Download Networks in leaf development

Networks in leaf development
Mary E Byrne
Shoots are characterized by indeterminate growth resulting
from divisions of undifferentiated cells in the central region of
the shoot apical meristem. These cells give rise to peripheral
derivatives from which lateral organ initials are recruited.
During initial stages of cell recruitment, the three-dimensional
form of lateral organs is specified. Lateral organs such as
leaves develop and differentiate along proximodistal
(base-to-tip), dorsoventral (top-to bottom) and mediolateral
(middle-to-margin) planes. Current findings are refining our
knowledge of the genes and genetic interactions that
regulate these early processes and are providing a picture
of how these pathways may contribute to variation in leaf
form.
Addresses
Department of Crop Genetics, John Innes Centre, Norwich Research
Park, Norwich NR4 7UH, UK
Corresponding author: Byrne, Mary E ([email protected])
Current Opinion in Plant Biology 2005, 8:59–66
This review comes from a themed issue on
Growth and development
Edited by Liam Dolan and Michael Freeling
Available online 25th November 2004
1369-5266/$ – see front matter
# 2005 Elsevier Ltd. All rights reserved.
cells from the peripheral region of the shoot apical meristem (SAM). The extent of founder-cell recruitment from
the flanks of the SAM varies between species, with
Arabidopsis and maize representing two developmental
extremes (Figure 1). Development along adaxial–abaxial
(dorsoventral), proximal–distal, and midvein–margin
(mediolateral) planes establishes leaf polarity (Figures 1
and 2). After this ground plan is set, continued cell
division and expansion further contribute to leaf shape
and form. At the same time, there is differentiation of
specific cell and tissue types, such as outer layer epidermal cells, inner photosynthetic mesophyll and vasculature. Together, these processes establish the specialized
function of the leaf as the main light-harvesting organ of
the plant.
Leaf initiation and patterning has long been the subject of
experimental and theoretical work. Recent studies are
building on results of classic work and are now defining
molecular networks that are involved in many different
aspects of leaf development. This review aims only to
spotlight several of the more recent studies that have
contributed to our understanding of the mechanisms that
regulate leaf initiation, ground-plan patterning and specification of final form. Several recent reviews provide
further reading [1–3].
Cell recruitment
Introduction
Leaf development initiates by recruitment of cells from
the peripheral region of the SAM. Although the extent of
founder-cell recruitment from the flanks of the SAM
varies between species (Figure 1; [4–6]), genetic programs that control this early stage of leaf development
appear to be conserved. For example, founder-cell
recruitment in both Arabidopsis and maize is intimately
linked with downregulation of KNOX homeobox transcription factors [3]. Auxin could be one regulator of
this early event as chemical inhibition of polar auxin
transport results in failure to downregulate KNOX
expression in founder cells [7]. However, in Arabidopsis,
PIN-FORMED1, a gene necessary for polar auxin transport in the SAM, is not required for downregulation of
KNOX genes in founder cells [8,9]. Furthermore, in
maize, ectopic expression of KNOX genes disrupts polar
auxin transport and inhibition of polar auxin transport
mimics the effects of KNOX gene overexpression [7,10].
Potentially, there are mutual inhibitory interactions
between KNOX genes and auxin transport in the SAM.
Leaves are the fundamental lateral appendage of land
plants. The initiation and ground-plan patterning of
leaves is a multistage process of interdependent events.
Leaf primordia are initiated by recruitment of founder
Recent work on the maize narrow sheath (ns) mutants has
added to this picture. ns1 and ns2 are duplicate genes that
are required for KNOX downregulation specifically in
DOI 10.1016/j.pbi.2004.11.009
Abbreviations
AGO1
ARGONAUTE1
AS1
ASYMMETRIC LEAVES1
CIN
CINCINNATA
FIL
FILAMENTOUS FLOWER
GA
gibberellic acid
GRAM GRAMINAFOLIA
JAG
JAGGED
KAN
KANADI
ns
narrow sheath
PHAN PHANTASTICA
PHB
PHABULOSA
PHV
PHAVOLUTA
PRS
PRESSED FLOWER
REV
REVOLUTA
rs2
rough sheath2
SAM
shoot apical meristem
yab3
yabby3
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Current Opinion in Plant Biology 2005, 8:59–66
60 Growth and development
Figure 1
tions primarily affect floral organ development, but prs
mutants also lack stipules that are normally found at the
margins and base of the Arabidopsis leaf (Figure 1a;
[12,13]). Therefore, like ns mutants in maize, prs mutants
are disrupted in the specification of lateral and proximal
features of the leaf. Consistent with a requirement for
regional specific founder cell recruitment, ns and PRS are
both expressed in two lateral foci in the peripheral region
of the SAM (Figure 3).
Dorsoventrality and lamina outgrowth
Development at the plant shoot apex. (a) Arabidopsis and (b) maize
SAM and developing leaf primordia. In Arabidopsis, primordia are
established by recruitment of cells from a limited region on the
flanks of the SAM. In maize, cells from around the circumference
of the SAM are recruited into the developing primordia. Young
primordia grow out from the SAM establishing proximodistal
(base-to-tip) polarity. Differential development of the side of the leaf
closest to the SAM (adaxial) compared with the side away from the
SAM (abaxial) establishes dorsoventral polarity. Mediolateral
polarity is evident by the formation of lateral stipules in Arabidopsis
and midvein-margin regions in maize.
founder cells that specify the lateral domain of the leaf
[11]. Leaves that are mutant for ns1 and ns2 are narrower
than wildtype leaves but only in the proximal region of
the leaf. The ns genes encode WUSCHEL-related
homeobox transcription factors and are related to
PRESSED FLOWER (PRS) in Arabidopsis [12]. prs muta-
It is now well established that a dorsoventrally flattened
lamina requires adjacent adaxial and abaxial leaf domains
[1,14]. Loss of either the adaxial or abaxial domain results
in partial or complete radialisation of the leaf.
Adaxial identity in Arabidopsis is specified by the class III
HD-ZIP family genes PHABULOSA (PHB), PHAVOLUTA (PHV) and REVOLUTA (REV) [15,16,17,18,19].
Dominant gain-of-function mutants have adaxial leaves.
Loss of function of any one gene in this family has little
effect on leaf development. When combined, however,
mutations in all three genes results in radial abaxial
leaves, a phenotype that is complementary to the dominant mutant phenotypes [15]. Conservation of the function of this gene family is reflected in mutations in other
species. Thus, dominant mutations in rolled leaf1, the
maize orthologue of REV, and in NSPHAVOLUTA, a
tobacco orthologue of PHV, also result in leaf polarity
defects with gain of adaxial features on the abaxial side of
the leaf [20,21]. Consistent with a role in determining
leaf polarity, the expression of this gene family is confined
Figure 2
Leaf polarity. The adaxial side of the leaves of (a) Arabidopsis and (b) maize, indicating the proximal and distal ends, which define the
proximodistal plane, and the midvein and margin, which define the mediolateral plane. In Arabidopsis, the proximal region of the vegetative
rosette leaf forms a petiole and the lamina or leaf blade develops more distally. In maize, a sheath develops in the proximal region of the leaf,
and the blade develops in the distal region of the leaf. The sheath and blade are separated by the auricle and ligule.
Current Opinion in Plant Biology 2005, 8:59–66
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Networks in leaf development Byrne 61
Figure 3
Adaxial–abaxial polarity. Gene expression patterns in the shoot apex of (a) Arabidopsis and (b) maize. PHB/PHV/REV genes (red) are expressed
in the SAM. In Arabidopsis, these genes are expressed throughout the initiating primordium and their expression becomes confined to the
adaxial domain upon further development of the primordium. In maize, the expression of the REV-related gene rolled leaf1 is adaxial in initiating
and young primordia, and becomes confined to the margins later in development. Regulatory microRNAs, miRNA165/166 (yellow), are expressed
on the abaxial side of the leaf in a domain that is complementary to the expression zone of target PHB/PHV/REV genes. The expression pattern
of PRS in Arabidopsis and ns in maize is confined to a lateral region of the SAM (purple) and to the margins of leaf primordia (not indicated).
The expression domain of the KNOX gene SHOOT MERISTEMLESS (blue) in Arabidopsis is also indicated. P1 to P5 indicate successive leaf
primordia. M, meristem.
to the adaxial domain of the leaf (Figure 3). Exclusion
from the abaxial domain is mediated, at least in part,
by miRNA-mediated posttranscriptional cleavage. All
PHB, PHV, and REV genes have a sequence that is
complementary to miR165 and miR166 [22,23]. Dominant mutations in PHB/PHV/REV genes all disrupt the
miRNA-binding site [15,19,20,21]. Furthermore, in
Arabidopsis and maize, miR165 and miR166 are expressed
on the abaxial side of the leaf, a domain opposite that of
PHB/PHV/REV target genes [20,24]. Spatial regulation of these target genes is necessary for the establishment of leaf polarity, but regulation of miR165 function
also appears to be crucial for leaf patterning [24].
Mutations in ARGONAUTE1 (AGO1), a key component
in RNA interference (RNAi)-mediated posttranscriptional gene regulation (see Kidner and Martienssen, this
issue), result in ectopic expression of PHB and adaxialisation of the leaf.
Abaxial cell fate is specified by the KANADI (KAN) genes
[15,25,26,27,28]. Members of this family are expressed
in the abaxial domain of the leaf. KAN genes are members
of the GARP family of transcription factors, which
includes four closely related genes in Arabidopsis. Mutations in individual family members only have subtle
effects on leaf polarity, whereas combined mutations
reveal a role for KAN genes in abaxial specification
[26,27,29]. The leaves of kan1 kan2 mutants are partially
adaxialised, and kan1 kan2 kan3 mutants display more
complete adaxialisation. KAN and PHB/PHV/REV genes
appear to establish an abaxial–adaxial leaf by mutual
suppression [29]. These two gene families also show polar
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expression in vasculature [15,20]. KAN genes are expressed in the abaxial phloem and PHB genes are expressed in
the adaxial xylem, and both gene families are required for
the polar development of vasculature. It is possible that
genes that are required for polar vascular development
have been co-opted during evolution of the leaf [1].
Another class of leaf patterning genes are members of the
YABBY family. Of the five YABBY genes in Arabidopsis,
three are expressed in leaves [28,30,31]. Deletion analysis
of the promoter of one YABBY gene, FILAMENTOUS
FLOWER (FIL), has revealed independent cis-acting
sequences that promote the expression of FIL throughout
the leaf primordium and repress FIL expression on the
adaxial side of the leaf primordium. This demonstrates
that FIL is actively excluded from the adaxial domain
[32]. The role of YABBY genes in abaxial specification is
not clear, however, because loss-of-function mutants do
not have obvious dorsoventral defects. This may be due,
in part, to redundancy within the YABBY gene family and
also with KAN genes. For instance, there are no obvious
polarity defects in the fil and yabby3 (yab3) double mutant,
but abaxial fate is compromised in this double mutant
when KAN activity is reduced [26,30]. These two YABBY
genes have further interactions with KAN genes. Double
kan1 kan2 mutants have ectopic lamina outgrowths on the
abaxial side of the leaf. It is not clear what preconditions
lamina outgrowth as this phenotype is not always evident
in backgrounds in which abaxial fate is disrupted. However, ectopic outgrowths are dependent on FIL and
YAB3, supporting a role for YABBY genes in lamina
outgrowth. GRAMINAFOLIA (GRAM) in Antirrhinum is
Current Opinion in Plant Biology 2005, 8:59–66
62 Growth and development
closely related to FIL and YAB3 [33]. As with YABBY
genes in Arabidopsis, GRAM is expressed in the abaxial
domain of the leaf. However, genetic interactions indicate that GRAM may regulate leaf polarity by repressing
adaxial fate in the abaxial domain of the leaf. Furthermore, GRAM appears to promote adaxial fate in a noncell-autonomous manner. This suggests that the role of
YABBY genes in dorsoventral polarity differs between
species, although it is also possible that differences in
loss-of-function phenotypes of different species reflect
divergent levels of redundancy.
PHANTASTICA genes and leaf patterning
Leaf patterning can be altered by the ectopic expression
of class I KNOX genes (reviewed in [3,34]). Typically,
these genes are expressed in the SAM and downregulated
in leaf primordia. The myb domain transcription factors
PHANTASTICA (PHAN) in Antirrhinum, rough sheath2
(rs2) in maize and ASYMMETRIC LEAVES1 (AS1) in
Arabidopsis are key negative regulators of KNOX gene
expression in leaves [35–38]. The sequence identities and
expression patterns of these genes clearly indicate that
they form an orthologous gene family. The mutant phenotype in each species is not immediately comparable,
however, leading to disparate interpretations of the
defect. In phan mutants, early leaves have patches of
abaxial tissue associated with ectopic lamina outgrowth
on their adaxial leaf surface. The lamina of later leaves
becomes progressively restricted to the distal tip of the
leaf. In the most extreme form, the leaf is radial and
abaxial [14]. PHAN is therefore required for leaf dorsoventral patterning. In comparison, as1 leaves are shorter
and rounder than wildtype leaves, have occasional lobes
and show no obvious dorsoventral defects [35,39,40],
although under some conditions the base of the petiole
may be radial [41,42]. Despite these differences, the
maize gene rs2 rescues as1, indicating that function is
conserved within this gene family.
Overexpression of either AS1 or rs2 in Arabidopsis does
not result in dorsoventral defects [42,43]. This is in
contrast to overexpression of the LOB domain gene
AS2, which is a protein partner of AS1 [42,44]. Mutations
in AS2 result in leaf patterning defects that are comparable to those of as1, and in growth-condition-dependant
radialisation of the petiole base [39,40,42,45]. However,
overexpression of AS2 results in dorsoventral defects that
are consistent with adaxialisation of the leaf [42,46].
Lamina outgrowths, similar to those of kan1 kan2
mutants, occur on the abaxial side of leaf of AS2-overexpressing lines. This phenotype is dependant on AS1.
Together, the data indicate that AS1 and AS2 have at least
retained the potential to pattern dorsoventral development and act by repression of abaxial fate in the adaxial
domain of the leaf [46]. If this is the case, adaxial
specification in Arabidopsis is determined by pathways
that are redundant with AS1.
Current Opinion in Plant Biology 2005, 8:59–66
The phenotype of the maize rs2 mutant sheds a different
light on the role of PHAN genes in leaf development. In
rs2 mutants, proximal features of the sheath, ligule and
auricle (Figure 2) are displaced distally into the leaf blade
[47]. rs2, therefore, is defective in proximodistal patterning. On the basis of the maize phenotype, an alternative
interpretation of the phan phenotype proposed that radialisation of the Antirrhinum leaf is due to transformation of
distal lamina into tissue that has petiole or stem features
[37]. A recent report describing the effects of reduced
NSPHAN in tobacco revisits this interpretation [48]. The
upper leaves of plants with reduced NSPHAN expression
are similar to those of phan mutants, with leaf lamina
being confined to the distal tip of the leaf. More proximal
regions develop dorsoventrality but, as in the petiole,
there is no leaf lamina. The tobacco leaves are radial only
at the base of the leaf. Surprisingly, the radial region has
phloem surrounding xylem, a morphology that is indicative of abaxialisation, but the expression of NSPHB, a
marker for adaxial fate, remains on the adaxial side of the
leaf. This suggests that the radial leaves maintain some
adaxial features. Thus, reducing NSPHAN levels potentially disrupts proximodistal development, with proximal
features of stem and petiole being displaced distally along
the leaf base-to-tip axis.
The lower leaves of antisense NSPHAN plants have
adaxial ectopic lamina outgrowths. Unlike those of phan
mutants, these outgrowths are not associated with obvious
dorsoventral defects. Instead, the lamina outgrowths of
antisense NSPHAN plants may be associated with
delayed maturation or indeterminacy in the leaf caused
by misexpression of KNOX genes. Consistent with this
idea, ectopic lamina is suppressed by application of
gibberellic acid (GA), a hormone whose function is negatively regulated by KNOX genes [48,49,50]. Misregulation of KNOX genes in simple leaved species is typically
associated with ectopic shoots. However, reducing GA
levels in a background in which KNOX genes are ectopically expressed can generate ectopic callus, lamina or
shoots on the leaf [49]. Thus, the formation of shoot as
opposed to leaf may be determined by the relative
temporal and spatial levels of KNOX genes and GA.
Interestingly the tomato PHAN orthologue, LePHAN, is
expressed in the SAM and on the adaxial side of leaf
primordia [51,52]. Decreased LePHAN expression
results in leaves that have various degrees of reduced
lamina development. The proximal region may be radialised and the distal lamina can develop as a trumpet or as
leaflets at the tip of the radial petiole. Leaflets may be
confined to the abaxial side of the petiole or be arranged
around the entire petiole circumference, phenotypes that
are comparable to non-peltate and peltate palmate leaves,
respectively. LePHAN antisense phenotypes are correlated with the expression of LePHAN being progressively
confined to the distal tip of the leaf. Furthermore, the
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Networks in leaf development Byrne 63
expression domain of PHAN in a range of species that
have compound leaves correlates with the type of compound leaf, whether pinnate, palmate or peltate-palmate.
Convergent evolutionary changes in the expression of
PHAN may be responsible for phenotypic variation in
compound leaf species. Equally likely, PHAN expression
could be a consequence of developmental variation
mediated by one or more alternative regulators.
Elaboration of the leaf lamina
Subsequent to events that direct leaf polarity, the control
of final leaf shape and size continues by coordinated
regulation of cell division and expansion along the length
and width of the leaf [53]. Cessation of cell division and
differentiation proceeds along the proximodistal plane
from leaf tip to base (Figure 2). In the dorsoventral plane,
continued divisions in the adaxial mesophyll differentiate
the adaxial pallisade from the abaxial spongy mesophyll
[54,55,56]. Another dimension of control is provided by
the relative rates of cell division across the mediolateral
plane of the developing leaf. Cell divisions cease in the
mid-region of the leaf slightly ahead of divisions at the
margins. Maintaining this pattern of cell division is crucial
for the development of a flat leaf surface, as highlighted
by mutations in CINCINNATA (CIN) in Antirrhinum
[55,57]. In cin mutants, the leaf margin is rumpled as
a result of the slower arrest of cell divisions at the leaf
margins relative to the middle of the leaf. A comparable
phenotype is seen in jaw-D mutants in Arabidopsis [58].
In this case, overexpression of a miRNA results in the
downregulation of target genes belonging to the TCP
family of transcription factors, which are closely related to
CIN in Antirrhinum [58,59]. Ubiquitous expression of
TCPs partially suppresses the jaw-D mutant phenotype,
and the degree of rescue is dependent on the level of target
gene expression. This suggests a dose-dependent interaction between the miRNA and its direct target. Interactions
such as these may serve to fine-tune development.
Another gene that is involved in specifying final leaf
shape is JAGGED (JAG) [60,61]. In jag mutants, the
leaves are more predominantly serrated than those in the
wildtype and the distal tips of floral organs are jagged,
absent or reduced. Misexpression of JAG results in ectopic leaf-like lamina outgrowths in proximal leaf regions
and on the stem. The development of blade on the
petiole is reminiscent of the phenotypes of recessive
blade on petiole (bop) mutants and of dominant mutations
that affect the LEAFY PETIOLE gene [62–64]. In one
sense, these mutations may represent the disruption of
proximodistal specification, with transformation of proximal features to a more distal fate. The expression of a cell
division marker is decreased in jag mutant leaves, however, indicating that JAG is required to prevent premature
cell differentiation. In this respect, JAG and JAW may
specify opposing but complementary functions in lamina
outgrowth.
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Conclusions
Early surgical experiments demonstrated that the separation of an initiating primordium from the SAM resulted in
a radial leaf that has abaxial features [65,66]. Subsequently, the notion of interdependence of SAM function
and leaf patterning has been reinforced by studies defining genes and genetic interactions that are essential to
these processes. In simple leaves, this involves turning off
the KNOX genes that maintain meristem indeterminacy.
KNOX repression is maintained during leaf development
by several different gene classes, including PHAN, BOP,
and YABBY genes, all apparently acting in distinct pathways. As cells are recruited into the initiating leaf primordia, adaxial PHB family class III HD-ZIP genes
repress abaxial KAN genes. Abaxial fate is either established or reinforced by KAN and miRNA-mediated
repression of PHB family genes. Layered onto this information, YABBY genes contribute to abaxial fate as well as
to mediolateral outgrowth of the leaf lamina. In addition
to specification of dorsoventral fate, PHB and KAN family
genes are required for correct patterning of polar vascular
development. Furthermore, PHB family genes and regulation of the corresponding miRNA are required for
SAM function, potentially reflecting polar centralperipheral development along the main axis of the shoot
([65,66]; see del Mar Castellano and Sablowski, this
issue). Thus, this shared genetic pathway can be seen
as a reflection of a common developmental theme.
Although positional information in the developing primordium depends on contact with or signalling from the
SAM, the nature of this signal is still to be determined.
Suggested candidates are regulators of adaxial fate and
may be either a miRNA or a sterol ligand that targets the
PHB gene family [15,16,20,24]. Although some genes
that specify dorsoventrality also affect other planes of leaf
development, our understanding of the mechanisms that
regulate proximodistal outgrowth and bilateral symmetry
is limited. Flexibility in these pathways is likely to contribute to the diversity of leaf form.
Acknowledgements
I thank Cathie Martin and Robert Sablowski for comments on the
manuscript. I apologise to those whose work I failed to address in this
review because of lack of space.
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of special interest
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Current Opinion in Plant Biology 2005, 8:59–66
66 Growth and development
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features of the Arabidopsis inflorescence.
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Current Opinion in Plant Biology 2005, 8:59–66
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