Section of Plant Biology, University of California, 1 Shields Avenue, Davis, CA 95616, USA
* Author for correspondence (e-mail: nrsinha{at}ucdavis.edu)
SUMMARY
The leaves of seed plants can be classified as being either simple or compound according to their shape. Two hypotheses address the homology between simple and compound leaves, which equate either individual leaflets of compound leaves with simple leaves or the entire compound leaf with a simple leaf. Here we discuss the genes that function in simple and compound leaf development, such as KNOX1 genes, including how they interact with growth hormones to link growth regulation and development to cause changes in leaf complexity. Studies of transcription factors that control leaf development, their downstream targets, and how these targets are regulated are areas of inquiry that should increase our understanding of how leaf complexity is regulated and how it evolved through time.
Introduction
The major light gathering organ in most plants is the leaf. Evolution has produced a variety of leaves with different shapes, sizes and arrangements that reflect the diverse conditions that plants grow in. Recently, significant progress has been made in understanding the molecular mechanisms that regulate leaf development in a few model plant species. This has been achieved by combining careful morphological observations and traditional genetic analyses with advances in molecular biology, such as genetic transformation, and with information from completed genome projects. The current challenge is to explore whether the regulatory mechanisms that control leaf development in model species have been conserved in non-model species and how these regulatory mechanisms have evolved to produce various leaf forms.
The leaves of seed plants can be classified as being either simple or
compound according to their degree of complexity (see
Box 1). Two hypotheses have
been proposed to explain the homology of simple and compound leaves. The first
hypothesis equates individual leaflets of compound leaves with simple leaves.
In this model, compound leaves are seen as partially indeterminate structures
that share properties with both shoots and leaves
(Fig. 1A) (Sattler and Rutishauser,
1992). The second hypothesis suggests that the entire compound
leaf is equivalent to a simple leaf and that leaflets arise by subdivisions of
a simple blade (Fig. 1B) (Kaplan, 1975
). Viewed in this
way, leaf shape is seen as a continuum that ranges from simple leaves with
entire margins, to serrated, lobed, or compound leaves. Both hypotheses can be
used to guide investigators as to which genes might regulate compound leaf
development. For example, if the genes that regulate shoot indeterminacy were
shown to regulate compound leaf morphogenesis, this would support the
hypothesis that compound leaves are partially indeterminate structures.
Conversely, the alternative hypothesis would be supported by the finding that
the genes that regulate blade development in simple leaves generate compound
leaf pinnae.
|
Genes controlling compound leaf development
Intensive research in model plant systems has identified numerous genes that control plant growth and development. The shoot apical meristem (SAM) of seed plants is an indeterminate structure that maintains itself and is the source of cells that give rise to determinate organs, such as leaves and flowers. Indeterminacy during vegetative and reproductive development is controlled by a suite of genes that function at different stages in the SAM. The process of leaf or floral organ initiation begins when cells in the incipient organ primordium alter their identity from being indeterminate to determinate. By comparing gene expression patterns between simple and compound leafed species during their development, it might be possible to assess the level of determinacy that each of these leaf types possesses.
The role of meristem genes
The indeterminate SAM is characterized by the expression of the Class 1
KNOTTED1-LIKE HOMEOBOX (KNOX1) genes. One of the earliest
known indicators of a change in fate from indeterminate meristem cells to
determinate leaf primordium cells is the downregulation of KNOX1
genes. KNOX1 genes have been implicated in the acquisition and/or
maintenance of meristematic fate. Evidence for this is based on the phenotypes
of loss-of-function mutants, misexpression mutants and overexpression
transgenic plants. For example, loss-of-function mutations in the
KNOX1 genes shoot meristemless (stm) and
knotted1 (kn1) in Arabidopsis and maize,
respectively, result in plants that are unable to maintain a SAM
(Long et al., 1996;
Vollbrecht et al., 2000
).
Maize plants that misexpress KNOX1 genes outside of their normal
domain have ectopic proliferation of tissue in leaves, described as knots,
which often grow over veins (Vollbrecht
et al., 1990
; Schneeberger et
al., 1995
; Muehlbauer et al.,
1999
). Transgenic overexpression of KNOX1 genes often
results in plants with curled, wrinkled and lobed leaves that form ectopic
meristems (Sinha et al., 1993
;
Chuck et al., 1996
;
Tamaoki et al., 1997
;
Schneeberger et al., 1998
).
Ectopic expression of STM inhibits the differentiation of leaf cells,
activates G1/S cell cycle markers (Gallois
et al., 2002
), and activates a CyclinB::GUS reporter gene
(Lenhard et al., 2002
). Thus,
KNOX1 expression within or outside of the meristem appears to be
sufficient to promote stem cell proliferation and indeterminacy.
KNOX1 genes are downregulated in the incipient leaf primordia in
both compound leafed and simple leafed species
(Fig. 2). In most plants with
simple leaves, such as Arabidopsis, tobacco, snapdragon and maize,
this downregulation is permanent (Fig.
2A,B) (Smith et al.,
1992; Lincoln et al.,
1994
; Nishimura et al.,
1998
; Waites et al.,
1998
; Nishimura et al.,
1999
). However, KNOX1 gene expression is re-established
later in the developing primordia of most plants with compound leaves (with
the exception of pea, see below), such as in tomato and Oxalis
(Fig. 2C,D)
(Hareven et al., 1996
;
Chen et al., 1997
;
Janssen et al., 1998
;
Bharathan et al., 2002
).
Additionally, overexpression of KNOX1 genes in transgenic plants or
in naturally occurring tomato mutants results in leaves with increased numbers
of leaflets (Hareven et al.,
1996
; Chen et al.,
1997
; Parnis et al.,
1997
). It has therefore been concluded that KNOX1 genes
are involved in regulating compound leaf development by establishing a more
indeterminate environment within developing primordia. A survey of
KNOX1 gene expression in diverse seed plant taxa has indicated that
KNOX1 genes may have been recruited multiple times during evolution
for the regulation of leaf complexity across the flowering seed plants
(angiosperms) (Bharathan et al.,
2002
).
|
The tomato FLO/LFY ortholog is FALSIFLORA (FA).
Like in other angiosperms, the fa tomato mutant has altered flowering
time and inflorescence development. Floral meristem identity is lost in these
mutants and flowers are replaced by secondary shoots. Interestingly, the
fa mutant has a subtle leaf phenotype the number of small
intercalary leaflets is slightly reduced, which can be interpreted as a
reduction in complexity (Molinero-Rosales
et al., 1999). Known expression patterns of
FLO/LFY orthologs in vegetative apices have been summarized
recently (Busch and Gleissberg,
2003
). In species with compound leaves, such as pea, tomato,
grapevine and poppy, FLO/LFY expression is prolonged during
leaf development and accompanies organogenesis at the marginal blastozone
(Busch and Gleissberg, 2003
).
Therefore, it is possible that FLO/LFY also functions in
compound leaf development in species other than pea. The regulation of both
vegetative and floral meristem development by FLO/LFY may reflect the
ancestral condition of seed plants, and, if this were the case, compound leaf
development in most situations would be regulated by a combination of
KNOX1 and FLO/LFY genes. In pea, the role of
KNOX1 genes in regulating compound leaf development would have been
completely taken over by the FLO/LFY ortholog, UNI. Thus,
the role of FLO/LFY in regulating compound leaf development
in all angiosperms is an area worthy of further investigation.
STAMINA PISTILLOIDA (STP) has been identified as another
floral meristem gene that is involved in regulating compound leaf development
in pea. Severe mutant stp alleles produce phenotypes similar to those
observed in the uni mutant: flowers consisting of sepals and carpels,
and a reduction in leaf complexity, in addition to other abnormalities. Weak
mutant alleles of stp and uni act synergistically in pea,
indicating that these two genes may act together to regulate common pathways
(Taylor et al., 2001).
STP is homologous to the UNUSUAL FLORAL ORGANS
(UFO) gene of Arabidopsis and to the FIMBRIATA
(FIM) gene of snapdragon (Simon
et al., 1994
; Ingram et al.,
1995
; Taylor et al.,
2001
). UFO is considered to co-regulate floral organ
identity genes together with LFY
(Lee et al., 1997
).
Overexpression of UFO in wild-type Arabidopsis leads to
excessive leaf lobing, a phenotype that is also observed when KNOX1
genes are overexpressed. However, overexpression of UFO in a
lfy mutant background results in Arabidopsis plants with
normal leaves, indicating that LFY is required to phenocopy the
KNOX1 overexpression results (Lee
et al., 1997
). stm mutants do not accumulate UFO
transcripts, suggesting that expression of UFO depends on
STM, and that these two pathways are linked
(Long and Barton, 1998
).
It is possible that FLO/LFY and FIM/UFO
orthologs function together, and with KNOX1 genes, to regulate
compound leaf development in angiosperms (see also
Tsiantis and Hay, 2003). Pea
appears to be an excellent model species for revealing additional candidate
genes that contribute to the regulation of compound leaf development. These
additional regulators may be masked by KNOX1 genes, which might act
redundantly to control similar pathways in other angiosperms, such as tomato.
The fact that meristem genes, like KNOXI and LFY, which
regulate indeterminacy at the vegetative and reproductive SAM, also play a
role in making compound leaves suggests that the acquisition of a level of
indeterminacy is necessary for compound leaf development. This supports the
hypothesis that individual leaflets of compound leaves are similar to simple
leaves.
The role of leaf function genes
Leaf morphology is organized along three major axes: the proximodistal
axis, the mediolateral axis and the abaxial/adaxial axis (see
Box 2) (Waites and Hudson, 1995;
McConnell and Barton, 1998
).
It is thought that the juxtaposition of the adaxial and abaxial domains is
required for blade outgrowth (Waites and
Hudson, 1995
; McConnell and
Barton, 1998
).
Box 2. Leaf polarity
The primordium and its resulting leaf have inherent polarities with respect to the meristem, as shown in these Kalanchoë daigremontiana leaves. The proximal region of the primordium or leaf is the region that is closest to the attachment point on the meristem or stem, and the distal region is the tip of the primordium or leaf, furthest away from the attachment point. The mediolateral axis spans across the leaf blade, from the middle region to the edge of the blade. The adaxial domain of a leaf, which corresponds to the top of the leaf, is the side of the primordium that is adjacent to the meristem. The abaxial domain is derived from the side of the primordium furthest away from the meristem, and forms the bottom of the leaf.
|
PHANTASTICA (PHAN) is a MYB-domain transcription factor that was first
identified in snapdragon (Waites et al.,
1998). Loss-of-function phan mutants have reduced adaxial
domains. The most severe mutants have complete loss of the adaxial domain and
radialized, needle-like leaves. Axillary buds, a marker of adaxial identity,
are seen in phan mutants, suggesting that some adaxial identity is
retained at the leaf base (Waites and
Hudson, 1995
; Waites et al.,
1998
). However, mutations in orthologous genes ROUGH
SHEATH2 (RS2) and ASYMMETRIC LEAVES1 (AS1), in
maize and Arabidopsis, respectively, usually do not cause major
aberrations in the leaf adaxial domain in these plants
(Schneeberger et al., 1998
;
Serrano-Cartagena et al.,
1999
). Nevertheless, the as1-101 allele, in the
Ler background of Arabidopsis, occasionally produces plants
that have lotus-like leaves, with the radial petiole attached to the abaxial
surface of the leaf lamina, and the most severely affected as1-101
Ler plants have needle-like leaves
(Sun et al., 2002
;
Xu et al., 2003
).
PHAN and its orthologs are expressed in the incipient leaf
primordium, and in the developing leaves of simple leafed plants, in a pattern
that is mutually exclusive to the expression pattern of KNOX1 genes
(Waites et al., 1998
;
Timmermans et al., 1999
;
Tsiantis et al., 1999
;
Byrne et al., 2000
;
Byrne et al., 2002
).
Differences in the PHAN mutant phenotypes between species have
raised uncertainties about the role of PHAN in regulating the adaxial
domain of leaf primordia (Timmermans et
al., 1999; Tsiantis et al.,
1999
; Byrne et al.,
2000
) and about the function of this domain in blade outgrowth
(McHale and Koning, 2004
).
Downregulation of PHAN orthologs in mutant and transgenic plants is
always accompanied by upregulation and ectopic expression of KNOX1 in
leaves. This has led to the proposal that, in plants with decreased levels of
PHAN, there is a KNOX1-mediated displacement of stem
identity into the leaf, causing it to become radial. In tobacco,
KNOX1-expressing leaf blade cells maintain an immature identity, and
juxtaposition of these cell types, with differentiated cells in the vein
region of the leaf, leads to ectopic blade outgrowth along veins, and may also
explain normal blade outgrowth (McHale and
Koning, 2004
). However, radial leaves and petioles do not show a
stem-like vasculature because they are missing a central pith, which is
normally present within the stem (Waites
and Hudson, 1995
; Sun et al.,
2002
; Kim et al.,
2003c
; Xu et al.,
2003
). While these data suggest a general role for PHAN
in determining the adaxial domain, it is likely that PHAN also
functions to regulate adaxial mesophyll development.
Recently, the role of PHAN orthologs in compound leaf development
has been investigated. The tomato gene LePHAN is expressed in the
SAM, developing vascular traces, and along the entire adaxial domain of
developing leaves (Koltai and Bird,
2000; Kim et al.,
2003b
; Kim et al.,
2003c
). Transgenic tomato plants that express an antisense
LePHAN construct have a diminished adaxial domain
(Kim et al., 2003b
). Various
leaf phenotypes, such as needle-like or cup-shaped leaves, were generated
depending on the amount and location of LePHAN production.
Interestingly, some transgenic tomato plants produced peltate palmate leaves
instead of pinnate leaves. In situ RNA expression analysis of plants with
needle-like leaves showed that they had no LePHAN transcripts in
developing leaves. Plants with cup-shaped leaves or with peltate palmate
leaves had LePHAN expression restricted to the distal region of the
leaf primordium. The most parsimonious explanation for these phenotypes is
that the PHAN expression domain coincides with the adaxial domain,
and that blades and leaflets only occur where an adaxial domain is present in
these leaves (Kim et al.,
2003b
).
The results of altered LePHAN expression in tomato suggest that
restriction of the adaxial domain in compound leafed species may be a natural
mechanism to control compound leaf morphology. There is a high degree of
sequence identity between PHAN orthologs from many species, and this
indicates a conserved function for PHAN in defining the adaxial
domain (Kim et al., 2003b).
PHAN expression determines the placement and extent of this domain.
Indeed, a broad survey of compound leafed species showed that pinnate leaves
possess a distinct adaxial domain in the petiole and rachis, and PHAN
is expressed along the entire adaxial region of the leaf primordium.
Furthermore, peltate palmate leaf petioles are radial and do not have an
adaxial domain. In these leaves, PHAN expression and the adaxial
domain are restricted to the distal region of the primordium
(Kim et al., 2003b
). The
common role of PHAN in simple leaf development and in compound leaf
development is the regulation of adaxial domain identity, which, in the proper
context, leads to blade expansion. An additional role for PHAN in
compound leaves is the regulation of leaflet initiation and placement, as
determined by the extent and placement of the adaxial domain
(Fig. 3). The regulation, not
only of blade outgrowth, but also of leaflet formation by PHAN
suggests a common mechanism by which these two types of outgrowths occur, and
that leaflets could arise by interruptions in blade outgrowth, supporting the
hypothesis that the entire compound leaf is equivalent to a simple leaf.
|
|
|
Plant growth regulators (PGRs) are small molecules that regulate many
aspects of plant growth and development. PGRs such as gibberellic acid (GA),
cytokinin and auxin have been implicated in controlling leaf morphology.
Meristem genes like KNOX1 and FLO/LFY orthologs may
be regulated by plant hormones and may coordinate hormone networks
(Fig. 4). For example,
KNOX1 misexpression phenotypes are similar to cytokinin
overexpression phenotypes (Estruch et al.,
1991; Sinha et al.,
1993
). In addition, there are several examples of overexpression
of KNOX1 genes stimulating cytokinin synthesis
(Kusaba et al., 1998b
;
Frugis et al., 1999
;
Ori et al., 1999
;
Hewelt et al., 2000
). A clear
relationship between GA and KNOX1 genes has also been established.
Their interaction was first noted in studies that showed that ectopic
expression of KNOX1 in various species resulted in decreased levels
of GA (Tamaoki et al., 1997
;
Kusaba et al., 1998a
;
Kusaba et al., 1998b
;
Tanaka-Ueguchi et al., 1998
).
Subsequently, it was demonstrated that the tobacco KNOX1 gene
NTH15 directly binds to, and represses the transcription of, a
GA20-OXIDASE gene, which is involved in GA biosynthesis
(Sakamoto et al., 2001
).
KNOX1 genes from Arabidopsis and tomato also repress
GA20-OXIDASE (Hay et al.,
2002
). Thus, one role of KNOX1 genes is to inhibit GA
biosynthesis in the meristem.
Me and Cu tomato mutants both exhibit ectopic expression
of LeT6, the tomato STM ortholog, and a concomitant
reduction in GA20-OXIDASE, leading to reduced GA levels. The
exogenous application of GA, or constitutive GA signaling (as exhibited in the
tomato procera mutant), results in a reduction in leaf compounding in
wild-type and Me backgrounds, indicating that leaf complexity in
tomato is regulated by GA (Hay et al.,
2002; Hay et al.,
2004
). Recruitment of KNOX1 genes into developing
primordia, and the preservation of the interaction between KNOX1
genes and GA biosynthesis, may have been a mechanism that has been used
several times in evolution to promote the partially indeterminate state that
is required for compound leaf development.
Polar auxin transport and auxin gradients regulate the site of primordia
formation on a SAM, and control the arrangement of leaves on the stem
(phyllotaxy) (Reinhardt et al.,
2000; Kuhlemeier and
Reinhardt, 2001
; Stieger et
al., 2002
; Reinhardt et al.,
2003
). In maize, a polar auxin transport inhibitor, called
N-1-naphthylphthalamic acid (NPA), prevents leaf initiation and inhibits the
downregulation of KNOX1 proteins in the incipient primordium of cultured
shoots (Scanlon, 2003
). It is
possible that KNOX1 genes in simple and compound leaves are
downregulated in response to an auxin gradient
(Scanlon, 2003
;
Hay et al., 2004
). Recently,
the role of auxin in pea leaf development has been examined. Wild-type and
uni-tac (a mild allele of uni) plantlets were cultured on
auxin transport inhibitors and an auxin antagonist. Both wild-type and mutant
plantlets displayed reduced leaf complexity, and had reduced UNI
transcript levels within the shoot apex
(DeMason and Chawla, 2004
). In
young pea leaves, auxin concentrations are highest at the tip. Pinna type
(either leaflet or tendril) is primarily determined by the position of the
pinna along the rachis, and thus may respond to the auxin gradient. DeMason
and Chawla speculate that UNI is regulated by auxin concentration
gradients and/or auxin transport. In wild-type pea, UNI expression
correlates with the predicted site of auxin action
(DeMason and Chawla, 2004
).
Interestingly, in Arabidopsis, LFY is regulated by GA via MYB-domain
proteins (Gocal et al., 2001
).
DeMason and Chawla propose that auxin may regulate LFY/UNI
expression through GA in pea (DeMason and
Chawla, 2004
), as it has been established that auxins regulate GA
biosynthesis.
Future research in compound leaf development
Evolution of meristem and leaf genes
The evolution of expression domains
Changes in the expression domains of key morphogenetic regulators, such as
KNOX1 genes and PHAN orthologs, correlate with, and may have
contributed to, the evolution of compound leaves. Changes that might have this
effect include those to promoters and regulatory regions of these genes
(cis-alterations), and/or changes in the proteins that interact with the
regulatory regions of these genes (trans-alterations). Phylogenetic analyses
and comparisons of non-coding regions from genes such as KNOX1,
FLO/LFY and PHAN orthologs might help address this
issue. At this time, there are no known proteins that directly interact with
the promoters of KNOX1 genes. In Arabidopsis, a MYB domain
protein (AtMYB33), which mediates response to GA, binds to a specific sequence
in the LFY promoter (Gocal et
al., 2001). The identification of trans-factors that interact with
the promoters of KNOX1 and FLO/LFY orthologs will
be crucial to our understanding of how the expression domains of these genes
are controlled.
Two other mechanisms that may control where important regulators are
expressed are RNA and protein movement. KNOX1 RNA and protein
movement has been well documented. KN1 mRNA expression in maize was
not detected in the tunica layer of the meristem, although expression of the
KN1 protein was observed in these cells
(Jackson et al., 1994). Lucas
et al. used microinjection studies in both maize and tobacco to demonstrate
that labelled KN1 protein is transported between cells via plasmodesmata
(Lucas et al., 1995
). The
movement of GFP-labelled KN1, BP and STM is differentially regulated within
leaf tissue and the meristem (Kim et al.,
2002
; Kim et al.,
2003a
). Additionally, the long-distance movement of a
LeT6-fusion transcript from a tomato Me mutant stock to a
wild-type scion across a graft union has been reported and is developmentally
significant (Kim et al.,
2001
). Likewise, LFY is also capable of moving between
cells. In wild-type Arabidopsis, LFY mRNA is expressed in all cell
layers of young flower primordia. Using a promoter that restricts
transcription of LFY to the outer cell layer of the meristem rescues
lfy mutants, indicating that LFY protein can move between cell layers
(Sessions et al., 2000
).
Movement of a LFY-GFP fusion protein across several layers is considered to be
non-targeted and driven by diffusion (Wu
et al., 2003
). Wu et al. suggest that diffusion of macromolecules
within the apex of Arabidopsis may be the default state and the
retention of certain macromolecules may be significant
(Wu et al., 2003
). Movement
(or retention) of RNA and protein between cells and over long distances could
have multiple points of regulation, which, if altered, could influence the
localization of transcription factors and the regulation of downstream
targets.
The role of meristem signals and polarity genes
Changes in the timing, concentration and location of signals that establish
patterns and gradients may also contribute to the expression domains of
factors that regulate leaf morphology. A prime candidate for investigation is
auxin, which may control the expression of KNOX1 and LFY
orthologs. Additionally, signals that emanate from the meristem act to promote
development of the adaxial domain of leaves. Incisions that isolate the
incipient leaf primordium from the meristem result in radialized leaves that
lack an adaxial domain (Sussex,
1954; Sussex,
1955
; Snow and Snow,
1959
). This suggests that in the absence of the signal(s) from the
meristem, the default state is development of the abaxial domain. To date, the
identity of the adaxial-promoting signal(s) has remained elusive.
In Arabidopsis, PHABULOSA (PHB), PHAVOLUTA
(PHV) and REVOLUTA (REV), a group of closely
related Class III HD-ZIP proteins with sterol/lipid-binding domains, promote
the adaxial domain. One hypothesis is that these genes, which positively
regulate adaxial identity, act as receptors for the meristem signal. Upon
receiving the signal, they promote the adaxial domain and SAM maintenance, and
repress abaxial identity (Talbert et al.,
1995; McConnell and Barton,
1998
; Eshed et al.,
2001
; McConnell et al.,
2001
; Otsuga et al.,
2001
; Bowman et al.,
2002
). Two groups of genes that promote abaxial cell fate appear
to be the likely targets of such repression: the YABBY family of putative
transcription factors (Siegfried et al.,
1999
) and the three GARP transcription factors called KANADI1, 2
and 3 (Eshed et al., 2001
;
Kerstetter et al., 2001
;
Eshed et al., 2004
). All
YABBY genes are expressed in abaxial domains, and all asymmetric
lateral organs express at least one YABBY gene
(Bowman et al., 2002
).
Gain-of-function kan alleles result in radialized organs with abaxial
tissue in place of adaxial tissue (Eshed
et al., 2001
; Kerstetter et
al., 2001
). Interestingly, expression of PHB, PHV and
REV are regulated by microRNAs, and this regulation occurs in all
land plants (Reinhart et al.,
2002
; Rhoades et al.,
2002
; Emery et al.,
2003
; Floyd and Bowman,
2004
). To our knowledge, the roles of these other polarity genes
remain uninvestigated in compound leafed species. It will be fascinating to
see whether changes in PHB, PHV and REV expression correlate
with compound leaf morphology and, if so, whether the altered expression
patterns are mediated through microRNAs.
Competence to respond
The evolution of downstream targets of key regulators, such as
KNOX1 genes, FLO/LFY orthologs and polarity genes, may also
drive modifications to leaf shape. The acquisition or loss of targets of these
genes through changes in their regulatory regions would be significant for
leaf evolution. Even changes in the affinity of a regulator for its target
sequence could alter the amount of product produced. If the product is
required at a certain threshold level to be effective, this alteration could
be important as well. In addition to directly regulating GA20-OXIDASE,
KNOX1 genes also appear to regulate the biosynthesis of lignin, a
component of the cell wall (Mele et al.,
2003). Apart from these genes, little is known about the targets
of KNOX1 transcription factors. More is known about the genes regulated by
LFY in Arabidopsis. For example, AGAMOUS, APETALA3
and APETALA1 are direct targets of LFY
(Busch et al., 1999
;
Wagner et al., 1999
;
Lamb et al., 2002
). Microarray
analysis has identified 15 additional candidates that respond to LFY
(William et al., 2004
).
However, targets of FLO/LFY orthologs have not been
investigated in compound leafed species. Comparisons of KNOX1 and
LFY targets between simple and compound leafed species should be a
useful future research avenue.
The regulation of target genes by factors that control leaf complexity is
also subject to epigenetic control that is exerted by chromatin remodeling
factors. as1 and as2 single mutants in Arabidopsis
misexpress BP and KNAT2, and have mild KNOX1
overexpression phenotypes (Ori et al.,
2000). Ori et al. found that crossing each single mutant with
either serrate (se) or pickle (pkl)
dramatically enhanced the overexpression phenotypes of the progeny
(Ori et al., 2000
).
PKL encodes a CHD chromatin-remodeling factor
(Eshed et al., 1999
;
Ogas et al., 1999
).
SE encodes a putative single 2Cys-2His zinc finger transcription
factor, which also might modify chromatin structure
(Prigge and Wagner, 2001
).
BP and KNAT2 are not misexpressed in se single
mutants, nor were BP and KNAT2 expression levels increased
in se/as1 or se/as2 double mutants
(Ori et al., 2000
). It is
possible that SE and PKL negatively regulate KNOX1
target genes. In support of this, GA20-OXIDASE transcript levels are
reduced in the pkl mutant (Hay et
al., 2004
). This suggests that other KNOX1 targets may
also be subject to epigenetic control.
In addition, the presence or absence of interacting partners could temper
the response to transcription factors that regulate leaf complexity. KNOX1
proteins belong to the TALE (three-amino acid loop extension) family of
homeodomain transcription factors. In simple leafed species, KNOX1 proteins
can form heterodimers with another group of TALE proteins belonging to the
BELL (BEL) family (Bellaoui et al.,
2001; Muller et al.,
2001
; Smith et al.,
2002
; Chen et al.,
2003
; Smith and Hake,
2003
). This interaction occurs in compound leafed species as well.
The potato KNOX1 protein POTH1 interacts with several BEL-like proteins
(Chen et al., 2003
).
StBEL5-POTH1 heterodimers bind to the GA20-OXIDASE promoter with
greater affinity than the individual proteins
(Chen et al., 2004
). It is
possible that KNOX1/BEL heterodimers in simple and compound leafed species may
have a different subset of targets. The availability of interacting partners
could limit the activity of KNOX1 transcription factors. Additionally,
different interacting partners may allow the complex to behave as an activator
or a repressor.
Box 3. Secondary morphogenesis
The ultimate morphology of a leaf is a culmination of both the primary
elaboration of primordia and secondary morphogenesis. For example, leaves that
have a single blade at maturity may develop from simple primordia, or from
compound primordia that are simplified by secondary morphogenesis
(Bharathan et al., 2002
The palms present an interesting case of a simple primordium giving rise to
a compound leaf by secondary morphogenesis that includes folding and
abscission of part of the primordium
(Kaplan et al., 1982a
|
Secondary morphogenesis
Final leaf morphology provides only an incomplete picture of the true
nature of the leaf. Studies that analyze all stages of leaf development are
crucial for obtaining an accurate view of leaf morphogenesis (see
Box 3). Cell division and cell
expansion both contribute to growth. One way to control the spatial and
temporal distribution of growth is to regulate cell-cycle arrest. If
cell-cycle arrest is precocious, morphogenesis would rely solely on cell
expansion. The delay to or absence of cell-cycle arrest could result in
abnormally shaped leaves, or leaves that grow indeterminately. Mutations have
been isolated in Arabidopsis and snapdragon in which entry into
cell-cycle arrest has been perturbed. The CINCINNATA (CIN)
gene from snapdragon encodes a TCP transcription factor (that belongs to a
group of plant-specific basic helix-loop-helix DNA binding proteins) that
promotes cell-cycle arrest. It is expressed in a dynamic pattern in actively
dividing cells, in front of, or overlapping with, the arrest front. The
perimeter of cin mutant leaves grows faster than can be accommodated
in flat leaves, resulting in crinkled, uneven leaves
(Nath et al., 2003). Studies
in Arabidopsis reveal that a microRNA encoded by the JAW
locus can cleave several TCP mRNAs that control leaf development.
jaw mutant plants are reminiscent of the cin mutant in that
they have uneven leaf shape and abnormal curvature
(Palatnik et al., 2003
). The
JAGGED (JAG) gene in Arabidopsis also functions to
control entry into cell-cycle arrest. JAG encodes a putative
C2H2 zinc-finger transcription factor that suppresses
cell-cycle arrest. Lateral organs do not develop completely in
loss-of-function jag mutants. As a consequence, leaves have
serrations, especially in distal regions. Dinneny et al. speculate that the
serrations could be due to a reduction in growth in regions of blade between
the hydathodes (pores that exude water)
(Dinneny et al., 2004
).
The regulation of cell-cycle arrest and cell expansion could contribute to compound leaf evolution. It is possible that the inhibition or promotion of cell-cycle arrest could result in the formation of leaflets, or the growth of entire margins, respectively. It would be interesting to evaluate and compare the roles of genes that control the cell cycle in simple leafed species with simple primordia, in simple leafed species with compound primordia that undergo secondary simplification, and in compound leafed species.
Discovering other loci that regulate leaf complexity
Researchers have used the knowledge gained from model organisms like
Arabidopsis, maize and rice to identify genes that might play a role
in compound leaf development. However, there must exist genes that have, as
yet, unknown functions in these model species that could be important for
compound leaf morphogenesis. The present challenge is to identify these
unknown genes. One possible fruitful approach involves using the genetic
variation in naturally occurring species to identify quantitative trait loci
(QTL) that might regulate leaf complexity. The analysis of segmental
introgression lines between two tomato species, Lycopersicon
esculentum and Lycopersicon pennellii, led to the identification
of 30 QTL that contribute to leaf size and complexity
(Holtan and Hake, 2003).
These, and other, QTL studies could eventually lead to the discovery of
relevant genes and add to our knowledge of compound leaf development. Tomato
and pea have served as useful model species for studying compound leaf
development. Numerous mutations that alter the compound leaf exist in both
species (Marx, 1987
;
Kessler et al., 2001
). For
instance, the semi-dominant mutation Lanceolate regulates leaf
morphogenesis and shoot meristem activity. Heterozygotes have simple leaves,
whereas homozygous mutants have no SAM
(Mathan and Jenkins, 1962
).
Continued genetic and molecular studies of this and other mutations should
eventually identify new pertinent genes and provide additional tools with
which to study compound-leaf evolution.
Conclusions
The ancestral angiosperm is thought to have had simple leaves, and compound
leaves are believed to have arisen numerous times in this group, with several
reversions back to the simple state. This suggests that the conversion from
simple to compound leaves and back can be attained with relative ease. Yet
saturation mutagenesis in Arabidopsis has not yielded any single
mutation that can convert the simple leaf into a compound one. Certain mutant
combinations produce deeply lobed leaves that often have accompanying
KNOX1 gene expression in the leaves, thereby mimicking the situation
of KNOX1 gene expression seen in most compound leaves. A mutation in
the UNI gene can lead to an almost simple leaf. Collectively, these
data support the partial shoot homology of compound leaves by indicating that
genes regulating indeterminacy are required to make compound leaves. However,
PHAN/RS2/AS1 (a gene that regulates blade development in simple
leaves) also regulates adaxial identity in tomato and determines leaflet
placement in various compound leaves. In addition, although
PHAN/RS2/AS1 expression is excluded from the SAM in simple leafed
species, all compound leafed species examined thus far show
PHAN/RS2/AS1 expression in the SAM
(Kim et al., 2003b). These
data suggest that there may be a blurring of the boundary between the
determinate leaf and the indeterminate SAM, as suggested by Arber
(Arber, 1950
). Because
KNOX1 and PHAN are mutually antagonistic but may also be
co-dependent in manifesting phenotypes
(Fig. 5), studies of these
genes do not allow us to clearly distinguish between the two proposed
hypotheses for compound leaf development. Perhaps other genes that play
specific roles in either blade outgrowth or SAM function need to be analyzed
in order to understand the true nature of compound leaves.
ACKNOWLEDGMENTS
We thank Dan Koenig, Rakefet David-Schwartz, Suzanne Gerttula and members of the Sinha Laboratory for critical comments and helpful discussions, Brad Townsley for providing leaf samples, Tom Goliber for the Oxalis expression data, Helena Garcês for the photograph of Kalanchoë daigremontiana, and Tim Metcalf and Ernesto Sandoval (Plant Conservatory, Section of Plant Biology, UC Davis) for providing plant materials. Our research on leaf development is supported by the National Science Foundation.
REFERENCES
Arber, A. (1950). The Natural Philosophy of Plant Form. Cambridge University Press, Cambridge, UK.
Bellaoui, M., Pidkowich, M. S., Samach, A., Kushalappa, K.,
Kohalmi, S. E., Modrusan, Z., Crosby, W. L. and Haughn, G. W.
(2001). The Arabidopsis BELL1 and KNOX TALE homeodomain proteins
interact through a domain conserved between plants and animals.
Plant Cell 13,2455
-2470.
Bharathan, G., Goliber, T. E., Moore, C., Kessler, S., Pham, T.
and Sinha, N. R. (2002). Homologies in leaf form
inferred from KNOXI gene expression during development.
Science 296,1858
-1860.
Bowman, J. L., Eshed, Y. and Baum, S. F. (2002). Establishment of polarity in angiosperm lateral organs. Trends Genet. 18,134 -141.[CrossRef][Medline]
Busch, A. and Gleissberg, S. (2003). EcFLO, a FLORICAULA-like gene from Eschscholzia californica is expressed during organogenesis at the vegetative shoot apex. Planta 217,841 -848.[CrossRef][Medline]
Busch, M. A., Bomblies, K. and Weigel, D.
(1999). Activation of a floral homeotic gene in Arabidopsis.
Science 285,585
-587.
Byrne, M. E., Barley, R., Curtis, M., Arroyo, J. M., Dunham, M., Hudson, A. and Martienssen, R. A. (2000). Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408,967 -971.[CrossRef][Medline]
Byrne, M. E., Simorowski, J. and Martienssen, R. A. (2002). ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129,1957 -1965.[Medline]
Chen, H., Rosin, F. M., Prat, S. and Hannapel, D. J.
(2003). Interacting transcription factors from the three-amino
acid loop extension superclass regulate tuber formation. Plant
Physiol. 132,1391
-1404.
Chen, H., Banerjee, A. K. and Hannapel, D. J. (2004). The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J. 38,276 -284.[CrossRef][Medline]
Chen, J.-J., Janssen, B.-J., Williams, A. and Sinha, N.
(1997). A gene fusion at a homeobox locus: alternations in leaf
shape and implications for morphological evolution. Plant
Cell 9,1289
-1304.
Chuck, G., Lincoln, C. and Hake, S. (1996).
KNAT1 induces lobed leaves with ectopic meristems when overexpressed in
Arabidopsis. Plant Cell
8,1277
-1289.
Coen, E. S., Romero, J. M., Doyle, S., Elliott, R., Murphy, G. and Carpenter, R. (1990). floricaula: a homeotic gene required for flower development in antirrhinum majus. Cell 63,1311 -1322.[Medline]
DeMason, D. A. and Chawla, R. (2004). Roles for auxin during morphogenesis of the compound leaves of pea (Pisum sativum). Planta 218,894 .[CrossRef]
DeMason, D. A. and Schmidt, R. J. (2001). Roles of the uni gene in shoot and leaf development of pea (Pisum sativum): phenotypic characterization and leaf development in the uni and uni-tac mutants. Int. J. Plant Sci. 162,1033 -1051.[CrossRef]
Dinneny, J. R., Yadegari, R., Fischer, R. L., Yanofsky, M. F.
and Weigel, D. (2004). The role of JAGGED in shaping
lateral organs. Development
131,1101
-1110.
Emery, J. F., Floyd, S. K., Alvarez, J., Eshed, Y., Hawker, N. P., Izhaki, A., Baum, S. F. and Bowman, J. L. (2003). Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13,1768 -1774.[CrossRef][Medline]
Eshed, Y., Baum, S. F. and Bowman, J. L. (1999). Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99,199 -209.[Medline]
Eshed, Y., Baum, S. F., Perea, J. V. and Bowman, J. L. (2001). Establishment of polarity in lateral organs of plants. Curr. Biol. 11,1251 -1260.[CrossRef][Medline]
Eshed, Y., Izhaki, A., Baum, S. F., Floyd, S. K. and Bowman, J.
L. (2004). Asymmetric leaf development and blade expansion in
Arabidopsis are mediated by KANADI and YABBY activities.
Development 131,2997
-3006.
Estruch, J. J., Prinsen, E., van Onckelen, H., Schell, J. and Spena, A. (1991). Viviparous leaves produced by somatic activation of an inactive cytokinin-synthesizing gene. Science 254,1364 -1367.
Floyd, S. K. and Bowman, J. L. (2004). Gene regulation: ancient microRNA target sequences in plants. Nature 428,485 -486.[CrossRef][Medline]
Frugis, G., Giannino, D., Mele, G., Nicolodi, C., Innocenti, A.
M., Chiappetta, A., Bitonti, M. B., Dewitte, W., van Onckelen, H. and
Mariotti, D. (1999). Are homeobox knotted-like genes and
cytokinins the leaf architects? Plant Physiol.
119,371
-374.
Gallois, J. L., Woodward, C., Reddy, G. V. and Sablowski, R.
(2002). Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic
organogenesis in Arabidopsis. Development
129,3207
-3217.
Gocal, G. F., Sheldon, C. C., Gubler, F., Moritz, T., Bagnall,
D. J., MacMillan, C. P., Li, S. F., Parish, R. W., Dennis, E. S.,
Weigel, D. et al. (2001). GAMYB-like genes, flowering, and
gibberellin signaling in Arabidopsis. Plant Physiol.
127,1682
-1693.
Gourlay, C. W., Hofer, J. M. and Ellis, T. H.
(2000). Pea compound leaf architecture is regulated by
interactions among the genes UNIFOLIATA, cochleata, afila, and tendril-lessn.
Plant Cell 12,1279
-1294.
Hareven, D., Gutfinger, T., Parnis, A., Eshed, Y. and Lifschitz, E. (1996). The making of a compound leaf: genetic manipulation of leaf architecture in tomato. Cell 84,735 -744.[Medline]
Hay, A., Kaur, H., Phillips, A., Hedden, P., Hake, S. and Tsiantis, M. (2002). The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr. Biol. 12,1557 -1565.[Medline]
Hay, A., Craft, J. and Tsiantis, M. (2004). Plant hormones and homeoboxes: bridging the gap? Bioessays 26,395 -404.[CrossRef][Medline]
Hewelt, A., Prinsen, E., Thomas, M., van Onckelen, H. and Meins, F., Jr (2000). Ectopic expression of maize knotted1 results in the cytokinin-autotrophic growth of cultured tobacco tissues. Planta 210,884 -889.[CrossRef][Medline]
Hofer, J., Turner, L., Hellens, R., Ambrose, M., Matthews, P., Michael, A. and Ellis, N. (1997). UNIFOLIATA regulates leaf and flower morphogenesis in pea. Curr. Biol. 7, 581-587.[Medline]
Hofer, J., Gourlay, C., Michael, A. and Ellis, T. H. (2001). Expression of a class 1 knotted1-like homeobox gene is down-regulated in pea compound leaf primordia. Plant Mol. Biol. 45,387 -398.[CrossRef][Medline]
Holtan, H. E. and Hake, S. (2003). Quantitative
trait locus analysis of leaf dissection in tomato using Lycopersicon pennellii
segmental introgression lines. Genetics
165,1541
-1550.
Ingram, G. C., Goodrich, J., Wilkinson, M. D., Simon, R.,
Haughn, G. W. and Coen, E. S. (1995). Parallels between
UNUSUAL FLORAL ORGANS and FIMBRIATA, genes controlling flower development in
arabidopsis and antirrhinum. Plant Cell
7,1501
-1510.
Iwakawa, H., Ueno, Y., Semiarti, E., Onouchi, H., Kojima, S.,
Tsukaya, H., Hasebe, M., Soma, T., Ikezaki, M., Machida, C. et al.
(2002). The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana,
required for formation of a symmetric flat leaf lamina, encodes a member of a
novel family of proteins characterized by cysteine repeats and a leucine
zipper. Plant Cell Physiol.
43,467
-478.
Jackson, D., Veit, B. and Hake, S. (1994).
Expression of maize KNOTTED 1 related homeobox genes in the
shoot apical meristem predicts patterns of morphogenesis in the vegetative
shoot. Development 120,405
-413.
Janssen, B.-J., Lund, L. and Sinha, N. (1998).
Overexpression of a Homeobox Gene, LeT6, reveals indeterminate
features in the tomato compound leaf. Plant Physiol.
117,771
-786.
Kaplan, D. R. (1975). Comparative developmental evaluation of the morphology of Unifacial leaves in the monocotyledons. Bot. Jahrb. Syst. 95,1 -105.
Kaplan, D. R., Dengler, N. G. and Dengler, R. E. (1982a). The mechanisms of plication inception in palm leaves: histogenetic observations of the palmate leaves of Rhapis excelsa. Can. J. Bot. 60,2999 -3016.
Kaplan, D. R., Dengler, R. E. and Dengler, N. G. (1982b). The mechanisms of plication inception in palm leaves: problem of developmental morphology. Can. J. Bot. 60,2939 -2975.
Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. and Poethig, R. S. (2001). KANADI regulates organ polarity in Arabidopsis. Nature 411,706 -709.[CrossRef][Medline]
Kessler, S., Kim, M., Pham, T., Weber, N. and Sinha, N. (2001). Mutations altering leaf morphology in tomato. Int. J. Plant Sci. 162,475 -492.[CrossRef]
Kim, M., Canio, W., Kessler, S. and Sinha, N.
(2001). Developmental changes due to long-distance movement of a
homeobox fusion transcript in tomato. Science
293,287
-289.
Kim, J. Y., Yuan, Z., Cilia, M., Khalfan-Jagani, Z. and Jackson,
D. (2002). Intercellular trafficking of a knotted1 green
fluorescent protein fusion in the leaf and shoot meristem of Arabidopsis.
Proc. Natl. Acad. Sci. USA
99,4103
-4108.
Kim, J. Y., Yuan, Z. and Jackson, D. (2003a).
Developmental regulation and significance of KNOX protein trafficking in
Arabidopsis. Development
130,4351
-4362.
Kim, M., McCormick, S., Timmermans, M. and Sinha, N. (2003b). The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424,438 -443.[CrossRef][Medline]
Kim, M., Pham, T., Hamidi, A., McCormick, S., Kuzoff, R. K. and
Sinha, N. (2003c). Reduced leaf complexity in tomato
wiry mutants suggests a role for PHAN and KNOX genes in generating compound
leaves. Development 130,4405
-4415.
Koltai, H. and Bird, D. M. (2000). Epistatic repression of PHANTASTICA and class 1 KNOTTED genes is uncoupled in tomato. Plant J. 22,455 -459.[CrossRef][Medline]
Kuhlemeier, C. and Reinhardt, D. (2001). Auxin and phyllotaxis. Trends Plant Sci. 6, 187-189.[CrossRef][Medline]
Kusaba, S., Fukumoto, M., Honda, C., Yamaguchi, I., Sakamoto, T.
and Kano-Murakami, Y. (1998a). Decreased GA1 content
caused by the overexpression of OSH1 is accompanied by suppression of GA
20-oxidase gene expression. Plant Physiol.
117,1179
-1184.
Kusaba, S., Kano-Murakami, Y., Matsuoka, M., Tamaoki, M.,
Sakamoto, T., Yamaguchi, I. and Fukumoto, M. (1998b).
Alteration of hormone levels in transgenic tobacco plants overexpressing a
rice homeobox gene OSH1. Plant Physiol.
116,471
-476.
Lamb, R. S., Hill, T. A., Tan, Q. K. and Irish, V. F.
(2002). Regulation of APETALA3 floral homeotic gene expression by
meristem identity genes. Development
129,2079
-2086.
Lee, I., Wolfe, D. S., Nilsson, O. and Weigel, D. (1997). A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS. Curr. Biol. 7,95 -104.[Medline]
Lenhard, M., Jurgens, G. and Laux, T. (2002).
The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in
Arabidopsis shoot meristem regulation. Development
129,3195
-3206.
Lin, W. C., Shuai, B. and Springer, P. S.
(2003). The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene
ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in
adaxial-abaxial patterning. Plant Cell
15,2241
-2252.
Lincoln, C., Long, J., Yamaguchi, J., Serikawa, K. and Hake,
S. (1994). A Knotted1-like homeobox gene in
Arabidopsis is expressed in the vegetative meristem and dramatically alters
leaf morphology when overexpressed in transgenic plants. Plant
Cell. 6,1859
-1876.
Long, J. A. and Barton, M. K. (1998). The
development of apical embryonic pattern in Arabidopsis.
Development 125,3027
-3035.
Long, J. A., Moan, E. I., Medford, J. I. and Barton, M. K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66-69.[CrossRef][Medline]
Lucas, W. J., Bouche-Pillon, S., Jackson, D. P., Nguyen, L., Baker, L., Ding, B. and Hake, S. (1995). Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270,1980 -1983.[Abstract]
Marx, G. A. (1987). A suite of mutants that modify pattern formation in pea leaves. Plant Mol. Biol. Rep. 5,311 -335.
Mathan, D. S. and Jenkins, J. A. (1962). A morphogenetic study of lanceolate, a leaf-shape mutant in the tomato. Am. J. Bot. 49,504 -514.
McConnell, J. R. and Barton, M. K. (1998). Leaf polarity and meristem formation in Arabidopsis.Development 125,2953 -2942.
McConnell, J. R., Emery, J., Eshed, Y., Bao, N., Bowman, J. and Barton, M. K. (2001). Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411,709 -713.[CrossRef][Medline]
McHale, N. A. and Koning, R. E. (2004).
PHANTASTICA regulates development of the adaxial mesophyll in nicotiana
leaves. Plant Cell 16,1251
-1262.
Mele, G., Ori, N., Sato, Y. and Hake, S.
(2003). The knotted1-like homeobox gene BREVIPEDICELLUS regulates
cell differentiation by modulating metabolic pathways. Genes
Dev. 17,2088
-2093.
Molinero-Rosales, N., Jamilena, M., Zurita, S., Gomez, P., Capel, J. and Lozano, R. (1999). FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J. 20,685 -693.[CrossRef][Medline]
Muehlbauer, G. J., Fowler, J. E., Girard, L., Tyers, R., Harper,
L. and Freeling, M. (1999). Ectopic expression of the
maize homeobox gene Liguleless3 alters cell fates in the leaf.
Plant Physiol. 119,651
-662.
Muller, J., Wang, Y., Franzen, R., Santi, L., Salamini, F. and Rohde, W. (2001). In vitro interactions between barley TALE homeodomain proteins suggest a role for protein-protein associations in the regulation of Knox gene function. Plant J. 27, 13-23.[CrossRef][Medline]
Nath, U., Crawford, B. C., Carpenter, R. and Coen, E.
(2003). Genetic control of surface curvature.
Science 299,1404
-1407.
Nishimura, A., Tamaoki, M. and Matsuoka, M. (1998). Expression pattern of KN1-type tobacco homeobox genes. Plant Cell Physiol. 39,S60 .
Nishimura, A., Tamaoki, M., Sato, Y. and Matsuoka, M. (1999). The expression of tobacco knotted1-type class 1 homeobox genes correspond to regions predicted by the cytohistological zonation model. Plant J. 18,337 -347.[CrossRef][Medline]
Ogas, J., Kaufmann, S., Henderson, J. and Somerville, C.
(1999). PICKLE is a CHD3 chromatin-remodeling factor that
regulates the transition from embryonic to vegetative development in
Arabidopsis. Proc. Natl. Acad. Sci. USA
96,13839
-13844.
Ori, N., Juarez, M. T., Jackson, D., Yamaguchi, J., Banowetz, G.
M. and Hake, S. (1999). Leaf senescence is delayed in
tobacco plants expressing the maize homeobox gene knotted1 under the control
of a senescence-activated promoter. Plant Cell
11,1073
-1080.
Ori, N., Eshed, Y., Chuck, G., Bowman, J. L. and Hake, S.
(2000). Mechanisms that control knox gene expression in the
Arabidopsis shoot. Development
127,5523
-5532.
Otsuga, D., DeGuzman, B., Prigge, M. J., Drews, G. N. and Clark, S. E. (2001). REVOLUTA regulates meristem initiation at lateral positions. Plant J. 25,223 -236.[CrossRef][Medline]
Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C. and Weigel, D. (2003). Control of leaf morphogenesis by microRNAs. Nature 425,257 -263.[CrossRef][Medline]
Parnis, A., Cohen, O., Gutfinger, T., Hareven, D., Zamir, D. and
Lifschitz, E. (1997). The dominant developmental
mutants of tomato, Mouse-ear and Curl, are associated with
distinct modes of abnormal transcriptional regulation of a Knotted gene.
Plant Cell 9,2143
-2158.
Prigge, M. J. and Wagner, D. R. (2001). The
arabidopsis serrate gene encodes a zinc-finger protein required for normal
shoot development. Plant Cell
13,1263
-1279.
Reinhardt, D., Mandel, T. and Kuhlemeier, C.
(2000). Auxin regulates the initiation and radial position of
plant lateral organs. Plant Cell
12,507
-518.
Reinhardt, D., Pesce, E. R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J. and Kuhlemeier, C. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426,255 -260.[CrossRef][Medline]
Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B.
and Bartel, D. P. (2002). MicroRNAs in plants.
Genes Dev. 16,1616
-1626.
Rhoades, M. W., Reinhart, B. J., Lim, L. P., Burge, C. B., Bartel, B. and Bartel, D. P. (2002). Prediction of plant microRNA targets. Cell 110,513 -520.[Medline]
Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S.
and Matsuoka, M. (2001). KNOX homeodomain protein
directly suppresses the expression of a giberellin biosynthetic gene in the
tobacco shoot apical meristem. Genes Dev.
15,581
-590.
Sattler, R. and Rutishauser, R. (1992). Partial homology of pinnate leaves and shoots: orientation of leaflet inception. Bot. Jahrb. Syst. Pflanzengesch. Pflanzengeogr. 114, 61-79.
Scanlon, M. J. (2003). The polar auxin
transport inhibitor N-1-naphthylphthalamic acid disrupts leaf initiation, KNOX
protein regulation, and formation of leaf margins in maize. Plant
Physiol. 133,597
-605.
Schneeberger, R. G., Becraft, P. W., Hake, S. and Freeling, M. (1995). Ectopic expression of the knox homeobox gene rough sheath 1 alters cell fate in the maize leaf. Genes Dev. 9,2292 -2304.[Abstract]
Schneeberger, R., Tsiantis, M., Freeling, M. and Langdale, J.
A. (1998). The rough sheath2 gene negatively regulates
homeobox gene expression during maize leaf development.
Development 125,2857
-2865.
Semiarti, E., Ueno, Y., Tsukaya, H., Iwakawa, H., Machida, C.
and Machida, Y. (2001). The ASYMMETRIC LEAVES2 gene of
Arabidopsis thaliana regulates formation of a symmetric lamina, establishment
of venation and repression of meristem-related homeobox genes in leaves.
Development 128,1771
-1783.
Serrano-Cartagena, J., Robles, P., Ponce, M. R. and Micol, J. L. (1999). Genetic analysis of leaf form mutants from the Arabidopsis Information Service collection. Mol. Gen. Genet. 261,725 -739.[CrossRef][Medline]
Sessions, A., Yanofsky, M. F. and Weigel, D.
(2000). Cell-cell signaling and movement by the floral
transcription factors LEAFY and APETALA1. Science
289,779
-781.
Siegfried, K. R., Eshed, Y., Baum, S. F., Otsuga, D., Drews, G.
N. and Bowman, J. L. (1999). Members of the YABBY gene
family specify abaxial cell fate in Arabidopsis.
Development 126,4117
-4128.
Simon, R., Carpenter, R., Doyle, S. and Coen, E. (1994). Fimbriata controls flower development by mediating between meristem and organ identity genes. Cell 78, 99-107.[Medline]
Sinha, N., Williams, R. E. and Hake, S. (1993). Overexpression of the maize homeobox gene, KNOTTED-1, cause a switch from determinate to indeterminate cell fates. Genes Dev. 7,787 -795.[Abstract]
Smith, H. M. and Hake, S. (2003). The
interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates
internode patterning in the Arabidopsis inflorescence. Plant
Cell 15,1717
-1727.
Smith, L. G., Greene, B., Veit, B. and Hake, S.
(1992). A dominant mutation in the maize homeobox gene,
Knotted-1, cause its ectopic expression in leaf cells with altered
fates. Development 116,21
-30.
Smith, H. M. S., Boschke, I. and Hake, S.
(2002). Selective interaction of plant homeodomain proteins
mediates high DNA-binding affinity. Proc. Natl. Acad. Sci.
USA 99,9579
-9584.
Snow, M. and Snow, R. (1959). The dorsiventrality of leaf primordium. New Phytol. 58,188 -207.
Souer, E., van der Krol, A., Kloos, D., Spelt, C., Bliek, M.,
Mol, J. and Koes, R. (1998). Genetic control of
branching pattern and floral identity during Petunia inflorescence
development. Development
125,733
-742.
Stieger, P. A., Reinhardt, D. and Kuhlemeier, C. (2002). The auxin influx carrier is essential for correct leaf positioning. Plant J. 32,509 -517.[CrossRef][Medline]
Sun, Y., Zhou, Q., Zhang, W., Fu, Y. and Huang, H. (2002). ASYMMETRIC LEAVES1, an Arabidopsis gene that is involved in the control of cell differentiation in leaves. Planta 214,694 -702.[CrossRef][Medline]
Sussex, I. M. (1954). Experiments on the cause of dorsiventrality in leaves. Nature 167,651 -652.
Sussex, I. M. (1955). Morphogenesis in Solanum tuberosum L. Apical structure and developmental pattern of the juvenile shoot. Phytomorphology 5,253 -273.
Talbert, P. B., Adler, H. T., Parks, D. W. and Comai, L.
(1995). The REVOLUTA gene is necessary for apical meristem
development and for limiting cell divisions in the leaves and stems of
Arabidopsis thaliana. Development
121,2723
-2735.
Tamaoki, M., Kusaba, S., Kano-Murakami, Y. and Matsuoka, M. (1997). Ectopic expression of a tobacco homeobox gene, NTH15, dramatically alters leaf morphology and hormone levels in transgenic tobacco. Plant Cell Physiol. 38,917 -927.[Medline]
Tanaka-Ueguchi, M., Itoh, H., Oyama, N., Koshioka, M. and Matsuoka, M. (1998). Over-expression of a tobacco homeobox gene, NTH15, decreases the expression of a gibberellin biosynthetic gene encoding GA 20-oxidase. Plant J. 15,391 -400.[CrossRef][Medline]
Taylor, S., Hofer, J. and Murfet, I. (2001).
Stamina pistilloida, the Pea ortholog of Fim and UFO, is required for normal
development of flowers, inflorescences, and leaves. Plant
Cell 13,31
-46.
Timmermans, M. C. P., Hudson, A., Becraft, P. W. and Nelson,
T. (1999). Rough sheath2: a Myb protein that represses knox
homeobox genes in maize lateral organ primordia.
Science 284,151
-153.
Tsiantis, M. and Hay, A. (2003). Comparative plant development: the time of the leaf? Nat. Rev. Genet. 4,169 -180.[CrossRef][Medline]
Tsiantis, M., Schneeberger, R., Golz, J. F., Freeling, M. and
Langdale, J. A. (1999). The maize rough sheath2 gene
and leaf development programs in monocot and dicot plants.
Science 284,154
-156.
Tsukaya, H. and Uchimiya, H. (1997). Genetic analyses of the formation of the serrated margin of leaf blades in Arabidopsis: combination of a mutational analysis of leaf morphogenesis with the characterization of a specific marker gene expressed in hydathodes and stipules. Mol. Gen. Genet. 256,231 -238.[CrossRef][Medline]
Vollbrecht, E., Veit, B., Sinha, N. and Hake, S. (1990). The developmental gene Knotted-1 is a member of a maize homeobox gene family. Nature 350,241 -243.[CrossRef]
Vollbrecht, E., Reiser, L. and Hake, S. (2000).
Shoot meristem size is dependent on inbred background and presence of the
maize homeobox gene, knotted1. Development
127,3161
-3172.
Wagner, D., Sablowski, R. W. and Meyerowitz, E. M.
(1999). Transcriptional activation of APETALA1 by LEAFY.
Science 285,582
-584.
Waites, R. and Hudson, A. (1995).
phantastica: a gene required for dorsoventrality of leaves in
Antirrhnum majus. Development
121,2143
-2154.
Waites, R., Selvadurai, H. R. N., Oliver, I. R. and Hudson, A. (1998). The Phantastica gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum. Cell 93,779 -789.[Medline]
Weigel, D., Alvarez, J., Smyth, D. R., Yanofsky, M. F. and Meyerowitz, E. M. (1992). LEAFY controls floral meristem identity in Arabidopsis. Cell 69,843 -859.[Medline]
William, D. A., Su, Y., Smith, M. R., Lu, M., Baldwin, D. A. and
Wagner, D. (2004). Genomic identification of direct
target genes of LEAFY. Proc. Natl. Acad. Sci. USA
101,1775
-1780.
Wu, X., Dinneny, J. R., Crawford, K. M., Rhee, Y., Citovsky,
V., Zambryski, P. C. and Weigel, D. (2003). Modes of
intercellular transcription factor movement in the Arabidopsis apex.
Development 130,3735
-3745.
Xu, L., Xu, Y., Dong, A., Sun, Y., Pi, L. and Huang, H.
(2003). Novel as1 and as2 defects in leaf adaxial-abaxial
polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA
functions in specifying leaf adaxial identity.
Development 130,4097
-4107.