influence then and for some time afterwards; its later revival,
according to Sachs, resulted from Wolff ’s thoughtfulness
rather than his accuracy (Sachs, 1890). The observations
led Goebel to declare Wolff the ‘true founder of the history
of development’ (Goebel, 1926). For it was Wolff who
discovered the growing point of the plant, the ‘punctum
vegetationis’ as he named it (Fig. 2). Here, he claimed, was
evidence that growth of the plant proceeded by a process of
epigenesis, that is, construction de novo, and not by
‘preformation’, whereby the mature plant resulted simply
from the unfolding of preformed structures. He recognized
too that leaf and flower primordia were derived by similar
processes leading to the suggestion, many years before it was
made by Goethe, that floral organs were modified leaves
(Singer, 1931).
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That Wolff made this proposal, we can surmise, was the
result of a combination of factors: he had a question he
wanted answered (epigenesis vs preformation), patience and
observational skill, and suitable equipment (the microscope).
In this way the most essential of plant structures was revealed,
Review
together with its mode of action (epigenesis) and, by implication, the ‘open’ form of development of plants in contrast
to the ‘closed’ development of animals. The punctum vegetationis
did not, however, become a clear focus of research at once.
Thus in 1842, Schleiden could suggest, presumably with a
sense of originality, that the study of ‘developmental history’
as opposed to complete structures, might be the key to
morphology (Goebel, 1926). The approach to phyllotaxis
further illustrates this reluctance to view plants as dynamic
entities. Despite dating back to the time of Pliny, morphological explanations of phyllotaxis that involved the apex and
primordia were not put forward until the 1860s at the earliest
(Adler et al., 1997). Before this time studies were made of
the mature, complete leaf arrangement. Transverse sections
through the shoot apical meristem to reveal the organization
of the primordia were an innovation of the early 20th century
(see Church, below).
III. Cytology
The term ‘meristem’ appears not to have entered botanical
vocabulary until 1858. It is attributed to Nageli who in his
work ‘Beitrage zur wissenschaftichen Botanik’ classified
tissues as ‘generating’ or ‘permanent’, according to their
morphology. Parenchymatous generating tissue was termed
‘primary meristem’ (Sachs, 1890). The application of this
term implies a recognition of function because ‘meristem’ is
from the Greek word ‘merizein’, meaning ‘to divide’. The
early published views of the shoot apical meristem were
largely observational, aiming to give accurate descriptions of
meristems under natural, nonexperimental conditions (Sifton,
1944).
Nageli’s work centred on the apical cell, which he found in
algae and moss, and its power to divide continuously. At the
time it was assumed that this large, dividing cell was a feature
of all plants, and Nageli believed that the sequence of cell divisions was of great importance in determining the form of the
plant (Reed, 1942). Whilst the apical cell concept remains
important today in the study of bryophytes and pteridophytes, in 1868 Hanstein redirected attention to cell layers,
Fig. 3 Cytological approaches to the shoot apical meristem.
(a) Hanstein: histogenic layers. ep, epidermis; ec, subepidermis; cc,
central core; d, dermatogen initial layer; pe, periblem initial layer; pl,
plerome initial layer. (b) Schmidt: tunica-corpus. t, tunica; c, corpus.
(c) Foster: cytohistological zones. zia, apical initial zone; cmc, central
mother cells; zp, peripheral zone; mc, central meristem (rib zone).
(d) Buvat: méristème d’attente. mm, méristème médullaire; ma,
méristème d’attente; pmsp, proméristème sporogène; pmr,
proméristème réceptaculaire. (e) Comparison of terminology.
Composed from Majumdar (1942) and Buvat (1952). Diagrams
reprinted from Annales des Sciences Naturelles (Botanique) 8: Buvat,
Structure, évolution et fonctionnement du méristème apical de
quelques dicotylédons. pp. 199 –300, copyright (1952), with
permission from Masson, Paris.
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with his histogenic layer theory of the shoot apical meristem
(Fig. 3a,e). On the basis of cell layers he found and studied in
angiosperms, Hanstein divided the meristem into dermatogen,
periblem and plerome, from which layer initials were derived
the epidermis, cortex and stele, respectively (Foster, 1939; Reed,
1942). In Hanstein’s thinking there is an implicit idea of ‘destiny’,
certain cells being predetermined to differentiate in a manner
commensurate with their layer. Echoes of these ‘prospective
values’ (Foster, 1939) can be seen in later clonal analysis of
cell layer behaviour. Satina’s colchicine-induced chimeras of
Datura (Satina et al., 1940) provided evidence supporting
Hanstein’s histogen concept, but some redefinition was required
(see Fig. 4a,b,c). In his work on cranberry chimeras however,
Dermen (1947) found that there was no reason to support
these inherent functions of the cell layers (Fig. 4d,e).
Schmidt in 1924 followed a somewhat different approach.
Based purely on patterns of growth and cell division, his
model defined the overlying tunica layer(s) by their anticlinal
divisions, with more variable division planes found in the
corpus below (Fig. 3b; Foster, 1939; Steeves & Sussex, 1989).
Dermen (1947) considered that the tunica-corpus essentially
lacked meaning but Sifton (1944) believed that adherents of
the tunica-corpus theory were liberated from the limitations
that consideration of destiny imposed.
In 1938 Foster made a much broader application of cell
division analysis (Foster, 1938). Like Schmidt’s tunica-corpus
layers, Foster’s was a largely structural model, but it was more
extensive, dividing the meristem into cytohistological zones
(apical initial zone, central mother cell zone, transition,
peripheral and rib zones) (Fig. 3c). This recognized the array
of cellular features that Foster found. Foster used a gymnosperm, Gingko, for this original work, but the concept was
found to be applicable to angiosperms (Majumdar, 1942).
Clowes (1961) criticized the imprecision of zonation models
Fig. 4 Chimeras. (a) (b) and (c) Colchicine-induced periclinal chimeras of Datura. Below each diagram the chromosome number of the cell layers
is given. Each layer had an independent response to colchicine treatment. The authors recognized a 2-layered tunica, plus corpus. The 3 germ
layers proposed by Hanstein were evident, but the constancy of chromosome number of layer 3 and the central core implied that ‘plerome’ in
Datura is not an independent tissue but a derivative of L3. Reprinted from American Journal of Botany, 27: Satina et al. Demonstration of the
three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras. pp. 895–905, copyright (1940), with
permission from the Botanical Society of America. (d) Longitudinal section through the shoot apical meristem of a cranberry chimera. The first
3 layers, at least, are diploid and the inner layers, tetraploid. (e) Transverse section of the stem of the plant shown in D. The dark black line
marks the boundary between the inner tetraploid area and outer diploid zone. Reprinted from American Journal of Botany, 34: Dermen,
Periclinal cytochimeras and histogenesis in cranberry. pp. 32–34, copyright (1947), with permission from the Botanical Society of America.
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saying, ‘… it depends so much on the pattern which catches
the eye, and the pattern is made of many different visual
impressions’. Yet the terms derived from Foster’s work –
central zone (CZ), peripheral zone (PZ) and rib zone (RZ), are
now in regular usage as locational reference points in the
meristem. What is the basis of that revival today? Clark (1996)
suggests that you could ‘superimpose’ these regions with those
of the central undifferentiated cell pool and its surrounding
cells heading for differentiation and organ formation. Hence,
although Clark admits to a lack of evidence for this interpretation, a functional significance fortifies a histological model.
Furthermore, it takes on a molecular significance with the
suggestion that the genes WUSCHEL (WUS) CLAVATA
(CLV), SHOOTMERISTEMLESS (STM) are involved in
delimiting/maintaining the CZ and PZ regions (see Developmental genetics, below; Clark, 1996; Weigel & Clark, 1996).
With the exception of Hanstein, concepts of the shoot apical meristem based on cell division patterns were until the
1940s generally structurally based. Few attempts were made
to ascertain the functional significance of cell division rates or
patterns. This makes the méristème d’attente theory of Buvat
(1952) something of a turning point. To Buvat, the infrequency of cell divisions in the central region of the meristem
was of great significance. It was this area he named the
méristème d’attente, a zone of cells he envisaged waiting, inactively, until the initiation of floral activity (Fig. 3d,e; Buvat,
1952; Steeves & Sussex, 1989). Until flowering, the focus of
vegetative development of the plant was the peripheral region,
the ‘anneau initial’.
In arriving at this model, Buvat defined the ‘French School’
(Fig. 5; Wardlaw, 1957; Cutter, 1959). The theories of
Majumdar (1942) and Plantefol (1946) were acknowledged
by the attention given to the peripheral regions of the meristem. Majumdar had seen the apex as a ‘self-perpetuating
group of central initial cells, surrounded by a cylinder of more
active flank meristem from which the primordia originate’
(Majumdar, 1942). This idea was reinforced in Plantefol’s
phyllotaxis theory (see Morphology below) in which leaves
Fig. 5 The French School.
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arise from the ‘anneau initial’ incorporated into Buvat’s
theory. There would appear also to be some influence of
Grègoire’s ‘radical viewpoint’ (Foster, 1939) which strayed far
from the classical interpretation of the flower, by suggesting
that vegetative and floral meristems bore no relation to each
other. To Grègoire, whilst tunica and corpus were recognizable in vegetative meristems, the floral meristem was defined as
a ‘manchon meristematique’, a cloak or mantle of meristematic tissue overlying the ‘massif parenchymateux’, a region of
highly vacuolated infrequently dividing cells (Foster, 1939;
Philipson, 1949; Buvat, 1952). This perception of the floral
meristem as independent, rather than a derivative of the vegetative meristem, is reflected in Buvat’s delimitation of vegetative and floral zones in the meristem.
Beyond the French School, criticized by Wardlaw (1957)
for observations ‘somewhat selective in character’, the
méristème d’attente theory was a view not shared by many.
Nevertheless, the theory did galvanise enquiry into cell behaviour in the meristem. This was in spite of differences of interpretation and crucially, the limited evidence for the inactivity
required of the waiting cells in the meristem summit (Wardlaw,
1957; Cutter, 1959; Steeves & Sussex, 1989).
IV. Morphology
Morphological approaches to the shoot apical meristem are
essentially concerned with how and where the meristem
establishes growth. Featuring strongly in this aspect of shoot
apical meristem research were the Snows who recognized that
models of phyllotaxis until that time (1931) fell into two
groups – those that proposed pattern to be determined by an
unknown property of the stem itself, and those that advocated
leaf arrangement to be dictated by contact with existing
primordia. The Snows set about testing the validity of the
models – assuming that if those in the second group were
correct, manipulating primordia as they arose could influence
the positions of those that formed later. Where others had
observed and calculated (for review see Schwabe, 1984), the
Snows became experimentally involved using a ‘cataract knife’
and a dissecting microscope to perform microsurgery on the
shoot apical meristem. The Snows observed that, under certain
circumstances isolating a primordium or its site caused the
phyllotactic spiral to be reversed with a primordium and its
successors forming at opposite sides to those expected, had
normal phyllotaxy been retained (Fig. 6a,b). This led the
Snows to propose a concept of ‘first available space.’ Existing
primordia determined where a new primordium formed –
and this was in the widest gap, furthest from the growing apex
(Snow & Snow, 1931).
The Snows also pioneered the study of how a leaf forms.
They found that application of auxin to the shoot apical meristem of Lupinus albus and Epilobium hirsutum gave rise to
enlarged, united primordia in an altered arrangement and
interpreted these results to support their model of phyllotaxis
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Fig. 6 The Snows and Wardlaw – first available space/inhibitory fields. (a) and (b) Diagrams of transverse sections of the shoot meristem of
Lupinus albus from Snow & Snow (1931). The straight line across (a), a normal bud, marks the position of the incision made to isolate the area
of tissue (I1 region), about to initiate the next primordium. The phyllotactic alteration that this causes is shown in (b). Note the different positions
of I4 and I5 after incision (b). P1, P2, P3, etc. = existing primordia, in order of increasing age. I1, I2, etc. = incipient primordia, invisible at the
time of operation, in order of appearance. Reprinted from Philosophical Transactions of the Royal Society, London, Series B 221: Snow M, Snow
R. Experiments on phyllotaxis. I. The effect of isolating a primordium. pp. 1 – 43, copyright (1931), with permission from The Royal Society. (c) and
(d) Representations of the shoot apex of Dryopteris showing, in (c), the position of leaf primordia and incipient primordia, and in (d), the possible
‘fields’ associated with these ‘growth centres’. ac, apical cell; b, bud rudiments; m-m1, lower limits of apical meristem. The dashed line indicates the
approximate base of the apical cone. I1, I2, etc., as above. Numbers = existing primordia (increasing age). Reprinted from Growth (supplement)
13: Wardlaw, Experiments on organogenesis in ferns. pp. 93–131, copyright (1949), with permission from Growth Publishing Co. Inc.
(Snow & Snow, 1937). To an extent this work foreshadows
contemporary morphological approaches (see below).
The 1940s brought two influential models of phyllotaxis.
The first was Plantefol’s ‘multiple foliar helices’ model which
is rarely considered now but was a very significant feature of
the French School (Fig. 7; Wardlaw, 1957; Cutter, 1959). In
this model, leaves were arranged in helices of variable numbers
depending on the plant. Helices terminated in leaf-generating
centres in the anneau initial and these were under the control
of an organizer (Plantefol, 1946; Cutter, 1959). This theory
has not gained wide acceptance because it is not clear how to
determine which foliar helices have most ‘biological reality.’
Neither has it been given rigorous mathematical testing.
In the second of the post-Snow models, we return to their
surgical approach, the knife this time wielded by Wardlaw. He
favoured the large meristems and widely spaced primordia of
the fern Dryopteris, and using a similar technique arrived at
similar results to those of the Snows. He did not reject the
Snows’ ‘first available space’ hypothesis but instead set about
interpreting ‘space’ along the lines of Schoute in 1913, drawing
inhibitory fields across the meristem (Fig. 6c,d). Wardlaw
argued that space itself does not ‘do’ anything and is not a
‘causal factor’ in morphogenesis. A new primordium emerged
at the position of weakest inhibition with the most recently
formed primordium the inhibitor source (Wardlaw, 1949).
The view that phyllotactic patterns can be explained by inhibitory fields is an enduring one.
Richards (1951) sought a phyllotactic description that
completely defined the arrangement of leaves and, most significantly, was independent of any theory of the origin of
phyllotactic pattern. He achieved this using the divergence
angle and the plastochron ratio (the radial distances of successively initiated primordia from the centre of the system).
Richards clearly saw the importance (and limitations) of treatments by Schimper and Braun more than 100 years earlier, in
which phyllotaxis was partly defined by the divergence between
two successive leaves in a tangential direction; Church’s classification by pairs of orthogonally intersecting contact
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shoot apical meristem. He wanted to explain the origin of pattern as well as its further propagation (Green et al., 1996), and
he recognized that initiation and patterning mechanisms were
not necessarily divorced from each other (Green, 1992). Perhaps most significantly, Green suggested that concepts of pattern formation need not be anticipatory (i.e. that no regional
differences need precede and direct development), a contrasting view to that which predominates in developmental genetics today. Whilst Meyerowitz has advocated that ‘global
patterning’ arises out of the coordination of local control
mechanisms (Meyerowitz, 1996), Green considered this
approach to be anticipatory and favoured a view of development which was reflective of global pattern; so for example, in
some cases, ‘a tissue-level physical process appears to be
upstream of organ-specific expression’ (Green, 1997).
Green proposed a biophysical solution to shoot apical meristem pattern formation, similar to that which gives ‘wrinkles
in wet skin’ (Hernandez & Green, 1993); this was the physical
buckling theory. Patterning in this model arose from instability, in turn arising from the ‘need to expand’ of a uniform
sheet tied to a uniform underlying layer which gave upward
pressure. These attributes were provided by the tunica and
corpus of the meristem (Fig. 8). To redress this unbalanced
state, physical buckling would occur and generate bulges on
the meristem surface (Green, 1992; Hernandez & Green,
Fig. 7 Plantefol: multiple foliar helices. (a) Stem of Lilium candidum
showing three foliar helices. (b) The classical view of leaf generation
and the multiple foliar helices model for a stem with three foliar helices.
Reprinted from Annales des Sciences Naturelles (Botanique) 7:
Plantefol, Fondements d’une théorie phyllotaxique nouvelle.
pp. 1–77, copyright (1946), with permission from Masson,
Paris.
parastichies (Church, 1904, 1920); and van Iterson’s studies
of packing of spheres on cylinders.
Although Richards’ treatment of phyllotaxis did not
depend on any particular mechanism, it was consistent with
the inhibitor theory adopted by Wardlaw. Later mathematical
models simulating the growing shoot apex by, for example,
Thornley (1975a,b), and Veen & Lindenmayer (1977) used
the idea that primordia (and the bare apex) are sources of an
inhibitor of primordium initiation (see Schwabe, 1984; Jean,
1994 for reviews).
These models tend to be concerned with the mechanism by
which the shoot apical meristem continues to function. A
more contemporary morphologist, Green, was, however, not
so concerned with maintenance of existing pattern at the
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Fig. 8 Green: undulations. (a) Wild-type floral meristem of
Antirrhinum. Stamens arising in whorl 3. (b) Floral meristem of a
deficiens mutant of Antirrhinum, which makes sepals in the first two
whorls of the flower, followed by carpels. (c) and (d) Mechanical
simulations of undulations in a fixed circular region. It is proposed that
in the meristem, undulations depend on the ratio of corpus (flexible)
to tunica (rigid). A shift from out-of-plane undulations, giving
stamens, to in-plane undulations will give rise to carpels, mimicking
the effects of the deficiens mutant. s, sepals; p, petals; st, stamens;
c, carpels. Reprinted from American Journal of Botany 86: Green,
Expression of pattern in plants: combining molecular and calculusbased biophysical paradigms. pp.1059–1076, copyright (1999), with
permission from the Botanical Society of America.
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1993; Green et al., 1996). These bumps could then provide a
new set of physical parameters for continued buckling to
propagate pattern (Green, 1992). A nice example of the process of leaf initiation and the subsequent organization of a
shoot apical meristem is provided by the work of Selker &
Lyndon (1996) with axillary explants of watercress (Nasturtium officinale). Roughly triangular surfaces, showing none of
the characteristic structural organization of a meristem, were
able to initiate new buds. The phyllotactic pattern of these
explant buds was sometimes different to that of the parent
plant. The authors interpret their observations as showing
that the pattern is related to the shape of the bud-forming
space and mechanical stresses within it (Selker & Lyndon,
1996; Lyndon, 1998).
Green perceived that in the shoot apical meristem pattern
was generated from ‘nothing’ (Hernandez & Green, 1993)
and he saw this model as preferable to the more commonly
applied positional information and reaction-diffusion genre,
both of which require an anticipatory prepattern for which he
found very little evidence (Green, 1992; Hernandez & Green,
1993). Nor under the physical buckling mechanism was there
a need for inhibitory fields to account for phyllotaxis. Green
suggested that there was no reason to believe that organ initiation would be spontaneous unless inhibited (Green, 1992).
In Green’s model ‘inhibition’ derives from the ‘intrinsic reluctance’ of the surface to undergo a sharp change in shape
(Green et al., 1996).
To a degree Green’s work was carried out on inanimate
models, simulations which gave phenocopies of plant
mutants and fused organs (Green, 1996). Applying the principles in vivo, growing sunflower heads in constraints resulted
not only in predictable alterations in pattern but also in
altered organ identity (Hernandez & Green, 1993). Green
interpreted this as ‘abnormal buckling’, that is, a physical
process having an influence on gene expression (Hernandez &
Green, 1993; Green, 1994).
Overall, Green’s approach to meristems was strikingly original; this is apparent not least in the vocabulary he used to
describe them. He placed emphasis on shape and form, writing of ‘tissue undulations’, ‘an initial bump pattern’ which is
‘roughly sinusoidal’ and primordia ‘delimited by parallel creases
of equivalent clarity and depth’ (Hernandez & Green, 1993).
Green’s work spanned a time when morphology was, to some
extent, giving way to the emerging field of developmental
genetics. Perhaps partly because of this, his work on pattern
initiation was founded on almost uniquely held principles.
Modern-day morphologists have much in common with
the Snows in attempting to discover the workings of the shoot
apical meristem through its manipulation. Reinhardt applied
a similar technique to the Snows – the application of synthetic
indole-3-acetic acid (IAA), but in combination with plant
material in which auxin transport had been inhibited, chemically (with N-1-naphthylphthalamic acid (NPA) in tomato
shoot apical meristems) or genetically (the pin-formed 1-1
(pin1-1) mutant of Arabidopsis) (Reinhardt et al., 2000).
Tomato shoot apical meristems on NPA media failed to produce leaves, but leaf initiation could be restored by auxin.
Similarly auxin application recovered flower formation in
pin 1-1 mutants. The finding that leaves always appeared at
the precise point of auxin application in the radial axis of
the shoot apical meristem but at a constant distance from the
meristem tip led Reinhardt to propose a model of shoot apical
meristem function in which the apical-basal axis, Foster’s CZ/
PZ, is maintained by genes such as CLV, WUS, STM (see
Developmental Genetics, below) but that radial patterning is
auxin dependent. Organogenesis of leaves and flowers requires
auxin, and, in line with the Snows, correct positioning of
leaves (but not their initiation) requires existing primordia
(Reinhardt et al., 2000; Kuhlemeier & Reinhardt, 2001).
Recently a more comprehensive model, linking transcription
factors, hormones and primordium outgrowth has been elaborated. A new leaf differentiates where there is gibberellin and
a high concentration of auxin. These conditions arise through an
auxin gradient in the meristem with existing primordia acting
as auxin sinks. Gibberellin levels are affected when homeodomain transcription factors such as KNAT1 and STM, which
normally inhibit gibberellin biosynthesis are down-regulated.
In this way transcription factors can regulate meristematic cells
through growth hormones (Vogler & Kuhlemeier, 2003).
At a biophysical level, expansins are proposed to operate in
cell wall expansion during cell extension. Reinhardt suggested
that genes such as the tomato expansin LeEXP18 could be
activated to induce bulging of the meristem in the final element of a phyllotactic mechanism (Reinhardt et al., 1998).
This role of expansin in leaf development is supported by the
work of Fleming et al. (1997) and Pien et al. (2001). In both
cases expansin in localized areas induced leaf primordia and
reversed phyllotaxis. Pien et al. suggested that this was ‘evidence of cell-division independent mechanisms controlling
morphogenesis’ (Pien et al., 2001).
V. Developmental genetics
Although there is little to suggest that cytological and
morphological considerations of the shoot apical meristem are
now implausible, the developmental genetics era of the last
15 years is largely independent and disconnected from these
earlier phases – phases which may now sometimes appear
irrelevant. Models are a significant component of this research
phase, being typically the end result and the starting point for
further work. In the current climate of genetic determinism
there is a sense that, in molecular biology, we have the answer;
that this is the time when we will define the root causes of
meristem functions.
The molecular models do, however, elaborate on earlier
structural models, being particularly concerned with the balance between self-perpetuating and differentiating cells that
underlies meristem maintenance. Attention is also given to
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how meristems form, initiate the organs characteristic of
vegetative or floral phases, and terminate.
Barton has considered the origin of leaves and of the shoot
apical meristem itself. These are processes that require tissue
differentiation, to distinguish the shoot apical meristem from
other embryonic tissues, and, later to define leaf founder cells
from amongst the undifferentiated cells of the shoot apical
meristem. Barton’s research addresses patterning arising in the
embryo and ‘genetic circuitry that distinguishes meristem
from leaf ’ (Barton, 2001). She has studied these differentiations using the homeodomain transcription factor STM in
Arabidopsis. stm mutants fail to make a functional shoot apical
meristem. The gene is expressed in the late globular stage of
the embryo and then in the shoot apical meristem throughout
the life of the plant, suggesting a role in the formation and
maintenance of the meristem. STM is down-regulated in cells
destined to become leaves (Long et al., 1996), although this is
not the first sign of leaf identity as the expression of PINHEAD/ZWILLE (PNH) precedes the down-regulation of
STM (Lynn et al., 1999). Barton revived an earlier term,
‘promeristem’ to encompass the initials and their recent undifferentiated derivatives in the shoot apical meristem (Barton,
1998). STM and PNH are effectively markers for the outcome
of decisions facing promeristem cells – to continue in a meristematic role or to become leaf.
Barton proposes a model of cyclic action. In this model the
shoot apical meristem initiates leaves, then the adaxial side of
these leaves induces shoot apical meristem formation in the
leaf axil – so shoot apical meristems make leaves of which make
meristems (McConnell & Barton, 1998). In arriving at this model,
Barton considered the correlation that exists between adaxial
leaf tissue and the formation of meristems. This relationship
is seen in phabulosa mutants of Arabidopsis, in which leaves are
adaxialized, in overexpression studies with the maize homeodomain KNOX transcription factors and also in earlier work
by the Snows, in which surgery resulting in leaf abaxialization
was accompanied by a loss of axillary meristems. A significant
concern of this model is whether shoot meristem tissue arises
only once, as the original embryonic assignment, or many
times over in the life of the plant. Does the new axillary meristem arising in association with the adaxial side of the leaf
derive from ‘detached meristem’, that is, a few meristematic
cells that remain undifferentiated? Or is it possible for cells to
differentiate but then to respond to a localized signal that
re-establishes their meristematic properties? (McConnell &
Barton, 1998).
These considerations of the distinction between the leaf
and the meristem are reminiscent of the thoughts of Arber
(1950). Arber observed the self-similarity of the system: ‘each
branch shoot echoes the character of the parent shoot’ and
consolidated the earlier botanical interpretations on this
theme in her view of the leaf as a ‘partial-shoot’, adding that
‘the partial-shoot has an urge towards the development of
whole shoot characters’ (Arber, 1950).
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Laux and Clark have focused on how the meristem sustains
its two main functions, providing cells to an undifferentiated
pool, and differentiating cells into organs. Laux primarily
considers the Arabidopsis homeodomain transcription factor,
WUS (Mayer et al., 1998) and Clark investigates the role of
the signal transduction pathway encoded by the CLAVATA
genes. CLAVATA1 encodes a receptor kinase, CLAVATA2 a
receptor-like protein and CLAVATA3 a peptide ligand (Clark
et al., 1997; Jeong et al., 1999; Trotochaud et al., 2000). The
involvement of these genes in meristem maintenance can be
inferred from their mutant phenotypes. The meristems of wus
mutants terminate prematurely (Laux et al., 1996), whilst
those of clavata mutants proliferate (Clark et al., 1993,
reviewed in Clark, 1996). The model of meristem function
which emerges from mutant, expression and overexpression
analyses uses the CZ/PZ terminology of Foster to provide grid
references, within which gene expression patterns and cell
functions can be defined (Fig. 9). Laux’s group picture the
meristem as including an organizing centre defined by WUS
expression. This organizing centre lets overlying cells know
that they are stem cells by inducing CLV3 expression, which
maintains the cells in an undifferentiated state. To become
organs, cells need to be beyond the range of WUS, thus losing
their stem cell identity and becoming available to be assigned
organ fate (Schoof et al., 2000). Although WUS induces
CLV3 expression, CLV3 is secreted from the outer layers to the
lower layers of the meristem where the CLV1 and 2 genes are
responsible for curtailing the expression of WUS. It is this
WUS –CLV negative feedback interaction which is proposed
to maintain the balance of cells in the meristem (Schoof et al.,
2000).
Revealingly, Laux’s group have expressed WUS under the
control of the promoter of the AINTEGUMENTA (ANT )
gene, thereby directing its expression to organ primordia. The
resulting misexpression of WUS extends CLV3 induction
and undifferentiated cell fate to a tissue at an early stage
Fig. 9 The molecular basis of shoot apical meristem maintenance.
WUS expression in a subset of cells in the central region of the
meristem establishes an ‘organizing centre’ and activates CLV3
expression in the overlying outer cell layers of the meristem. CLV3
negatively regulates the expression of WUS via its interaction with
CLV1. These interactions between WUS and the CLV genes, regulate
the proliferation of stem cells in the meristem. STM is expressed
throughout the meristem where it represses cell differentiation. It is
down-regulated in organ primordia (see text for details). CZ, central
zone; PZ, peripheral zone.
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of differentiation (Schoof et al., 2000). Thus, WUS can apparently
respecify relatively undifferentiated tissue, such as organ primordia, and initiate stem cell identity there. More differentiated cells, however, require the action of both STM and WUS
to reverse their fate (Lenhard et al., 2002). These genes appear
to function independently, regulating different downstream
targets. Their common task is to prevent differentiation,
either through its suppression (STM) or by the specification
of stem cells (WUS). Lenhard et al. (2002) found that coexpression of STM and WUS led to an extension of small CLV3expressing cells from the apex onto the lamina of cotyledons.
Gallois et al. (2002) induced WUS expressing sectors in seedlings and independently activated STM, with the result that
outgrowths occurred from both abaxial and adaxial sides of
the cotyledons. These outgrowths expressed CLV1 transiently
but then developed as leaf-like organs, suggesting that they
had a meristem-like phase but ultimately were not selfmaintaining structures. Thus, the details of WUS / CLV/STM
action still need to be worked out, particularly when the
genes are expressed in pre-existing tissues in different stages of
differentiation.
In the era of developmental genetics the key question of
how leaf primordia are positioned has received relatively little
attention. Hake has described two mutants of maize which
provide possible support for Wardlaw’s inhibitory field model.
In the terminal ear 1 (te1) mutant alternate phyllotaxis is disrupted to an irregularly opposite or spiral arrangement (Veit
et al., 1998); in the abphyl1 mutant it becomes decussate
(Jackson & Hake, 1999). The expression of TE1, a putative
RNA-binding protein, was found in ‘horseshoe’ formations
alternating from side to side around the stem. New leaf primordia arose at the discontinuity of expression, leading Veit
et al. to suggest that TE1 inhibited cells from ‘acting as organizers of leaf development’ and Scanlon to wonder whether
TE1 might ‘divulge the first molecular evidence for the inhibitory field theory of plant phyllotaxy’ (Scanlon, 1998). Crucial to the interpretation of abphyl1 is the observation of the
enlargement of the embryonic shoot apical meristem, and
that the novel phyllotactic pattern is established in the
embryo. This implies that, depending on the precise timing of
leaf position determination, phyllotactic patterning may follow the change in meristem size and not vice-versa ( Jackson &
Hake, 1999), a finding consistent with the model proposed by
Richards (1951). Jackson and Hake envisage that the enlarged
meristem affects fields – all inhibitory – but either chemical or
biophysical.
Up to this point we have considered how differentiated and
undifferentiated tissues of the meristem are specified and
maintained. This is a constant underlying feature of the meristem, even when alterations to meristem function occur in
accordance with the growth phase of the plant. Mechanisms
that elaborate on this basic pattern during the floral phase
have been the subject of many models, which will now be
considered.
Coen’s view of the shoot apical meristem is unitary (i.e. the
meristem is divisible into a set of simple, self-contained
regions and functions), reductionist and highly conceptualized. He suggests that meristems have an ‘identity’ – vegetative, inflorescence or floral. This identity is controlled by
‘meristem identity genes’ and can be described and classified
in terms of four main features, phyllotaxy, organ identity,
determinacy and internode length (Coen, 1991; Coen &
Carpenter, 1993). Consequently, in interpreting the floricaula
( flo) mutant of Antirrhinum majus, Coen proposes that the
loss of FLO gene expression results in a failure of the transition
of the meristem from inflorescence to floral identity (Fig. 10a;
Coen et al., 1990). Hence FLO is a meristem identity gene
orchestrating a switch in the crucial meristem properties that
compose ‘identity’.
The conceptual nature of this picture is illustrated by the
work of Huala & Sussex (1993). Drawing largely on predevelopmental genetics work, they described cases in which
meristems may be considered determined but their derivatives
may not. For example, a maize meristem may be reproductively
determined yet still initiate primordia which develop as vegetative shoots (Huala & Sussex, 1993). In such cases assessment of meristem identity must rely on characteristics of
phyllotaxy, determinacy and internode length (Huala &
Sussex, 1993).
Fig. 10 Coen: FLORICAULA and partitioning. (a) Longitudinal
section of an inflorescence of Antirrhinum majus, viewed in
dark field. The section shows FLO expression in the meristem
detected using in situ hybridization with digoxigenin-labelled probes
(1990). Reprinted from Cell 63, Coen et al. FLORICAULA: a
homeotic gene required for flower development in Antirrhinum
majus. pp. 1311–1322, copyright (1990), with permission from
Elsevier. (b) Top view of a wild type meristem of Antirrhinum
majus, showing a regular initiation pattern of discrete primordia.
The outline of a double helix is marked. (c) flo mutant of Antirrhinum
majus lacking discrete primordia. Reprinted from Plant Cell 7,
Carpenter et al. Control of flower development and phyllotaxy by
meristem identity genes in Antirrhinum. pp. 2001–11, copyright
(1995), with permission from the American Society of Plant
Biologists.
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For Coen a unifying factor underlying a number of these
meristem properties is the idea of partitioning. Cells become
partitioned off from the shoot apical meristem to become
organ primordia or secondary meristems, and which of these
two types of partitioning is favoured dictates determinacy.
Conforming to a phyllotactic arrangement requires a precise
pattern of partitioning (Coen & Carpenter, 1993). This concept was elaborated further in one of the first molecular
approaches to phyllotaxis: the analysis of phyllotaxis of the
meristem identity gene mutants of FLORICAULA (FLO) and
SQUAMOSA (SQUA) (Carpenter et al., 1995). In both
mutants phyllotaxis is altered from that of the wild type,
implicating FLO and SQUA in promoting the transition from
spiral to whorled phyllotaxis. This change is considered to be
controlled by these genes in a two-stage process. Areas of the
meristem are set aside for ‘potential primordium initiation’ in
stage 1, and then partitioning of these areas in stage 2 results
in primordia. Rarely, in flo mutants, this second stage fails and
plants form double spirals, which led Carpenter et al. to question whether the primary initiation state is of discrete primordia (which unite in flo mutants) or of spirals which require
partitioning. This second proposal is recognized as identifying
with the ideas of Plantefol (Fig. 10b,c).
Coen proposes that the nature of the organs which a meristem of floral identity initiates is controlled by ‘organ identity
genes’ (Coen & Carpenter, 1993). The model of organ identity gene action, the ABC model, devised by Coen and Meyerowitz (1991, see below) is a current, highly influential
concept of flower development. Coen’s interest in this area
arose from a PhD on Drosophila, during which he became
interested in studying development and evolution from
genetic and molecular perspectives (Coen, 1996). By analyzing
Antirrhinum flower structure mutants, Coen began to construct a genetic model, with first two (independent), then
three gene functions to explain flower structure (Carpenter &
Coen, 1990; Coen, 1991). The resulting ABC model proposes
that organ identity genes operating in three overlapping
domains, A, B and C control the identity of organs in the
flower. a function expressed alone in whorl 1 gives rise to
sepals; a and b in whorl 2 to petals; b and c in whorl 3 to stamens; c in whorl 4 to carpels. a and c are antagonistic and cannot be expressed in the same domain (Fig. 11a,b; Coen &
Meyerowitz, 1991; Coen, 1991; Coen & Carpenter, 1993).
For Huala & Sussex (1993), floral homeotic mutants demonstrate that determination of the floral meristem and its primordia are separable events (see above). It is also evident that,
whilst mutation of organ identity genes alters identity, other
floral properties (e.g. phyllotaxy, lack of internodes) persist.
This narrow role for organ identity genes was apparent to
Lord, who proposed the importance of relative timing in meristem functions, and emphasized the heterochronic as well as
homeotic nature of floral mutants. One of the conclusions of
her work was that whilst organ identity was altered, the characteristic cell division patterns that gave rise to the primordia
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Fig. 11 Coen and Meyerowitz: the ABC model. (a) The ABC model
of floral organ identity. In this diagrammatic representation the
whorls of the flower are shown as concentric rings. Superimposed on
this are the domains A, B and C. See text for details. Redrawn from
Coen & Meyerowitz (1991). How this is proposed to translate to the
meristem is shown in (b), a diagram of the meristem in longitudinal
section, showing patterns of ABC expression in present or
presumptive whorls 1–4. Reprinted from Plant Cell 5, Coen and
Carpenter, The metamorphosis of flowers. pp. 1175–1181, copyright
(1993), with permission from the American Society of Plant
Biologists.
in each whorl remained as wild type (Lord et al., 1994; Hill &
Lord, 1989; Crone & Lord, 1994). Weigel has also considered
the mechanisms which underlie the correct positions of ABC
expression patterns, concluding that meristems have patterning systems common to vegetative and floral meristems,
which involve the genes UNUSUAL FLORAL ORGANS and
WUSCHEL (Parcy et al., 1998; Lohmann et al., 2001).
Coen introduced a second dimension to complete the
‘polar coordinate model’ for the control of primordium fate
(Coen, 1991). As well as the ‘r’ or radial axis, along which
organ identity varies in the flower, there is the ‘y’ axis. Along
this second axis, the expression of the gene CYCLOIDEA is
proposed to vary – and control the asymmetry (where relevant) of the flower. It achieves this, it is proposed, by slowing
the growth rate and reducing the organ number in the area of
its expression (Luo et al., 1995). According to this model, the
fate of a primordium is the reflection of its coordinates on the
identity (r) and symmetry (y) axes (Coen & Meyerowitz,
1991; Coen, 1991). What is striking about these models of
meristem function is that they rely on the ideas of identity and
symmetry as specific end points to which genetic cascades are
directed.
As Meyerowitz, coproposer of the ABC model, points out,
there are few, if any, reasons why a model of flower development along these lines could not have been arrived at
100 years earlier. Detailed descriptions of monstrous and normal flowers have been made for centuries, but, with some
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exceptions, it was not until the late 1980s that the study of
flower development capitalized on the availability of flower
abnormalities (Meyerowitz et al., 1989; Meyerowitz, 1995).
The aim of these approaches was to ‘understand the flow of
information from the genome that led to the 3-dimensional
structure of the flower’ (Meyerowitz, 1995). For Meyerowitz
this began with the description of recessive homeotic mutants
of Arabidopsis thaliana. He established that the mutations in
question were often flower-specific, the organs developed on
a time course linked to their whorl rather than their identity,
that replacement organs in the mutants were often mosaic in
nature, and there were few constraints on the identity of
organs in any whorl. This last discovery was evidence against
the few earlier mechanistic models there had been, which proposed sequential means of organ specification, and were at
odds with the data on abnormalities (Bowman et al., 1989;
Meyerowitz et al., 1989). Consideration of the mutant phenotypes led Meyerowitz to the proposal that the flower primordium could be ‘divided into fields or compartments, each
consisting of adjacent whorls’ with the genes acting in the
‘delineation of concentric-ring shaped compartments, each
with a different fate’ (Bowman et al., 1989). The preliminary
model proposed three classes of homeotic gene capable of producing a flower, with the leaf as a ‘ground state organ’ (Coen
& Meyerowitz, 1991; Meyerowitz et al., 1991). Later tests of
the model revealed the necessity for a further function, provided by the MADS-box SEPALLATA genes, to convert
leaves to floral organs (Honma & Goto, 2001). Theissen
(2001) considered this grounds to re-evaluate the ‘outmoded
ABC model’, by then amounting to the ABCDE model, questioning whether ‘floral homeotic functions are still a useful
concept at all’ since the concept ‘no longer provides a useful
simplification’ (Theissen, 2001).
In Coen’s opinion, we need now to think of the basis of
primordium fate in genetic terms and consider, ‘how are the
domains of whorl identity genes established?’ (Coen, 1991).
Seen in relation to the cytological and morphological
approaches outlined in earlier sections, this indicates a huge
shift in perspective. The view of the meristem here is abstract,
a recurrent feature of developmental genetics-based meristem
models. What are the relative merits of this direction in meristem research and how have these new ideas come about? The
ABC model is probably the most influential model of meristem function that there has been. It is simple and neat – two
desirable features in any model. It is possible that the ABC
model is so successful because it presents the closest explanation to the biological reality of how a flower forms. Certainly
it is reassuring that, almost independently, and working on
separate systems, Coen and Meyerowitz arrived at similar
models. But it could be argued that this has more to do with
their common perspective than with reality. The massive support found for this model shows that many choose to interpret
their data in the light of it, and that they share the same perspective as Coen and Meyerowitz.
A molecular model is necessarily abstract because, as Coen
has pointed out, what has recently been revealed is ‘how
organisms contain a whole series of regional differences that
were previously hidden from view’ (Coen, 1996). But, whilst
we can perceive the organization of floral organs, and in situ
hybridization allows us to visualize gene expression, in these
models we need to envisage partitioning, domains, ‘molecular
territories’ (Coen, 1996) and boundaries (Vincent et al.,
1995). This can be challenging, although similar demands
have been made in the past. In Wardlaw’s proposal of phyllotactic determinants we had to visualize inhibitory fields radiating from growth centres. Interestingly, both models provide
strong visual images, and it seems legitimate to ask how far
they colour our perceptions. Ask yourself: ‘would I have
thought like this from experience? How much is this a product of my imagination?’ The answer is that the model determines what you see, the questions you can ask; it defines a way
of thought.
How did we start to see plants in such unitary terms? Out
of the beginnings of mutant analyses arose ‘animal-plant’ thought.
Initially this was merely a recognition that the initiative to use
mutants for the study of pattern formation followed a precedent set in animal developmental studies. Drawing from earlier work on Drosophila, Meyerowitz concluded that finding
the genes underlying flower development was the next step
(Meyerowitz et al., 1989). When the first of these genes was
uncovered, the DEFICIENS A (DEF A) gene of Antirrhinum
majus (Sommer et al., 1990), and the functional significance
of its homology to transcription factors was considered, it was
possible to envisage a regulatory network determining morphogenesis at the meristem (Sommer et al., 1990).
It was, however, the report of the second transcription
factor to be cloned, AGAMOUS (AG) from Arabidopsis
(Yanofsky et al., 1990), that seemed to signal a turning point in
perceptions of how the meristem might function. Discovery
that this second gene had extensive homology to the DEF A
gene prompted many thoughts in an animal-plant direction.
The possibility that a family of transcription factors was at the
heart of pattern formation of flowers as well as flies grew ever
more likely. Meyerowitz proposed that we might consider
some sort of ‘floreo’ box, similar to the homeobox of Drosophila homeotic selector genes (Meyerowitz et al., 1991) and
the AG report concluded that, analogous to animal development, floral organ development might be regulated by a set of
closely related genes (Yanofsky et al., 1990). Furthermore,
with DEF and AG MADS box transcription factors (as they
became known, Schwarz-Sommer et al., 1990) from different
plant species, there was the possibility of an evolutionarily
conserved mechanism.
Thus the domains and compartments of meristems in today’s
developmental biology are traceable to concepts of animal
development. From a similarity of approach (analysis of developmental mutants) to a discovery of gene families, we have
reached a similarity of perception and mechanism. Sablowski
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Fig. 12 Meinhardt: segmentation. Schematic longitudinal section of
a plant. M indicates an ‘elementary module’ composed of node (N)
and internode (I), and producing a leaf (L) and bud (B). Each module
is made of at least 3 subunits M1, M2, M3, which ensure polarity.
A, shoot apical meristem; P, primordia. Stem shown, ‘unrolled’ in
2-dimensions. Cells produced by the shoot apical meristem aid stem
elongation and differentiate into subunits. Note leaf initiation on M1,
M2, border. Reprinted from International Journal of Developmental
Biology 40, Meinhardt, Models of biological pattern formation:
common mechanism in plant and animal development. pp. 123–134,
copyright (1996), with permission from the University of the Basque
Country Press.
& Meyerowitz (1998) commented that ‘homeotic mutations
have provided evidence for modularity in the development of
both animals and plants; the identity of discrete body parts
can be transformed by loss of function or ectopic expression
of homeotic genes’. This concept of modularity extends
beyond the meristem consumed with flowering, and also back
to a pre-developmental genetics era when vegetative modules
became known as phytomers.
More recently Meinhardt (1996) has proposed a segmentation model of plant development (Fig. 12). Disappointed in
the inability of morphological spacing models to explain how
leaves develop distinct abaxial and adaxial leaf surfaces with
correct orientation to the shoot apical meristem, Meinhardt
proposed that segments M1, M2 and M3 form a repeating
sequence to construct a vegetative plant. An activator-inhibitor
mechanism is involved in determining the generation of
leaves but, crucially, leaves only form at the junction of segments. The junction position ensures that leaves are composed of two tissue types, M1 and M2 (abaxial-adaxial
surface) and are correctly orientated. Thus the polar character
of the boundary ensures the polar structure of the leaf. Meinhardt sets this model amongst others of biological pattern
formation (tropical sea shells, leg, wing initiation … ) and
proposes a ‘common mechanism’ in plant and animal development. Further endorsements of such analogies come from
the comparisons of leaf and wing development ( Waites &
Hudson, 1995; Scanlon et al., 1996).
The end of the shoot apical meristem is most frequently considered as accompanying flower formation. This determinacy
© New Phytologist (2003) 159: 37 – 52 www.newphytologist.com
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dimension to flowering has been prominent in the thinking of
developmental geneticists and is associated with the C function gene AG (Yanofsky et al., 1990). ag mutants fail to make
the reproductive organs of the flower and produce an indeterminate proliferation of sepals and petals (Bowman et al., 1989),
whilst ectopic AG expression can convert an indeterminate
inflorescence meristem to a determinate floral meristem
(Mizukami & Ma, 1997). The termination of growth associated
with flowering results from an interaction between AG and
WUS (Lenhard et al., 2001; Lohmann et al., 2001). As described
above, WUS is involved in assigning stem cell fate via CLV3. In
conjunction with the meristem identify gene LEAFY it also
up-regulates AG expression but, later in development, AG acts
to repress WUS, thus halting the supply of undifferentiated
cells and preventing further growth. Although the C function
may lie at the heart of meristem determinacy, development
continues after the carpels it specifies. The D function genes
FBP7 and FBP11 evoke ovule and placental column development from the central meristem of Petunia (Angenent &
Colombo, 1996). In some cases determinacy is only incompletely maintained (Fig. 13).
When and where growth termination occurs dictates the
architecture of the plant (Battey, 2003). There are times when
flowering does not stop a meristem (floral reversion), and
other times when meristems cease growth without flowering.
One such example is found in Arabidopsis itself: the induced
apical meristem is an inflorescence meristem, and although
growth at this apical point is indeterminate, it isn’t infinite.
Another example is found in inflorescence meristems of
Bougainvillea, which under long day conditions fail to develop
and become lignified thorns (Hackett & Sachs, 1968). In calabrese,
apical abortion or ‘blindness’, an environmentally induced
disorder, results in cells losing their meristematic ability and
differentiating as parenchyma. The tunica-corpus distinctions
disappear and the meristem stops without death or flowering,
a case of ‘terminal differentiation’ (Forsyth et al., 1999).
VI. Conclusions
Describing the study of botany in the early 1800s, Sachs
observed that, ‘a curious misconception crept in among the
phytotomists at this time; they believed that more correct and
trustworthy figures would be obtained if the observer and
writer did not himself make them, but employed other eyes
and other hands for that purpose; they imagined that in this
way every kind of prejudice, of preconceived opinion would
be eliminated from the drawings’ (Sachs, 1890). Today we
might feel that in an age of photography, sequencing,
imaging, we have machines of objectivity that place us
beyond that problem, yet we still find only what we look for;
what we see depends on how we interpret the information
available. Through recent history the shoot apical meristem
has been a constant but its scientific representation has been
ever-changing. A model of shoot meristem function summarizes
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Fig. 13 An indeterminate flower of Impatiens balsamina. Proliferations of petal-like organs arise on the placental column and burst out from
within the seed pod. Photograph courtesy of Jason Pole.
available knowledge, directs future research, and promotes a
point of view.
Acknowledgements
FT would like to thank Lucy Cavendish College, Cambridge
and the Stanley Smith (UK) Horticultural Trust. NHB
acknowledges research funding from BBSRC, DEFRA and
The University of Reading Research Endowment Trust Fund.
The legend to Fig. 2 was kindly translated from the German
by Alex Angenendt (The University of Reading).
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