Download The mechanism of leaf morphogenesis

Planta (2002) 216: 17–22
DOI 10.1007/s00425-002-0864-8
R EV IE W
Andrew J. Fleming
The mechanism of leaf morphogenesis
Received: 25 April 2002 / Accepted: 15 July 2002
Ó Springer-Verlag 2002
Abstract Whether cell division is a driving force in plant
morphogenesis has long been debated. In this review, the
evidence for the existence of cell division-dependent and
cell division-independent mechanisms of plant morphogenesis is discussed. The potential mechanisms themselves are then analysed, as is our understanding of the
regulation of these mechanisms and how they are integrated into development, with particular emphasis on
data arising from the investigation of leaf morphogenesis. The analysis indicates the existence of both cell
division-dependent and cell division-independent mechanisms in leaf morphogenesis and highlights the
importance of future investigations to unravel the
co-ordination of these mechanisms.
Keywords Development Æ Cell cycle Æ Cell wall Æ
Morphogenesis
Abbreviation CDK: cyclin-dependent kinase
Introduction
Plants are made of cells. It is an intuitive expectation,
therefore, that the number of cells produced in a plant,
the size of those cells, and where and when those cells are
generated should play a major role in controlling plant
size and shape. Indeed, since processes of cell migration
and cell death are much more limited in plants during
most phases of development compared to their animal
counterparts, one might expect cell division pattern and
Dedicated to Nikolaus Amrhein, Zürich, on the occasion of his
60th birthday.
A.J. Fleming (&)
Institute of Plant Sciences,
Swiss Federal Institute of Technology (ETH),
Universitätsstrasse 2, 8092 Zürich, Switzerland
E-mail: andrew.fl[email protected]
Fax: +41-1-6321044
frequency to be deterministic in plant morphogenesis.
This expectation is not met by reality. Not only is it clear
that the vast majority of differentiation depends on cell
position rather than clonal parentage, it has also become
apparent that in many circumstances normal plant size
and shape can be achieved despite major alteration in
factors driving cell division. In this review, I will first
survey the evidence for the existence of cell divisiondependent and cell division-independent mechanisms of
plant morphogenesis before going on to examine the
actual mechanisms themselves. Finally, I will consider
the control and integration of these two mechanisms
into plant development, with special emphasis on leaf
formation.
Since morphogenesis in plants is intimately linked
with growth, an understanding of the control of plant
form also requires an understanding of the control of
organ size. Details on this aspect of morphogenesis will
also be discussed.
Evidence that a cell division-independent mechanism
for morphogenesis exists in plants
At the single-cell level it is clear that change of form
(linked with cell growth) can occur without division
(Folkers et al. 1997). However, what is the situation in a
multicellular organ, such as a leaf?
Significant advances have been made over the last
decade in our understanding of the proteins involved in
regulating the plant cell cycle (Potuschak and Doerner
2001; Stals and Inzé 2001). These data have shown that
plant cells contain a machinery which, although it has
some peculiarities, in general terms is similar to that
described in other eukaryotes. One consequence of this
work has been the generation of transgenic plants in
which specific modulators of the cell cycle have been
over- or under-expressed and, at least in some cases, this
has led to successful modulation of the cell cycle (i.e.,
increased and decreased cell division rate; Hemerley et al.
1995; Doerner et al. 1996; McKibbin et al. 1998;
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Cockcroft et al. 2000). The most surprising observation
from these experiments has been that direct modulation
of the cell cycle (and, thus, of cell division) generally
leads to only minimal alteration in plant morphogenesis
[although note the work of Wang et al. (2000) and
de Veylder et al. (2001) described in the next section].
Effects on plant growth rate are certainly observed
(Cockcroft et al. 2000), but these seem only to influence
the time taken until ‘‘normal’’ size and shape are
achieved.
One criticism of these data has been that morphogenesis might depend on local variations in cell division
rate and that the experiments performed did not alter
these local gradients (Meyerowitz 1996). Experiments
from our own laboratory approached this question by
locally inducing cell division within the apical meristem,
the site of leaf organogenesis (Wyrzykowska et al. 2002).
As shown in Fig. 1A, these manipulations led to an
accumulation of smaller cells on one flank of the apical
meristem. Despite these changes, meristem function and
leaf formation proceeded normally (Fig. 1B). These
experiments demonstrate that local alteration in cell
division rate within the meristem does not disturb
organogenesis.
Plant cell division is characterised not only by the rate
at which this process occurs but also by the fact that the
new cell wall (generated within the dividing cell) can take
up a number of orientations. The orientation of new
wall insertion is expected to have a major influence on
both the differentiation of the daughter cells generated
and the future growth characteristics of these cells
(Steeves and Sussex 1989). Nevertheless, mutants in
which cell division orientation is virtually randomised
still generate all essential organs (Traas et al. 1995) and
mutants in which cell division orientation is disrupted to
a lesser (but still significant) extent generate plants of
approximately normal morphology (Smith et al. 1996).
Again, it is possible to argue that it is local patterns of
cell division that are important and that in the mutants
described above these local patterns were still maintained, thus allowing cell division pattern to drive
morphogenesis. To address this point, we have locally
overexpressed the dynamin-like protein phragmoplastin
within the meristem. Phragmoplastin is involved in cell
c
Fig. 1A–E. Cell division-dependent and cell division-independent
mechanisms of morphogenesis. A Longitudinal section through a
tobacco (Nicotiana tabacum) meristem in which extra cell divisions
have been induced on one flank (arrow; Wyrzykowska et al. 2002).
Bar = 30 lm. B Scanning electron micrograph of a tobacco
meristem treated as in A. Leaf initiation is normal (Wyrzykowska
et al. 2002). Bar = 80 lm. C Tobacco leaf resulting from a
primordium in which part of one flank (arrow) has been induced to
transiently undergo extra cell divisions. An indentation of the
lamina has occurred (Wyrzykowska et al. 2002). Bar = 7 mm. D
Tobacco leaf resulting from a primordium in which part of one
flank (arrow) has been induced to overexpress expansin protein. An
increased lamina expansion has occurred (Pien et al. 2001). Bar =
5 mm. E Scanning electron micrograph of a meristem after local
application of expansin protein. Morphogenesis has occurred
(Fleming et al. 1999). Bar = 20 lm
19
plate formation and overexpression of the protein leads
to abnormal planes of cell division (Gu and Verma
1997). Local overexpression of phragmoplastin in the
meristem led to a disruption of the normally highly
regular pattern of cell division but with no overt
alteration in leaf organogenesis (J. Wyrzykowska and
A.J. Fleming, unpublished data).
Taken together, these studies indicate that plant
morphogenesis is dependent neither on the rate nor
orientation of cell division. A cell division-independent
mechanism of morphogenesis must exist.
Evidence that a cell division-dependent mechanism
for morphogenesis exists in plants
Cytokinesis involves the separation of the mother cell
cytoplasm into two daughter cells (Sylvester 2000). In
plants, this occurs by the formation of an internal cell
wall at a site dictated by the accretion of vesicles
containing new membrane and cell wall material. Mutations in genes encoding proteins involved in cell plate
formation (such as KNOLLE and KEULE) lead to
abnormal or incomplete cell wall formation. As a
consequence, although cell division and cytokinesis can
occur, the seedlings formed cease growth (Lukowitz
et al. 1996; Assad et al. 2000). Combinations of these
mutant genes are phenotypically additive and lead to
an even earlier cessation of development (Waizenegger
et al. 2000). These data indicate that morphogenesis
requires a certain minimum level of competence in cell
division.
More positive data supporting a role for cell division
in morphogenesis have come from the manipulation of
expression of proteins involved in inhibiting cyclin-dependent kinase (CDK) activity. CDK inhibitors (described as ICKs and KRPs in the plant literature)
inhibit the activity of CDK/cyclin complexes. Genes
encoding these proteins have been identified and constitutively overexpressed in plants (Wang et al. 2000;
de Veylder et al. 2001). This led to the production of
smaller plants and to a change in leaf morphology, in
particular an increase in leaf serration. These data show
that not only can cell division have an influence on
plant size, but also that constitutive expression of a cell
cycle regulator can result in a non-uniform response in
terms of organ morphology. Experiments from our own
group also indicate that manipulation of cell division
can influence leaf morphogenesis. Thus, local induction
of genes encoding proteins with a role in the cell cycle
on the flank of young leaf primordia led to a local increase in cell division rate. Subsequently, the induced
regions underwent decreased growth relative to the
surrounding tissue, thus leading to a change in leaf
shape, as shown in Fig. 1C and Wyrzykowska et al.
(2002).
Taken together, these data indicate that cell division
can influence morphogenesis, i.e, that a cell divisiondependent mechanism of morphogenesis exists.
Synthesis
Some level of cell division is required for normal morphogenesis in multicellular plants. Once this minimal level
is achieved, a degree of normal morphogenesis can occur.
In some regions of the plant (e.g., shoot apical meristem)
morphogenesis can occur despite large changes in the
parameters of cell division rate and orientation. In these
regions morphogenesis is not driven by cell division and
occurs primarily via a cell division-independent mechanism. In other regions of the plant both cell divisiondependent and cell division-independent mechanisms
may function. How do these mechanisms work?
The mechanism of cell division-independent
morphogenesis: the cell wall and growth rate
Plant cell growth is a biophysical process involving the
balance of a hydrostatic force acting outwards from the
cell (turgor) with a tensile force within the surrounding
cell wall (Cosgrove 2000). Growth requires a controlled
imbalance between these forces to allow inward flux of
water and the stretching of the cell wall until a new
physical equilibrium is established. The body of evidence
available indicates that while the internal turgor pressure
remains generally constant during growth processes, the
cell wall undergoes regulated changes in extensibility
(relaxation), which allows regulated increase in cell size
(Cosgrove 2000). Theoretically, this regulation in cell
wall extensibility could direct where and when growth in
plant tissue occurs (Green 1999). Evidence in support of
such a mechanism has come from the analysis and manipulation of a particular family of cell wall proteins,
termed expansins.
Expansins were first identified in cucumber seedlings
(McQueen-Mason et al. 1992). Since then, expansinrelated proteins have been identified in the majority of
plant groupings, as well as some non-plant organisms
(Li et al. 2002). Expansin proteins are characterised by
their in vitro ability to loosen cell wall material (hence,
their name). This activity, coupled with the general
correlation of high expansin gene expression and tissue
extension led to the suggestion that they played an endogenous role in the cell wall loosening process required
for growth. Causal evidence from the study of living
tissue has appeared over the last few years. Thus, directed over- and under-expression of an expansin gene in
leaf vascular tissue using a specific promoter element led
to a change in leaf size and morphology (Cho and
Cosgrove 2000) and local induction of expansin activity
on the flanks of young leaves led to a local increase in
tissue growth and lamina expansion, as shown in
Fig. 1D and by Pien et al. (2001). Moreover, localised
expansin activity within the meristem was sufficient to
induce morphogenesis (Fig. 1E), leading to the formation of leaves (Fleming et al. 1997; Pien et al. 2001).
Although the mechanism of expansin action is still
20
obscure, the experiments described above support the
contention that modulation of cell wall loosening controls cell growth and that, when these manipulations are
performed at a local tissue level, the discontinuities in
cell wall extensibility induced are sufficient to induce
relative differences in growth rate which become visible
as altered morphogenesis.
If cell wall relaxation controls growth rate, an important question is how the vector of this growth is
controlled. Recent analysis of the ANGUSTIFOLIA
mutant (in which leaves are narrower and thicker than
normal) has implicated elements associated with regulation of the microtubule cytoskeleton and the cell wall
in this process (Folkers et al. 2002; Kim et al. 2002).
The mechanism of cell division-dependent
morphogenesis: cell division and growth rate
Morphogenesis requires a change in relative growth rate
and, as described above, requires changes in biophysical
parameters of the tissue. The precise mechanism by
which cell division can influence these parameters is
unclear, but presumably factors associated with the cell
cycle (such as CDK/cyclin complexes) impact on target
proteins which regulate these growth processes. This
relatively indirect pathway allows a considerable degree
of flexibility in the relationship between cell division and
growth rate. For example, in monocot leaves the highest
rates of tissue expansion are measured in the region of
the leaf where cell division has ceased or is undergoing
cessation (Tardieu and Granier 2000), whereas in dicot
leaves cell division rate and tissue expansion tend to be
highly correlated (Granier et al. 2000). A further
example of the potentially complex interaction of cell
division and growth is provided by the observed nonuniformity of response of tissue to uniform expression of
regulators of the cell cycle, implying either a differential
sensitivity of tissue in terms of cell division to the same
input of regulator or a differential output of growth rate
in response to the same input of altered cell division
(Wang et al. 2000; de Veylder et al. 2001). Finally, cell
division can influence growth indirectly via its linkage
with differentiation. For example, in the context of leaf
development a key early event is the establishment of a
functional vascular tissue. If altered cell division pattern
were to disrupt vascular differentiation then transport
processes required to supply materials for growth would
be impaired, leading to retardation of growth and altered morphogenesis.
To summarise, the data indicate that cell division
has the potential to influence morphogenesis, but that
the outcome is dependent on the anatomical and developmental context in which the daughter cells are
generated. The link of cell division to growth rate may
be very indirect (via altered differentiation) but can
involve a mechanistic relationship with growth. The
nature of this relationship is discussed further in the
next section.
The integration and control of division-dependent
and division-independent mechanisms
of morphogenesis
The above discussion indicates that both divisiondependent and division-independent mechanisms of
morphogenesis exist. This raises the questions: How are
these mechanisms co-ordinated? Is one mechanism
‘‘superior’’ to the other?
At the cellular level it is clear that under most circumstances growth determines division, i.e., division
occurs only when a cell has reached a particular size
(Conlon and Raff 1999). However, we have little idea of
how a cell measures its size and transduces this information into a signal to promote (or repress) division.
Moreover, it is clear that the size/division relationship is
variable. Cells in a meristem are maintained at a particular size, but as cells are removed from the meristem
this balance between size and division is shifted. Moreover, this shift occurs in a tissue-specific manner (in fact,
in some ways defines tissue identity). The mechanism
controlling this shift in size/division relationship is unknown. The best we can say is that this shift is somehow
related to differentiation and, indeed, might be actually
causally involved in differentiation. This, however, simply moves our level of ignorance to the problem of defining differentiation. Certain cells of the meristem seem
to be maintained in an ‘‘undifferentiated’’ or ‘‘indeterminate’’ state by a complex cascade of transcription
factors (Byrne et al. 2002), but the nature of the
molecular changes induced (or repressed) by these
factors remains to be elucidated.
At the organ level, cell division-dependent and cell
division-independent mechanisms of morphogenesis are
co-ordinated to generate structures of ‘‘appropriate’’
size and shape. By balancing these mechanisms the plant
can both co-ordinate growth rates with environmental/
nutritional status and can provide a failsafe mechanism
by which if one element is removed or not functioning
properly, a compensatory mechanism can cut in to
ameliorate the situation and maintain at least the basic
morphogenic patterns required for plant function
(Doonan 2000). The system acts both to restrict growth
if cell division is promoted above normal levels, but also
to promote growth if cell division is lower than normally
required, leading to the formation of approximately
normal sized and shaped organs, but containing fewer
and larger cells (Hemerley et al. 1995; Jones et al. 1998).
The question, of course, is what is the nature of this
growth co-ordinator? A similar conundrum in animal
biology has led to the proposal of a system for measuring either tissue mass (Potter and Xu 2001) or a
morphogen gradient over space so that cells within the
gradient can sense discontinuities and respond accordingly by appropriate growth (Day and Lawrence 2000).
Although the molecular machinery involved in these
proposed sensors remains unknown, some progress has
been made in identifying factors that have an input into
21
the system. Thus, overexpression of the putative transcription factor AINTEGUMENTA leads to an increase
in organ size with little affect on shape (Krizak 1999;
Mizukami and Fischer 2000) and overexpression of the
ROTUNDIFOLIA3 protein (a cytochrome P450 with a
potential function in steroid biosynthesis) leads to increase in leaf length (Kim et al. 1999). This last paper
suggests that hormonal factors are likely to influence
organ size, as they do in animal systems (Potter and Xu
2001). This expectation seems to be borne out by observations on altered organ size associated with altered
hormone transport or perception (Ecker 1995; Zhong
and Ye 2001). However, the pleiotropic physiological
affects of plant hormones makes direct causal relationships difficult to identify, and its noticeable, for example,
that although altered perception to auxin can lead to
altered cell size within a leaf, no change in organ size
occurs (Jones et al. 1998).
Finally, much of the theoretical work on organ size
and shape assumes the presence of boundaries within
which growth is controlled (Day and Lawrence 2000). In
the context of leaf development, the margin appears to
be a boundary required for lamina extension to occur.
Thus, recent work has identified a number of genes
whose products are required for the acquisition of
abaxial or adaxial leaf identity (Byrne et al. 2001).
Significantly, lamina extension seems to require the
juxtaposition of cells possessing abaxial and adaxial
identities (Waites and Hudson 1995). The interaction of
these domains would thus seem to define a boundary
condition required for setting the limits of future lateral
growth of the leaf. Bearing in mind the specific cellular
processes of division and differentiation that occur in
these marginal cells (Poethig and Sussex 1985; Donnelly
et al. 1999), and the fact that our own experiments
modifying leaf shape involved modulation of these cells
(Pien et al. 2001; Wyrzykowska et al. 2002), the future
analysis of the mechanism of abaxial/adaxial domain
interaction and its downstream targets promises to shed
light on a fundamental aspect of leaf morphogenesis as
well as exploring the molecular nature of a classically
proposed morphogenic patterning mechanism.
Acknowledgements I would like to thank members of the group for
useful discussions during the preparation of this manuscript. The
author is a START Fellow of the Swiss National Science Foundation (SNF). Research in my laboratory is funded both by the
SNF and the Swiss Federal Institute of Technology. This research
was enabled by the generous provision of space, equipment and
materials by Nikolaus Amrhein.
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