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A matter of size: developmental control of organ size in plants
Yukiko Mizukami
The intrinsic size of plant organs is determined by developmental
signals, yet the molecular and genetic mechanisms that control
organ size are largely unknown. Ongoing functional analysis of
Arabidopsis genes is defining important regulators involved in
these mechanisms. Key features of this control are the
coordinated activation of growth and cell division by growth
regulators and the maintenance of meristematic competence by
the ANT gene, which acts as an organ-size checkpoint.
Alterations of genome size by polyploidization and
endoreduplication can reset this checkpoint by
ploidy-dependent, epigenetically regulated differential gene
expression. In addition, the regulation of polarized growth and
phytohormone signaling also affect final organ size. These
findings reveal unique aspects of plant organ-size control that
are distinct from animal organ-size control.
Addresses
Department of Plant and Microbial Biology, University of California,
231 Koshland Hall, Berkeley, California 94720, USA;
e-mail: mizukami@nature.berkeley.edu
Current Opinion in Plant Biology 2001, 4:533–539
1369-5266/01/$ — see front matter
© 2001 Elsevier Science Ltd. All rights reserved.
Abbreviations
ABP1
AUXIN-BINDING PROTEIN1
ANT
AINTEGUMENTA
CDK
cyclin-dependent kinase
CycD2 Cyclin-D2
FRL1
FRILL1
ICK1
INHIBITOR OF CDK1
IFL1
INTERFASCICULAR FIBERLESS1
KRP
KIP-related protein
REV
REVOLUTA
ROT3
ROTUNDIFOLIA3
SAM
shoot apical meristem
UFO
UNUSUAL FLORAL ORGANS
Introduction
Undoubtedly, size is one of the most obvious differences
among various plant organs, and among the same organs
from different plant species. Given their immovable,
light-dependent lifestyle, the organ size of plants is
often influenced by external environmental signals.
Nevertheless, there is clear evidence that organ size is
primarily controlled by internal developmental signals in
plants. For example, the flowers and petals of individual
Arabidopsis thaliana plants grown under the same conditions are remarkably uniform in size. In contrast, the
flowers and petals of Brassica napus, another member of
Brassicaceae, are always much larger than those of
Arabidopsis (Figure 1). Although it has long been established that organ size within a species is constant but
differs among species, the developmental mechanisms
that regulate the inherent organ size of plants have been
investigated only recently.
Plant organ size reflects both cell number and cell size.
Studies carried out during the 19th century reported that,
among the same type of organs from plant species of different size, larger organs tend to be composed of more cells
rather than bigger cells [1]. This is true for the absolute size
difference between Brassica and Arabidopsis petals, which
have epidermal cells of a similar size (Figure 1). On the other
hand, significant differences in cell size apparently contribute to the size difference between the leaves and petals
of Arabidopsis (Figure 1). However, alteration of cell proliferation or cell expansion is not always correlated with changes
in organ size. This is because the extent of organ growth is
controlled independently of cell division and cell expansion
during plant organogenesis [2,3]. Hence, a key to uncovering
the mechanisms that control plant organ size should be
found by studying how plants coordinate the extent of
growth with cell division and post-mitotic cell expansion during organogenesis. Although genetic analysis of the internal
control of plant organ size is just beginning, recent studies
are uncovering potential genes that define plant organ size
through coordination of growth and the cell cycle. In this
review, I focus on the genetic mechanisms underlying the
developmental control of shoot organ size in terrestrial
flowering plants, with emphasis on A. thaliana. Other recent
reviews provide more detailed information about cell-size
determination in plants [4•] and other systems [5], and about
control of organ and body size in animals [6,7,8•].
Polyploidy and endoreduplication:
evolutionary and developmental means for
controlling cell and organ size
The importance of genetic mechanisms in controlling the
size of plants, plant organs and plant cells can be seen in the
effect of polyploidy. Plant cell size is correlated with
nuclear size, and thus with genome size [4•]. This is also
true for animal cells and yeast cells, in which metabolic
activity is enhanced and patterns of gene expression altered
as ploidy levels increase [9]. In animal systems, however,
the size of an organ is determined by its total mass, and
ploidy levels do not reflect the size of organs or organisms
[6,7,8•]. In plants, systemic polyploidization directly
influences organ size, and therefore, the stature of the
whole plant. Many crop products, such as cotton, wheat,
and banana, have high-ploidy varieties, which produce larger
flowers, grains, or fruits than those of diploid counterparts.
Recently, Lee and Chen [10] reported ploidy-dependent,
epigenetically altered gene expression among diploid
A. thaliana, diploid Cardaminopsis arenosa and allotetraploid
Arabidopsis suecica plants, each of which have quite different
organ sizes. Thus, those genes that are expressed differentially may include components of organ-size control.
In addition to systemic polyploidization, somatic increase
of genome size commonly occurs during organogenesis of
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Cell biology
Figure 1
(a)
(c)
(b)
(d)
(f)
(e)
Current Opinion in Plant Biology
Evidence for intrinsic organ-size control in Brassicaceae plants. (a) Mature
A. thaliana (Col-0) flowers from eight individual plants grown under the
same long-day conditions. (b) A set of four petals from one of the flowers
shown in (a) (first four petals from the left) and petals from each of the
other seven flowers exhibiting size uniformity. (c) The size of flowers and
petals of two Brassicaceae species, A. thaliana (left) and B. napus
(right) are very different. However, the size of petal epidermal cells of
(d) A. thaliana and (e) B. napus are nearly the same. (f) In contrast,
most A. thaliana leaf epidermal cells are much larger than the petal cells
of the same plant. Images in (d–f) are of the same magnification.
angiosperm species. This process, termed endoreduplication,
involves DNA replication without nuclear and cell divisions, resulting in cells with nuclei that are larger than
diploid nuclei [11,12•]. In an extreme example, embryo
suspensors of Tropaolum majus have a DNA content of
2048C [11]. Presumably, endoreduplication has evolved
as a developmental means of providing differential gene
expression in species with a small genome [11]. Because
cell volume is directly correlated with the level of
endopolyploidy [13], the developmental regulation of
endoreduplication could be a mechanism employed to
control post-mitotic cell expansion and, hence, organ size.
FRILL1 (FRL1) could be a negative component of such a
mechanism [14•]. Although the distal portion of wildtype Arabidopsis petal epidermis consists of diploid cells,
cells in the distal portion of the frl1 mutant petal epidermis exhibit abnormal endoreduplication late in
development, giving rise to enlarged mature petals with
large polyploid cells [14•]. Conversely, Arabidopsis leaves,
in which a large proportion of cells are polyploid and larger
than diploid cells [13,15], were reduced dramatically in
size as the number of endoreduplication cycles was decreased
in gibberellin-deficient mutants [4•]. Thus, endoreduplication is an important determining factor for particular
organ size.
Phytohormone signaling components
sufficient for altering cell and organ size
Mutants that are defective in phytohormone biosynthesis
or perception clearly show the importance of these substances in regulating plant growth and morphology [16].
Often, alteration of final organ size is one of the consequences
of modified phytohormone signaling. Some signals may
regulate cell growth and cell division, whereas others
likely contribute to post-mitotic cell expansion associated
with cell differentiation to determine final organ size [16].
The Arabidopsis ethylene-overproduction1 (eto1) and constitutive
triple response1 (ctr1) mutations cause ethylene overproduction
and constitutive activation of ethylene signaling, respectively,
and result in smaller than normal organs due to reductions
in both cell size and cell number [17]. Conversely, leaves
and floral organs of plants with ethylene receptor1 (etr1) and
ethylene-insensitive2 (ein2) mutations, which interfere with
the ethylene-signaling pathway, are much larger than those
of wild-type plants [17]. Therefore ethylene signaling
regulates the direction and/or extent of cell expansion and
influences cell proliferation, ultimately having an effect on
final organ size.
Whereas ethylene and cytokinins increase cell expansion
along transverse axes, gibberellin, brassinosteroids, and
Developmental control of organ size in plants Mizukami
auxins regulate expansion along longitudinal axes and
greatly influence plant stature and organ size [18]. A role
for auxin signaling in cell expansion has been confirmed by
recent studies of the AUXIN-BINDING PROTEIN1
(ABP1) gene. Ectopic expression of ABP1 in transgenic
tobacco leaves led to remarkable increases in cell volume.
However, ABP1 does not seem to control organ size
because the increase in cell size was accompanied by a
compensatory decrease in cell numbers, resulting in no
major effect on mature leaf size [19]. In contrast, studies of
the REVOLUTA (REV)/INTERFASCICULAR FIBERLESS1
(IFL1) gene suggest that the polar flow of auxin may act as
a cue for organ-size control. In rev/ifl1 mutants, growth and
cell proliferation persist longer than in the wildtype,
resulting in larger leaves and flowers, and thicker stems
[20,21]. REV/IFL1 function is required for the activity of
auxin polar transport, as well as for secondary shoot
meristem formation and normal differentiation of interfascicular fiber cells [22]. Hence, REV/IFL1 links polar auxin
transport to fiber cell differentiation, and possibly to the
regulation of secondary meristem formation and the
determination of the extent of organ growth.
Genes that link pattern formation and
organ-size determination
In developing organs, growth is accompanied by pattern
formation that determines organ form. A number of studies
on plant allometry suggest a correlation between organ
form and organ size [1]. In theory, the extent of polarized
growth could contribute to differences in both size and
shape of mature organs. In fact, recent studies have shown
that there are developmental factors that are involved in
both pattern formation of organs or shoot architecture and
organ-size control. One such gene, ROTUNDIFOLIA3
(ROT3), regulates longitudinal leaf growth in Arabidopsis
[23]. Leaves of rot3 mutants are of normal width but shorter
than normal length. Conversely, overexpression of ROT3
results in increased leaf and floral organ length, with no
alteration in width [24]. Observations of cellular organization of the leaf epidermis revealed that ROT3 regulates
longitudinal cell growth and thereby defines organ length
during organogenesis.
Organ shape and size are characteristics unique to each
organ, such as leaves, petals or stamens. Thus, the identity
of the organ itself could be a determinant of ultimate organ
size. That is, some genes that specify organ identity also
determinate the size characteristics of a particular type of
organ. For example, UNUSUAL FLORAL ORGANS (UFO)
specifies floral organ and meristem identities in
Arabidopsis, but also influences organ size [25]. Besides
homeotic conversion of floral organs, ufo mutations cause a
reduction in the size and number of chimeric petals and
stamens, whereas overexpression of 35S::UFO gives rise to
highly lobed leaves [26] and wide petals (Y Mizukami,
unpublished data), thereby greatly increasing organ size.
UFO encodes a protein with an F-box domain [25], which
has been found in regulators of phytohormone signaling
535
in Arabidopsis and in cell cycle regulators that promote
the G1→S or G2→M transition in other systems [27].
Hence, in developing petals, UFO may couple the extent
and polarity of organ growth with cell division and with
the determination of organ identity.
Roles of cell division in organogenesis
A fundamental role for cell division in organogenesis and
organ-size determination is implied by the fact that larger
organs tend to consist of more cells than do smaller organs
[28,29]. In plants, a number of studies have indicated that
cell division is a consequence, but not the cause, of organ
growth [3]. In other words, cell division maintains progressing growth. Given this, how does cell division
contribute to growth and organ-size control? Presumably,
the crucial role of cell division is to reproduce and spread
nuclei, the source of information molecules (e.g. RNA and
proteins), by appropriate distances as organs grow. This
distribution of nuclei is required to maintain growth rate
because of the physical limits on information transfer. In
the absence of cell division, organ growth becomes slower
and eventually terminates prematurely, resulting in smaller
mature organs. This was shown by classic experiments
with gamma-irradiated wheat leaf primordia in which the
absence of cell divisions decreased the growth rate and
the final size of leaves and altered leaf shape, although
polarized growth continued to some extent, resulting in
the enlargement of pre-existing leaf cells [2]. This result
demonstrates that cell division is necessary for the
attainment of the final organ size, which is determined
independently; nevertheless, the effect of increased cell
division on organ size has not been tested.
Another key function of cell division in organ growth may
be to insert new cell walls, which give mechanical support
to developing organs, and to isolate cells for differentiation.
Several cell-wall mutants, such as radial-swelling1 (rsw1),
produce organs that are smaller than normal despite their
larger-than-normal cells [30], indicating the significance of
cell-wall formation in organ-size control.
Coordination of growth with cell division by
D-type cyclins
An important conclusion of the experiment on gammairradiated plants described above is that organ growth is
coordinated with cell division to maintain a certain
growth rate during organogenesis. How is this coordination carried out? A recent study using transgenic
tobacco plants revealed that Cyclin-D2 (CycD2), one of
the D-type cyclins of Arabidopsis, could coordinate growth
with cell division [31••]. In animal systems, D-type cyclins
associate with a cyclin-dependent kinase (CDK) partner to
mediate the G1→S cell-cycle transition [32]. It has been
suggested that the Cyclin-D–CDK complex could be a
key regulator that connects growth and the cell cycle in
animal systems [32,33,34•]. Ectopic expression of Arabidopsis
CycD2 was reported to increase the growth rate of transgenic
tobacco plants by accelerating the initiation of primordia
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Cell biology
Figure 2
(a)
WT/4C
frl1
ABP1OE
rev/ifl1
rot3
35S::ROT3
35S::UFO
ctr1
ein2, etr1
WT/2C
(b)
35S::CycD2
35S::ICK1
ant1
35S::ANT
(c)
Effects of altered gene function on plant
organ size. (a) The petal phenotypes of two
A. thaliana polyploids (WT/2C and WT/4C)
and 12 A. thaliana genotypes with altered
gene expression are shown. Below the outline
of each petal is a depiction of the relative size
and shape of cells comprising the petal.
The effects of 35S::CycD2 and ABP1OE on
petals are deduced from the results with
tobacco leaves. ctr1, constitutive triple
response1; ein2, ethylene-insensitive2; etr1,
ethylene receptor1; OE, overexpressor.
(b) Reduction of ANT function produces
A. thaliana leaves that are much smaller (left)
than normal (center), whereas constitutive
ANT expression dramatically increases leaf
size (right). (c) Ectopic expression of BANT,
an ANT ortholog from B. napus (right),
produces (center) A. thaliana floral organs
that are much larger than (left) normal.
A B. napus flower is shown on the right.
Current Opinion in Plant Biology
in the shoot apical meristem (SAM) [31••]. This result
suggests that CycD2 is a coordinator of growth and cell
division because ectopic CycD2 expression stimulates both
growth and the cell cycle in the SAM, which therefore
produces meristem cells at a faster-than-normal rate.
In animals, overexpression or mutational activation of D-type
cyclins and/or CDK not only enhanced both cell and organ
growth along with cell division, but also prolonged the
extent of growth during animal organogenesis and resulted
in hyperplasia [35,36•]. Thus, D-type cyclins are components of organ-size control in animals. In plants, however, the
role of D-type cyclins in organ-size control is inconclusive.
In contrast to the dramatic enhancement of whole-plant
growth resulting from CycD2 overexpression, CycD2 overexpression essentially did not affect the growth rate and
final size of organs [31••]. Therefore, CycD2 function in
growth stimulation is likely restricted to the SAM.
Arabidopsis has at least four D-type cyclins [37], one of
which, CycD3, is activated by the mitogenic phytohormone
cytokinin [38]. Ectopic expression of CycD3 bypasses the
requirement of cytokinin for shoot formation in callus [39].
It is possible that one of the plant D-type cyclins, like the
D-type cyclins in animal systems, is an organ-size regulator.
During G1-phase in mammalian cells, the assembly of the
Cyclin-D–CDK4 complex with p27KIP1, a CDK inhibitor
[32], is promoted by mitogenic signals. This assembly
sequesters p27KIP1 and facilitates activation of the CyclinE–CDK2 complex, thereby triggering entry into S phase
[32]. Interestingly, in mice, knock out of the p27KIP1 gene
caused hyperplasia [40], suggesting that p27KIP1 is involved
in organ-size control and plays a role as ‘an intrinsic timer’
in defining the extent of growth [6]. The plant homolog of
p27KIP1, INHIBITOR OF CDK1 (ICK1), has been isolated
in Arabidopsis. This protein has been shown to bind to both
CycD3 and Cdc2a (Cell division cycle 2a), and to inhibit
kinase activity in vitro [41]. Recently, expression of
35S::ICK1 was indeed shown to reduce cell numbers and
organ size in transgenic Arabidopsis plants [42••]. Seven
other Arabidopsis p27KIP1 homologs, the KIP-related proteins (KRPs), all of which share homology to animal p27KIP1
in the carboxy-terminal region, have been identified.
35S::KRP2 transgenic plants exhibited a slightly reduced
organ-size phenotype similar to that caused by 35S::ICK1
expression [43]. However, loss-of-function analyses of ICK1
and other KRPs have not yet been carried out. Future
investigation of the functions of other ICKs/KRPs may
reveal their roles in plant organ-size control.
AINTEGUMENTA: a regulator of the
organ-size checkpoint
Recent studies have revealed a gene that defines organ
size by regulating the extent of cell proliferation coordinately with growth. Loss-of-function mutations of the
AINTEGUMENTA (ANT) gene of Arabidopsis were shown
to reduce the numbers and size of floral organs [44,45] and
leaf size [46••]. Furthermore, ectopic expression of ANT
under the control of the constitutive CaMV 35S promoter
increased the size of vegetative shoot organs, such as
leaves and stems [46••], as well as of floral organs [46••,47]
(Figure 2). Altered ANT function modifies mature organ
Developmental control of organ size in plants Mizukami
537
Figure 3
A model for the control of plant organ size.
Developmental signals (i.e. growth
promoters) activate growth signal mediators
such as ANT, which stimulate growth
coordinators (e.g. D-type cyclins) to activate
and couple growth and cell division, and to
maintain meristematic competence. The
mediators also suppress differentiation
signals. As growth proceeds by increasing
translation, protein synthesis and other
growth-related processes (e.g. wall synthesis
and cytoskeletal organization), genome
replication and nuclear division occurs and
new cell walls form to complete cell division
so that growth continues. Growth rate is
monitored, and continued growth is ensured
by growth mediators via the maintenance of
the meristematic competence of cells
(dashed line). As the activity of the growth
mediators declines, cells lose meristematic
competence, and growth and cell division
eventually cease. Simultaneously,
differentiation begins; it suppresses
mitosis-dependent growth and reorganizes
the cell-size checkpoint (blue lines), such that
either endoreduplication or
Growth promoters
Differentiation signals
(Developmental signals)
Growth signal mediators
Organ-size checkpoint
Intrinsic organ size
Ploidy level
Growth coordinators
Growth
Meristematic competence
(Protein synthesis, etc.)
Cell division
cycle
(DNA synthesis)
DNA content/Cell-mass sensors
Cell-size checkpoint
Current Opinion in Plant Biology
differentiation-dependent cell expansion is
initiated, and finally, intrinsic organ size is
acquired. Polyploidy resets the thresholds for
size mainly by influencing total cell numbers, and thus
cell proliferation. Further examination of cell numbers
and cell size in developing petals and leaves revealed that
ANT does not control growth rate or the cell cycle, rather
it regulates the extent of organ growth and cell divisions
during organogenesis [46••]. These phenotypes strongly
suggest that ANT most likely maintains ongoing cell proliferation coordinately with growth. Loss of ANT function
causes cells to withdraw from the mitotic cell cycle
prematurely, resulting in early termination of growth and
reduced organ size. Conversely, gain of ANT function
allows cells to grow and proliferate for a period longer than
normal, thus causing organ enlargement (Figure 2).
ANT function is not limited to Arabidopsis; 35S::ANT
expression also increased organ size in transgenic tobacco
plants [46••]. ANT encodes a transcription factor of the
APETALA2-domain family, and its ortholog has been
identified in other plant systems [45,46••]. The finding that
ectopic expression of BANT, an ANT ortholog from
B. napus, also causes organ enlargement in Arabidopsis further
supports the existence of a conserved ANT function in
organ-size control in different plant species [46••] (Figure 2).
organ-size and cell-size checkpoints by
altering gene expression and metabolic
activities (purple lines).
begins with the emergence of organ primordia, in which
most cells have the ability to grow and divide by responding to developmental growth signals. In traditional terms,
this ability is defined as ‘meristematic competence’ [48].
As organs grow, they locally lose meristematic competence,
cell division ceases and differentiation begins along with
post-mitotic cell expansion. ANT ensures progressing
growth by maintaining meristematic competence, so that
growth continues as long as ANT functions in the developing organs. This hypothesis is supported by the following
findings: first, CycD3 expression was found to be sustained
in fully mature 35S::ANT leaves but not in wild-type
leaves [46••]; second, ANT mRNA accumulates in growing
domains of developing organs, where cells are actively
dividing, and is diminished as cells begin to differentiate
[45]; and finally, ectopic ANT function allowed cells in fully
mature organs to give rise to callus tissue and new organs
without cytokinin/auxin treatment [46••]. These observations clearly indicate that ANT sustains the ability of cells
to coordinately grow and divide during organogenesis,
that is, ANT maintains meristematic competence, thereby
helping to define intrinsic organ size.
Conclusions
Maintenance of meristematic competence
by ANT
How does ANT define the extent of growth and cell
proliferation to regulate intrinsic organ size in developing
plants? One hypothesis is that ANT mediates the signals
to growth coordinators, such as D-type cyclins, which in
turn activate growth and cell proliferation in response to
developmental signals (Figure 3). Plant organogenesis
Organ size in plants, as in animals, is genetically defined
by developmental cues. However, as plants have a unique
cellular structure, body architecture, and growth strategy
[3], the mechanisms that control organ size in plants appear
to be different from those for animal organ-size control.
Coordination of organ growth with cell division, and of cell
expansion with cell differentiation, is essential for organ-size
determination in both animals and plants. However, the
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Cell biology
size of plant organs is not determined by total mass, as is
the case for animal organs. Rather, the maintenance of
meristematic competence in developing organs is a key to
size control in plants. A model including recently found
regulators and potential interactions is depicted in
Figure 3. At present, the molecular nature of meristematic
competence is unknown. The identification of ANT target
genes [49] may help us to understand it. In addition to
studies on already known mutants and genes involved in
organ-size control, the identification of additional mutants
that increase organ size will provide important information
about the developmental control of organ size in plants. A
complementary approach that identifies organ size QTL
(quantitative trait loci) within Arabidopsis ecotypes [50],
and in other Brassicaceae species exhibiting significant
organ-size differences, may reveal genes responsible for
the evolution of organ size in plants.
Acknowledgements
I thank Joe Colasanti for helpful discussions and comments on the
manuscript and Bob Fischer for the opportunity to write this review.
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