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31
Developmental complexities of simple leaves
Michael J Scanlon
Recent papers have explored early events in the development
of simple leaves. Functional compartmentalization of the shoot
apical meristem correlates with distinct fields of cells
connected by plasmodesmata. Molecules important in the
initiation of phyllotactic pattern are described and the
relationship between dorsoventral patterning and lateral leaf
expansion is investigated.
Addresses
3609 Plant Sciences, Botany Department, University of Georgia,
Athens, GA 30602, USA; e-mail: [email protected]
Current Opinion in Plant Biology 2000, 3:31–36
1369-5266/00/$ — see front matter © 2000 Elsevier Science Ltd.
All rights reserved.
Abbreviations
CZ
central zone
knox
knotted1 class of homeobox
PZ
peripheral zone
SAM
shoot apical meristem
Introduction
Amid the vast diversity in plant morphology, no organ contributes more to phenotypic variation than the leaf. Plants
have evolved various spatial arrangements of leaves about
the stem (phyllotaxy), and disparate varieties of leaf size,
shape and complexity. Despite this inherent variability, at
least two developmental characters define most if not all
leaves [1,2]: namely leaves arise from a relatively large
number of progenitor ‘founder cells’ [3] recruited from the
periphery of the shoot apical meristem; leaves are dorsiventrally asymmetrical (bifacial) at their inception.
This review describes recent insights into leaf developmental mechanisms, focusing primarily on investigations
of simple leaves in the monocot maize plant, and in the
dicots Arabidopsis, tobacco and snapdragon (Antirrhinum).
Interested readers are directed to more historically comprehensive reviews [4–6] for discussions of compound leaf
development, and simple leaf development from nonmodel organisms. This review emphasizes newly published
research (from 1998 to present) relevant to the development of morphological diversity between monocot and
dicot leaf forms. Two early stages in the development of
simple leaves are discussed (see also [4,5]). The first stage
is characterized by leaf founder-cell recruitment, wherein
the transition from meristematic identity to leaf identity
occurs. The second stage engenders the expansion of the
founder cells into a young leaf primordium.
Meristem-leaf transition stage
The shoot apical meristems (SAMs) of maize and the dicots
Arabidopsis, tobacco and Antirrhinum exhibit similar patterns
of zonation and structure [7]. Leaf organogenesis occurs in a
lateral region of relatively high mitotic index called the
meristem ‘peripheral zone’ (PZ). The meristem ‘central
zone’ (CZ), characterized by a lower rate of cell division,
replenishes meristematic cells contributed to developing
leaves. The expression profiles of the knotted1 class of
homeobox (knox) genes in maize [8–13], and those of orthologous genes in Arabidopsis [14,15], mirror this pattern of
meristem zonation. Accordingly, knox genes are expressed at
very high levels in the CZ, and are downregulated in the PZ
of the meristem. These data indicate that the downregulation of knox genes might contribute to leaf founder-cell
determination during development of simple leaves.
The pattern and extent of knox downregulation in the
SAM also reflects morphological differences of leaf bases
in monocots and dicots. For example, maize leaves, in
which the leaf bases completely ensheath the circumference of the stem into which they are inserted [1,2], display
knox downregulation that extends from one meristem flank
to the opposite pole ([8,9]; Figure 1). In contrast, the leaf
bases of Arabidopsis exhibit far less spreading around the
stem than those of maize; this phenotype is correlated with
stm1 homeobox downregulation that is markedly more
localized ([15]; Figure 1). The molecular pathway leading
to founder-cell recruitment, and the specific role for knox
genes in this process, remain unknown; however, recent
analyses of symplasmic fields in plant meristems illuminate a route for the channeled movement of proposed
signaling molecules during founder-cell recruitment stages
of leaf morphogenesis [16••,17••].
Symplasmic fields are groups of plant cells united by plasmodesmatal connections. Rinne and van der Schoot [16••]
and Gisel et al. [17••] tracked the movement of fluorescent
dyes into vegetative SAMs in birch and Arabidopsis,
respectively. These studies showed that the PZ and CZ of
the outer meristem layer comprise distinct and separate
symplasmic fields. In the early initiation stages of foundercell recruitment [8,15], however, a transient connection
between the PZ and CZ is established [16••]. Therefore,
signaling molecules might theoretically move between
symplasmic fields and initiate leaf morphogenesis.
Spatial patterning of founder cell recruitment:
phyllotaxy
The geometrically-precise placement of leaves about the
stem — a process that ultimately depends upon the pattern of founder-cell recruitment in the SAM — has long
intrigued experimental botanists [18,19]. Surgical studies
demonstrated that the close proximity of existing leaf primordia inhibits the initiation of new leaves from the SAM
[20]. The nature of this purported inhibitory factor, albeit
chemical or physical or both, has been the subject of
botanical debate.
32
Growth and development
seedlings, and is correlated with an abnormally large meristem. Reversion of the mutant phenotype to normal
phyllotaxy is common in upper leaves, accompanied by
concomitant restoration of normal meristem size. Jackson
and Hake [23•] note that a correlation between SAM size
and change in phyllotaxy is characteristic of dicot species
that exhibit disparate phyllotaxies during their life cycle,
although cause and effect can not as yet be determined.
Figure 1
(a)
maize
Maize
maize
(b)
Dicots
Founder cell stage
Primordial stage
Current Opinion in Plant Biology
Early development of simple leaves. Model for stages in early leaf
development in (a) maize and (b) typical dicots. In (a) maize, founder
cell (darkly shaded) recruitment begins on one meristematic flank and
expands laterally to completely surround the SAM (lightly shaded). The
hooded primordium that subsequently emerges from the SAM displays
dorsoventral asymmetry and envelops the SAM because the lateral
domains of the leaf blade and sheath are established during founder
cell recruitment. In (b) dicots, however, founder cell recruitment does
not proceed extensively around the SAM. The peg-like primordium that
emerges, although dorsoventrally asymmetrical, contains a mildly
expanded leaf base but does not have a prominent lamina. Interaction
of dorsal and ventral domains in the distal regions of the primordium
induces expansive growth of the dicot lamina (striped). The petiole
forms from the unexpanded region of the primordium, between the
proximal leaf base and the distal lamina.
Recent research into the maize mutation terminal ear1 has
shed new light on the question of phyllotaxis. Veit et al.
[21••] found that the terminal ear1 gene encodes a mRNA
binding protein that is expressed in a horseshoe configuration subtending leaf primordia. The open end of the
horseshoe corresponds to the position of young primordia,
including the founder cells of the incipient leaf prior to any
visible morphogenesis. These researchers postulate that
the TERMINAL EAR protein might function to regulate
phyllotaxis in maize shoots via inhibition of leaf initiation
within its expression domain. Consistent with this prediction, terminal ear mutants produce superfluous numbers of
leaves in an disorganized pattern. Characterization of the,
as yet unknown, target(s) of the TERMINAL EAR protein promises to divulge crucial information to our
understanding of the earliest events in leaf development.
Another maize mutation impacting phyllotaxy is abphyl1
(aberrant phyllotaxy) [22,23•]. This intriguing mutant displays dechussate (two leaves per node) phyllotaxis, which
is common to many dicot plants. Normal maize, like all
grasses, produces vegetative leaves in an alternate (a single
leaf per node) phyllotaxis. The dechussate phenotype is
especially pronounced in abphyl mutant embryos and
A direct role for biophysics in leaf initiation is championed
by researchers studying the interaction of externally
administered EXPANSINS and shoot meristems
([24,25,26••]; see also review by Cosgrove, pp 73–78). In
these studies, the placement of beads soaked with
EXPANSINS — proteins that increase extensibility of
plant cell walls — induced leaf primordial development
from tomato meristems. The EXPANSIN-induced organs
satisfy several leaf developmental criteria, including
dorsoventrality and an influence on the positioning of
incipient leaves. In addition, Reinhardt et al. [26••] show
that the expansin gene LeExp18 is expressed in tomato
SAMs at the site of incipient leaf formation. Nonetheless,
the primordia that emerge from EXPANSIN-treated
meristems do not complete the full program of leaf morphogenesis, but cease development in early primordial
stages [24,25]. The abortion of leaf development is
ascribed to the external application of EXPANSINS,
which are normally produced endogenously [25].
Kuhlenmeier and colleagues [24,25,26••] argue that their
results support a biophysical model for leaf development
[27,28], in which meristematic stresses result in localized
buckling of the SAM and subsequent initiation of leaf
development. In this view, EXPANSIN-induced cell wall
loosening causes bulging of the meristem, which in turn
elicits morphogenesis. Additional data are required to clarify whether EXPANSIN accumulation is an initiator of, or
merely a later response to leaf morphogenetic programs.
The progression from founder cells to a leaf
primordium
The knox gene family [9,11] was first identified by dominant
mutations that cause ectopic expression of these meristematic genes in developing leaf primordia [8,10,12,13,29,30].
Although all of the dominant Knox mutations result in similar transformations of distal blade tissue into proximal
sheath-like tissue, a fascinating aspect of the Knox mutants
is the leaf domain-specific perturbations associated with
individual Knox mutant phenotypes (reviewed in [31]). Two
newly-cloned members of this mutational class are gnarley1
[12,32•] and liguless3 (lg3) [13], each characterized by dominant regulatory mutations that transform leaf cell/tissue
identities. Consistent with previous analyses of other Knox
mutations, lg3 is normally expressed in shoot apices, whereas Gnarley1 and Lg3 mutations result in the ectopic
accumulation of KNOX proteins in leaf primordia. Clonal
analyses indicate that the Gnarley1 mutant gene-product is
cell autonomous in the lateral dimension of the leaf, but
non-cell autonomous in the transverse dimension [32•].
Developmental complexities of simple leaves Scanlon
An exciting development in knox gene research is the identification of genes regulating knox gene expression
[33••–35••,36]. The phantastica gene encodes a member of
a small subfamily of MYB-related transcription factors
[33••] required for the proper regulation of a knox gene in
Antirrhinum [34••,35••]. Waites et al. [33••] show that phantastica is transcribed in developing lateral organs and,
therefore, represents the first molecular marker found to
be expressed in leaf founder cells.
Leaf dorsoventrality and lateral leaf expansion
Hudson and colleagues [33••,36] describe phantastica
mutant leaves as defective in several aspects of leaf development, including lateral expansion of the lamina,
dorsoventrality and proximal-distal patterning. A severe
phenotype of phantastica mutants is a radialized leaf, interpreted as lacking dorsal leaf identity [36]. These
researchers propose that PHANTASTICA promotes dorsal
leaf identity, which is required to initiate lateral growth
[33••,36]. This model is based upon the premise that dicot
leaves, which emerge from the meristem as peg-shaped
buttresses [2–5,7], undergo lateral expansion of the lamina
during primordial developmental stages (Figure 1). In this
view, dorsal (adaxial) and ventral (abaxial) leaf identity is
established at the founder-cell stage. Subsequently, the
juxtaposition of dorsal and ventral domains at the margins
of the dicot leaf primordium results in the elaboration of
leaf blade (lamina) development along a new lateral axis.
In contrast, the leaf blade domains of monocot grasses are
established prior to the primordial stage, as illustrated by the
flattened stem-encircling primordia of newly initiated grass
33
leaves ([1–3]; Figure 1). Analyses of the mutant narrow sheath,
which conditions the pre-primordial deletion of lateral leaf
domains [37,38], also support a model for founder-cell-staged
recruitment of leaf blade domains in maize.
Interpretations of the phenotypes of several new leaf pattern
mutants are inspired from the proposed model for PHANTASTICA function [33••], wherein lateral leaf expansion
requires the interaction of dorsal (adaxial) and ventral (abaxial) identities. Analyses of the bladeless tobacco leaf mutant
lam1 [39,40] demonstrate that the LAM1 ‘dorsalizing factor’
is required in L3-derived layers of the shoot (i.e. the innermost layers of the SAM) in order to establish dorsal
differentiation and lateral growth in leaf primordia.
The dicot model for lateral leaf expansion presupposes
that ventralizing, as well as dorsalizing mutations, should
likewise condition radialized leaves devoid of lamina. As
predicted, the dominant mutation phabulosa1 produces
dorsalized (adaxialized) leaves that often display radial
phenotypes and fail to develop leaf blades [41•]. A striking
phenotype observed in severe phabulosa mutants is the
development of ectopic meristems surrounding the bases
of adaxialized leaves. This phenotype, and the adaxialized
expression pattern of the putative meristem-forming factor
PINHEAD [42••], strongly suggests that the adaxial leaf
domain renders competency to develop SAMs. McConnell
and Barton [41•] propose that PHABULOSA may be
required to specify adaxial cell fate, although these predictions are tempered by the inherent difficulties in
discerning the wild-type function of genes identified by
dominant, gain-of-function mutations.
Figure 2
Morphology of simple leaves. Schematic
representations of leaf morphology in
(a) maize and (b) ‘typical’ dicots such as
Arabidopsis, tobacco, and Antirrhinum.
(a) Maize leaves have an expansive leaf base
that encircles the stem completely. The straplike leaf is comprised of distinct regions along
the proximal-distal axis: these include the
sheath, which wraps around the stem; the
epidermally derived ligule fringe; the wedgeshaped auricle, which acts as a hinge; and the
lamina (blade), which displays a prominent
midrib. (b) Dicot simple leaves typically have a
leaf base that expands only partially around
the stem. The leaf base may bear
appendages, called stipules. The proximal
petiole is radially symmetrical, whereas the
distal lamina is dorsoventrally flattened.
(a)
Midrib/midvein
(b)
Midrib/midvein
Lamina/blade
Lamina/blade
Auricle
Ligule
Sheath
Leaf base
Petiole
Stipules
Leaf base
Current Opinion in Plant Biology
34
Growth and development
The maize allele leafbladeless (ragged seedling1) is the first
proposed dorsoventral leaf mutation affecting monocot
leaves [43•]. In keeping with a model wherein lateral leaf
domains are established at the founder-cell stage in grass
leaves, Timmermans et al. [43•] report that this interesting
mutant disrupts dorsoventrality and founder-cell recruitment in maize lateral organs. Severe leafbladeless
phenotypes include radial ‘abaxialized’ leaves, although
the presence of a ligule (an adaxial leaf elaboration, see
Figure 2) on radial leaves might indicate that LEAFBLADELESS is required only for lateral leaf development
and not the establishment of dorsiventrality.
An alternative view of the radialized phantastica mutant
phenotype has been offered by analyses of the orthologous
gene product in maize [34••,35••,44•]. The recessive rough
sheath2 mutation causes ectopic expression of at least three
different knox genes in mutant leaves [44•], and conditions
leaf phenotypes resembling those observed in dominant
neomorphic knox mutants [29,31,44•]. A regulator of knox
gene expression in maize shoots, rough sheath2 is shown to
encode a MYB-like product orthologous to the PHANTASTICA gene product [34••,35••]; however, unlike
phantastica, rough sheath2 does not affect leaf dorsoventrality. Timmermans et al. [34••] suggest that the disparate
phenotypes of these orthologous mutations may be a result
of differences in developmental timing of expression of
these genes, or perhaps different molecular targets of the
gene products in the dicot and monocot shoots. Tsiantis et
al. [35••] prefer a different interpretation. These
researchers suggest that the rough sheath2 and phantastica
genes perform similar roles in leaf development, and the
dissimilar mutant phenotypes simply reflect differences in
maize and dicot leaf morphology (Figure 2). Specifically,
loss of knox gene repression in rough sheath2 mutant maize
leaves causes the acquisition of proximal developmental
fates, such as sheath and ligule/auricle identity (Figure 2),
in distal leaf domains of the blade [35••,45]. Because the
proximal region in dicot leaves is comprised of the radially
symmetrical petiole (Figure 2), however, loss of PHANTASTICA function in Antirrhinum results in a
‘proximalized’ and unifacial lamina. In this light, PHANTASTICA might not be seen to function as a dorsalizing
factor in the leaf at all. Consistent with this alternative
view, phantastica transcripts are not restricted to the dorsal
domain of leaf primordia but are expressed throughout the
young leaf [33••].
Three members of the YABBY gene family of Arabidopsis
display specific, polar expression patterns predicted for
genes that specify dorsoventral identity [46••]. Proposed to
encode overlapping functions, filamentous flower1, yabby2
and yabby3 are expressed in the abaxial domain of young
leaf primordia; moreover, ectopic expression of these
genes promotes the abaxialization of lateral organs. Taken
together these data comprise strong evidence that these
Yabby gene family members are responsible for acquisition
of abaxial cell fate in Arabidopsis [46••].
Conclusions
Recent research into early leaf development has provided
new evidence that founder-cell recruitment is correlated
with the patterned reduction of inhibitory factors and the
relaxation of biophysical stresses in the SAM. Although the
specific factors responsible for the recruitment of leaf
founder cells from meristematic precursors remain
unknown, this process might be mediated via signaling in
and between symplasmic fields in the shoot apex.
Regulatory loci governing the expression patterns of knotted1-like homeobox genes, molecular markers of the
leaf/non-leaf boundary in simple-leafed plants, promise to
generate important clues regarding the mechanisms of
early leaf development. Analyses of the often bizarre leafpatterning mutants are the source of experimental models
in which specific cell types comprising lateral, dorsoventral
and proximal-distal axes of the developing leaf intersect
and interact to assemble a completed organ. The expanded use of genomics technology to study the functions of
orthologous genes during monocot and dicot leaf development, combined with saturation mutagenesis [47]
promises to yield invaluable insight into the evolution of
leaf morphology.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
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6.
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Developmental complexities of simple leaves Scanlon
35
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This paper describes the use of fluorescent-dye loading techniques to reveal
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••
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proposed role as a negative regulator of leaf initiation in maize.
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•
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Describes the expression of the tomato expansin gene LeExp2 at the site of
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phyllotaxis determination proposes a key role for EXPANSINS — proteins
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The authors present a mosaic analysis of Gnarley1, a dominant, gain-of-function mutation in a Knotted1-like homeobox gene. X-ray induced sectors of
nonmutant tissue on mutant tissue support the idea that lateral veins serve
as developmental boundaries and that auricle propagation can be separated from auricle initiation.
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The phantastica gene — which is purported to be required for the establishment of dorsoventrality in Antirrhinum leaves, bracts and petals — is found to
encode a MYB-domain-containing transcription factor expressed in founder
cells and young primordia. Analyses of temperature-sensitive alleles indicates an additional role for PHAN in elaboration of the proximodistal axes of
snapdragon lateral organs.
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maize lateral organ primordia. Science 1999, 284:151-153.
The rough sheath2 gene is cloned in a PCR-based assay to identify the
maize orthologue of phantastica, a leaf-patterning mutation from Antirrhinum.
Despite similar expression pattern, mutations in the orthologous genes result
in dissimilar mutant phenotypes.
35. Tsiantis M, Schneeberger R, Golz JF, Freeling M, Langdale JA: The
•• maize rough sheath2 gene and leaf developmental programs in
monocot and dicot leaves. Science 1999, 284:154-156.
The maize orthologue of the phantastica gene from Antirrhinum is cloned by
transposon tagging. A model for ROUGH SHEATH2 and PHANTASTICA function argues that both genes are involved in negative repression of homeobox
gene expression in lateral organs. Loss-of-function mutations in both rough
sheath2 and phantastica, therefore, result in ‘proximalized’ leaf phenotypes.
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37.
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41. McConnel JR, Barton MK: Leaf polarity and meristem formation in
•
Arabidopsis. Development 1998, 125:2935-2942.
A dominant mutation leads to the adaxialization of Arabidopsis leaves. The
data support a model whereby shoot apical meristem formation is dependent upon signals emanating from adaxial leaf surfaces.
42. Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P,
•• Barton MK: The pinhead/zwille gene acts pleiotropically in
Arabidopsis development and has overlapping functions with the
argonaute1 gene. Development 1999, 126:469-481.
The PINHEAD protein is required for shoot apical meristem formation in
Arabidopsis. Evidence is presented that PINHEAD function defines a developmental domain also comprising the adaxial surface of young leaf primordia, and that this domain is essential for shoot meristem development.
43. Timmermans MCP, Schultes NP, Jankovsky JP, Nelson T:
•
leafbladeless1 is required for dorsoventrality of lateral organs in
maize. Development 1998, 125:2813-2823.
A recessive mutation causing variable reductions in lateral development and
dorsoventrality in maize lateral organs is described and a model for the establishment of maize leaf dorsoventrality during founder cell stages is presented.
36
Growth and development
44. Schneeberger R, Tsiantis M, Freeling M, Langdale JA: The rough
•
sheath2 gene negatively regulates homeobox gene expression
during maize leaf development. Development 1998, 125:2857-2865.
The recessive mutation rough sheath2 induces leaf and shoot developmental abnormalities similar to those reported for dominant Knotted1-like homeodomain mutants. The rough sheath2 phenotype is correlated with ectopic
expression of homeodomain genes in leaves, indicating that rough sheath2
is a negative regulator of Knotted1-like gene expressive in shoots.
45. Muehlbauer GJ, Fowler JE, Freeling M: Sectors expressing the
homeobox gene liguless3 implicate a time dependent mechanism
for cell fate acquisition along the proximal-distal axis.
Development 1997, 124:5097-5106.
46. Siegfried KR, Eshed Y, Baum S, Otsuga D, Drews GN, Bowman J:
•• Members of the YABBY gene family specify abaxial cell fate in
Arabidopsis. Development 1999, 126:4117-4128.
Three members of the YABBY gene family are expressed on the abaxial
domain of lateral organ primordia. The expression domains of these genes
are correspondingly altered in the abaxializing mutant phabulosa, whereas
ectopic expression of two YABBY members confers development of ectopic
abaxial tissue types. These data strongly suggest that the YABBY gene family may have evolved to encode overlapping functions in the specification of
abaxial identity.
47.
Berna G, Robles P, Micol JL: A mutational analysis of leaf
morphogenesis in Arabidopsis thaliana. Genetics 1999, 152:729-742.
Developmental complexities of simple leaves
Michael J Scanlon
Recent papers have explored early events in the development
of simple leaves. Functional compartmentalization of the shoot
apical meristem correlates with distinct fields of cells
connected by plasmodesmata. Molecules important in the
initiation of phyllotactic pattern are described and the
relationship between dorsoventral patterning and lateral leaf
expansion is investigated.
Addresses
3609 Plant Sciences, Botany Department, University of Georgia,
Athens, GA 30602, USA; e-mail: [email protected]
Current Opinion in Plant Biology 2000, 3:31–36
1369-5266/00/$ — see front matter © 2000 Elsevier Science Ltd.
All rights reserved.
Abbreviations
CZ
central zone
knox
knotted1 class of homeobox
PZ
peripheral zone
SAM
shoot apical meristem
Introduction
Amid the vast diversity in plant morphology, no organ contributes more to phenotypic variation than the leaf. Plants
have evolved various spatial arrangements of leaves about
the stem (phyllotaxy), and disparate varieties of leaf size,
shape and complexity. Despite this inherent variability, at
least two developmental characters define most if not all
leaves [1,2]: namely leaves arise from a relatively large
number of progenitor ‘founder cells’ [3] recruited from the
periphery of the shoot apical meristem; leaves are dorsiventrally asymmetrical (bifacial) at their inception.
This review describes recent insights into leaf developmental mechanisms, focusing primarily on investigations
of simple leaves in the monocot maize plant, and in the
dicots Arabidopsis, tobacco and snapdragon (Antirrhinum).
Interested readers are directed to more historically comprehensive reviews [4–6] for discussions of compound leaf
development, and simple leaf development from nonmodel organisms. This review emphasizes newly published
research (from 1998 to present) relevant to the development of morphological diversity between monocot and
dicot leaf forms. Two early stages in the development of
simple leaves are discussed (see also [4,5]). The first stage
is characterized by leaf founder-cell recruitment, wherein
the transition from meristematic identity to leaf identity
occurs. The second stage engenders the expansion of the
founder cells into a young leaf primordium.
Meristem-leaf transition stage
The shoot apical meristems (SAMs) of maize and the dicots
Arabidopsis, tobacco and Antirrhinum exhibit similar patterns
of zonation and structure [7]. Leaf organogenesis occurs in a
lateral region of relatively high mitotic index called the
meristem ‘peripheral zone’ (PZ). The meristem ‘central
zone’ (CZ), characterized by a lower rate of cell division,
replenishes meristematic cells contributed to developing
leaves. The expression profiles of the knotted1 class of
homeobox (knox) genes in maize [8–13], and those of orthologous genes in Arabidopsis [14,15], mirror this pattern of
meristem zonation. Accordingly, knox genes are expressed at
very high levels in the CZ, and are downregulated in the PZ
of the meristem. These data indicate that the downregulation of knox genes might contribute to leaf founder-cell
determination during development of simple leaves.
The pattern and extent of knox downregulation in the
SAM also reflects morphological differences of leaf bases
in monocots and dicots. For example, maize leaves, in
which the leaf bases completely ensheath the circumference of the stem into which they are inserted [1,2], display
knox downregulation that extends from one meristem flank
to the opposite pole ([8,9]; Figure 1). In contrast, the leaf
bases of Arabidopsis exhibit far less spreading around the
stem than those of maize; this phenotype is correlated with
stm1 homeobox downregulation that is markedly more
localized ([15]; Figure 1). The molecular pathway leading
to founder-cell recruitment, and the specific role for knox
genes in this process, remain unknown; however, recent
analyses of symplasmic fields in plant meristems illuminate a route for the channeled movement of proposed
signaling molecules during founder-cell recruitment stages
of leaf morphogenesis [16••,17••].
Symplasmic fields are groups of plant cells united by plasmodesmatal connections. Rinne and van der Schoot [16••]
and Gisel et al. [17••] tracked the movement of fluorescent
dyes into vegetative SAMs in birch and Arabidopsis,
respectively. These studies showed that the PZ and CZ of
the outer meristem layer comprise distinct and separate
symplasmic fields. In the early initiation stages of foundercell recruitment [8,15], however, a transient connection
between the PZ and CZ is established [16••]. Therefore,
signaling molecules might theoretically move between
symplasmic fields and initiate leaf morphogenesis.
Spatial patterning of founder cell recruitment:
phyllotaxy
The geometrically-precise placement of leaves about the
stem — a process that ultimately depends upon the pattern of founder-cell recruitment in the SAM — has long
intrigued experimental botanists [18,19]. Surgical studies
demonstrated that the close proximity of existing leaf primordia inhibits the initiation of new leaves from the SAM
[20]. The nature of this purported inhibitory factor, albeit
chemical or physical or both, has been the subject of
botanical debate.
32
Growth and development
seedlings, and is correlated with an abnormally large meristem. Reversion of the mutant phenotype to normal
phyllotaxy is common in upper leaves, accompanied by
concomitant restoration of normal meristem size. Jackson
and Hake [23•] note that a correlation between SAM size
and change in phyllotaxy is characteristic of dicot species
that exhibit disparate phyllotaxies during their life cycle,
although cause and effect can not as yet be determined.
Figure 1
(a)
maize
Maize
maize
(b)
Dicots
Founder cell stage
Primordial stage
Current Opinion in Plant Biology
Early development of simple leaves. Model for stages in early leaf
development in (a) maize and (b) typical dicots. In (a) maize, founder
cell (darkly shaded) recruitment begins on one meristematic flank and
expands laterally to completely surround the SAM (lightly shaded). The
hooded primordium that subsequently emerges from the SAM displays
dorsoventral asymmetry and envelops the SAM because the lateral
domains of the leaf blade and sheath are established during founder
cell recruitment. In (b) dicots, however, founder cell recruitment does
not proceed extensively around the SAM. The peg-like primordium that
emerges, although dorsoventrally asymmetrical, contains a mildly
expanded leaf base but does not have a prominent lamina. Interaction
of dorsal and ventral domains in the distal regions of the primordium
induces expansive growth of the dicot lamina (striped). The petiole
forms from the unexpanded region of the primordium, between the
proximal leaf base and the distal lamina.
Recent research into the maize mutation terminal ear1 has
shed new light on the question of phyllotaxis. Veit et al.
[21••] found that the terminal ear1 gene encodes a mRNA
binding protein that is expressed in a horseshoe configuration subtending leaf primordia. The open end of the
horseshoe corresponds to the position of young primordia,
including the founder cells of the incipient leaf prior to any
visible morphogenesis. These researchers postulate that
the TERMINAL EAR protein might function to regulate
phyllotaxis in maize shoots via inhibition of leaf initiation
within its expression domain. Consistent with this prediction, terminal ear mutants produce superfluous numbers of
leaves in an disorganized pattern. Characterization of the,
as yet unknown, target(s) of the TERMINAL EAR protein promises to divulge crucial information to our
understanding of the earliest events in leaf development.
Another maize mutation impacting phyllotaxy is abphyl1
(aberrant phyllotaxy) [22,23•]. This intriguing mutant displays dechussate (two leaves per node) phyllotaxis, which
is common to many dicot plants. Normal maize, like all
grasses, produces vegetative leaves in an alternate (a single
leaf per node) phyllotaxis. The dechussate phenotype is
especially pronounced in abphyl mutant embryos and
A direct role for biophysics in leaf initiation is championed
by researchers studying the interaction of externally
administered EXPANSINS and shoot meristems
([24,25,26••]; see also review by Cosgrove, pp 73–78). In
these studies, the placement of beads soaked with
EXPANSINS — proteins that increase extensibility of
plant cell walls — induced leaf primordial development
from tomato meristems. The EXPANSIN-induced organs
satisfy several leaf developmental criteria, including
dorsoventrality and an influence on the positioning of
incipient leaves. In addition, Reinhardt et al. [26••] show
that the expansin gene LeExp18 is expressed in tomato
SAMs at the site of incipient leaf formation. Nonetheless,
the primordia that emerge from EXPANSIN-treated
meristems do not complete the full program of leaf morphogenesis, but cease development in early primordial
stages [24,25]. The abortion of leaf development is
ascribed to the external application of EXPANSINS,
which are normally produced endogenously [25].
Kuhlenmeier and colleagues [24,25,26••] argue that their
results support a biophysical model for leaf development
[27,28], in which meristematic stresses result in localized
buckling of the SAM and subsequent initiation of leaf
development. In this view, EXPANSIN-induced cell wall
loosening causes bulging of the meristem, which in turn
elicits morphogenesis. Additional data are required to clarify whether EXPANSIN accumulation is an initiator of, or
merely a later response to leaf morphogenetic programs.
The progression from founder cells to a leaf
primordium
The knox gene family [9,11] was first identified by dominant
mutations that cause ectopic expression of these meristematic genes in developing leaf primordia [8,10,12,13,29,30].
Although all of the dominant Knox mutations result in similar transformations of distal blade tissue into proximal
sheath-like tissue, a fascinating aspect of the Knox mutants
is the leaf domain-specific perturbations associated with
individual Knox mutant phenotypes (reviewed in [31]). Two
newly-cloned members of this mutational class are gnarley1
[12,32•] and liguless3 (lg3) [13], each characterized by dominant regulatory mutations that transform leaf cell/tissue
identities. Consistent with previous analyses of other Knox
mutations, lg3 is normally expressed in shoot apices, whereas Gnarley1 and Lg3 mutations result in the ectopic
accumulation of KNOX proteins in leaf primordia. Clonal
analyses indicate that the Gnarley1 mutant gene-product is
cell autonomous in the lateral dimension of the leaf, but
non-cell autonomous in the transverse dimension [32•].
Developmental complexities of simple leaves Scanlon
An exciting development in knox gene research is the identification of genes regulating knox gene expression
[33••–35••,36]. The phantastica gene encodes a member of
a small subfamily of MYB-related transcription factors
[33••] required for the proper regulation of a knox gene in
Antirrhinum [34••,35••]. Waites et al. [33••] show that phantastica is transcribed in developing lateral organs and,
therefore, represents the first molecular marker found to
be expressed in leaf founder cells.
Leaf dorsoventrality and lateral leaf expansion
Hudson and colleagues [33••,36] describe phantastica
mutant leaves as defective in several aspects of leaf development, including lateral expansion of the lamina,
dorsoventrality and proximal-distal patterning. A severe
phenotype of phantastica mutants is a radialized leaf, interpreted as lacking dorsal leaf identity [36]. These
researchers propose that PHANTASTICA promotes dorsal
leaf identity, which is required to initiate lateral growth
[33••,36]. This model is based upon the premise that dicot
leaves, which emerge from the meristem as peg-shaped
buttresses [2–5,7], undergo lateral expansion of the lamina
during primordial developmental stages (Figure 1). In this
view, dorsal (adaxial) and ventral (abaxial) leaf identity is
established at the founder-cell stage. Subsequently, the
juxtaposition of dorsal and ventral domains at the margins
of the dicot leaf primordium results in the elaboration of
leaf blade (lamina) development along a new lateral axis.
In contrast, the leaf blade domains of monocot grasses are
established prior to the primordial stage, as illustrated by the
flattened stem-encircling primordia of newly initiated grass
33
leaves ([1–3]; Figure 1). Analyses of the mutant narrow sheath,
which conditions the pre-primordial deletion of lateral leaf
domains [37,38], also support a model for founder-cell-staged
recruitment of leaf blade domains in maize.
Interpretations of the phenotypes of several new leaf pattern
mutants are inspired from the proposed model for PHANTASTICA function [33••], wherein lateral leaf expansion
requires the interaction of dorsal (adaxial) and ventral (abaxial) identities. Analyses of the bladeless tobacco leaf mutant
lam1 [39,40] demonstrate that the LAM1 ‘dorsalizing factor’
is required in L3-derived layers of the shoot (i.e. the innermost layers of the SAM) in order to establish dorsal
differentiation and lateral growth in leaf primordia.
The dicot model for lateral leaf expansion presupposes
that ventralizing, as well as dorsalizing mutations, should
likewise condition radialized leaves devoid of lamina. As
predicted, the dominant mutation phabulosa1 produces
dorsalized (adaxialized) leaves that often display radial
phenotypes and fail to develop leaf blades [41•]. A striking
phenotype observed in severe phabulosa mutants is the
development of ectopic meristems surrounding the bases
of adaxialized leaves. This phenotype, and the adaxialized
expression pattern of the putative meristem-forming factor
PINHEAD [42••], strongly suggests that the adaxial leaf
domain renders competency to develop SAMs. McConnell
and Barton [41•] propose that PHABULOSA may be
required to specify adaxial cell fate, although these predictions are tempered by the inherent difficulties in
discerning the wild-type function of genes identified by
dominant, gain-of-function mutations.
Figure 2
Morphology of simple leaves. Schematic
representations of leaf morphology in
(a) maize and (b) ‘typical’ dicots such as
Arabidopsis, tobacco, and Antirrhinum.
(a) Maize leaves have an expansive leaf base
that encircles the stem completely. The straplike leaf is comprised of distinct regions along
the proximal-distal axis: these include the
sheath, which wraps around the stem; the
epidermally derived ligule fringe; the wedgeshaped auricle, which acts as a hinge; and the
lamina (blade), which displays a prominent
midrib. (b) Dicot simple leaves typically have a
leaf base that expands only partially around
the stem. The leaf base may bear
appendages, called stipules. The proximal
petiole is radially symmetrical, whereas the
distal lamina is dorsoventrally flattened.
(a)
Midrib/midvein
(b)
Midrib/midvein
Lamina/blade
Lamina/blade
Auricle
Ligule
Sheath
Leaf base
Petiole
Stipules
Leaf base
Current Opinion in Plant Biology
34
Growth and development
The maize allele leafbladeless (ragged seedling1) is the first
proposed dorsoventral leaf mutation affecting monocot
leaves [43•]. In keeping with a model wherein lateral leaf
domains are established at the founder-cell stage in grass
leaves, Timmermans et al. [43•] report that this interesting
mutant disrupts dorsoventrality and founder-cell recruitment in maize lateral organs. Severe leafbladeless
phenotypes include radial ‘abaxialized’ leaves, although
the presence of a ligule (an adaxial leaf elaboration, see
Figure 2) on radial leaves might indicate that LEAFBLADELESS is required only for lateral leaf development
and not the establishment of dorsiventrality.
An alternative view of the radialized phantastica mutant
phenotype has been offered by analyses of the orthologous
gene product in maize [34••,35••,44•]. The recessive rough
sheath2 mutation causes ectopic expression of at least three
different knox genes in mutant leaves [44•], and conditions
leaf phenotypes resembling those observed in dominant
neomorphic knox mutants [29,31,44•]. A regulator of knox
gene expression in maize shoots, rough sheath2 is shown to
encode a MYB-like product orthologous to the PHANTASTICA gene product [34••,35••]; however, unlike
phantastica, rough sheath2 does not affect leaf dorsoventrality. Timmermans et al. [34••] suggest that the disparate
phenotypes of these orthologous mutations may be a result
of differences in developmental timing of expression of
these genes, or perhaps different molecular targets of the
gene products in the dicot and monocot shoots. Tsiantis et
al. [35••] prefer a different interpretation. These
researchers suggest that the rough sheath2 and phantastica
genes perform similar roles in leaf development, and the
dissimilar mutant phenotypes simply reflect differences in
maize and dicot leaf morphology (Figure 2). Specifically,
loss of knox gene repression in rough sheath2 mutant maize
leaves causes the acquisition of proximal developmental
fates, such as sheath and ligule/auricle identity (Figure 2),
in distal leaf domains of the blade [35••,45]. Because the
proximal region in dicot leaves is comprised of the radially
symmetrical petiole (Figure 2), however, loss of PHANTASTICA function in Antirrhinum results in a
‘proximalized’ and unifacial lamina. In this light, PHANTASTICA might not be seen to function as a dorsalizing
factor in the leaf at all. Consistent with this alternative
view, phantastica transcripts are not restricted to the dorsal
domain of leaf primordia but are expressed throughout the
young leaf [33••].
Three members of the YABBY gene family of Arabidopsis
display specific, polar expression patterns predicted for
genes that specify dorsoventral identity [46••]. Proposed to
encode overlapping functions, filamentous flower1, yabby2
and yabby3 are expressed in the abaxial domain of young
leaf primordia; moreover, ectopic expression of these
genes promotes the abaxialization of lateral organs. Taken
together these data comprise strong evidence that these
Yabby gene family members are responsible for acquisition
of abaxial cell fate in Arabidopsis [46••].
Conclusions
Recent research into early leaf development has provided
new evidence that founder-cell recruitment is correlated
with the patterned reduction of inhibitory factors and the
relaxation of biophysical stresses in the SAM. Although the
specific factors responsible for the recruitment of leaf
founder cells from meristematic precursors remain
unknown, this process might be mediated via signaling in
and between symplasmic fields in the shoot apex.
Regulatory loci governing the expression patterns of knotted1-like homeobox genes, molecular markers of the
leaf/non-leaf boundary in simple-leafed plants, promise to
generate important clues regarding the mechanisms of
early leaf development. Analyses of the often bizarre leafpatterning mutants are the source of experimental models
in which specific cell types comprising lateral, dorsoventral
and proximal-distal axes of the developing leaf intersect
and interact to assemble a completed organ. The expanded use of genomics technology to study the functions of
orthologous genes during monocot and dicot leaf development, combined with saturation mutagenesis [47]
promises to yield invaluable insight into the evolution of
leaf morphology.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
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41. McConnel JR, Barton MK: Leaf polarity and meristem formation in
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Arabidopsis. Development 1998, 125:2935-2942.
A dominant mutation leads to the adaxialization of Arabidopsis leaves. The
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42. Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P,
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The PINHEAD protein is required for shoot apical meristem formation in
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43. Timmermans MCP, Schultes NP, Jankovsky JP, Nelson T:
•
leafbladeless1 is required for dorsoventrality of lateral organs in
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A recessive mutation causing variable reductions in lateral development and
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36
Growth and development
44. Schneeberger R, Tsiantis M, Freeling M, Langdale JA: The rough
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sheath2 gene negatively regulates homeobox gene expression
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The recessive mutation rough sheath2 induces leaf and shoot developmental abnormalities similar to those reported for dominant Knotted1-like homeodomain mutants. The rough sheath2 phenotype is correlated with ectopic
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•• Members of the YABBY gene family specify abaxial cell fate in
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Three members of the YABBY gene family are expressed on the abaxial
domain of lateral organ primordia. The expression domains of these genes
are correspondingly altered in the abaxializing mutant phabulosa, whereas
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