1 Section of Plant Biology, Division of Biological Sciences, University of
California, One Shields Avenue, Davis, CA 95616, USA
2 Department of Plant Sciences, The Weizmann Institute of Science, Rehovot,
76100 Israel
Authors for correspondence (e-mail:
jlbowman{at}ucdavis.edu
and
yuval.eshed{at}weizmann.ac.il)
Accepted 18 March 2004
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SUMMARY |
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Key words: Arabidopsis, Leaves, Abaxial-adaxial polarity, Pattern formation, YABBY, KANADI
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Introduction |
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The formation of the leaf lamina requires the establishment of polarity and
is proposed to be a result of interactions between juxtaposed abaxial and
adaxial cells (Sussex, 1955;
Waites and Hudson, 1995
). The
initial establishment of ad-abaxial polarity may result from a signal
emanating from the apical meristem to induce or maintain adaxial identity, and
in the absence of signal, abaxial identity may be the default. As
communication between the abaxial and adaxial domains has been proposed to be
responsible for lamina growth, factors promoting the identity of one or both
domains are probably involved in directing the initial stages of lamina
formation. In Arabidopsis, adaxial fates are promoted by the
expression of members of the class III HD-ZIP family of genes, such as
PHABULOSA (PHB), PHAVOLUTA (PHV) and
REVOLUTA (REV)
(McConnell and Barton, 1998
;
McConnell et al., 2001
;
Emery et al., 2003
). Abaxial
fates are promoted by members of two gene families, the KANADIs and the YABBYs
(Sawa et al., 1999
;
Siegfried et al., 1999
;
Eshed et al., 1999
;
Kerstetter et al., 2001
;
Eshed et al., 2001
).
Gain-of-function alleles of some class III HD-ZIP genes (PHB, PHV)
result in adaxialized radial leaves lacking lamina expansion
(McConnell and Barton, 1998
;
McConnell et al., 2001
), and
loss-of-function alleles result in abaxialized radial cotyledons
(Emery et al., 2003
).
Conversely, gain-of-function alleles of KANADI result in radial abaxialized
organs (Eshed et al., 2001
;
Kerstetter et al., 2001
).
Thus, homogenization, either to all abaxial or all adaxial identities results
in a loss of lamina development, consistent with the hypothesis of Waites and
Hudson (Waites and Hudson,
1995
) that juxtaposition of these two domains is critical for
lamina expansion.
Previously, members of the YABBY gene family have been proposed to promote
abaxial cell fates. This hypothesis was based on the observations that
gain-of-function alleles of several members, FILAMENTOUS FLOWER
(FIL) and YABBY3 (YAB3) and CRABS CLAW
(CRC), result in abaxial tissues differentiating in adaxial
positions, namely in the cotyledon, leaf and petal epidermises
(Sawa et al., 1999;
Siegfried et al., 1999
;
Eshed et al., 1999
).
Conversely, loss-of-function alleles of CRC, when in combination with
kan1 mutations result in adaxial tissues developing in abaxial
positions in the gynoecium (Eshed et al.,
1999
). During leaf development FIL and YAB3 are
expressed in the abaxial regions of Arabidopsis leaves and their
expression patterns parallel that of the progress of leaf differentiation
(Siegfried et al., 1999
;
Sawa et al., 1999
;
Kumaran et al., 2002
). We
present several lines of evidence that YABBY gene activity is associated with
lamina expansion and propose that boundaries of YABBY gene expression marking
the abaxial-adaxial boundary are intimately linked with the proposed
communication between the abaxial and adaxial domains during leaf
development.
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Materials and methods |
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Plants mutant for kan1, kan2, fil and yab3 were selected as follows: 25 phenotypically wild-type plants from the F2 of kan1 kan2 x fil yab3 were self-fertilized and tested in the F3. Families in which approximately 3/16 plants looked like either kan1 kan2 or fil yab3 (so kan2 and yab3 are homozygous) were subjected to further analysis. The rare 1/16 phenotype was considered to be the quadruple mutant, while the 3/16 plant that had trichomes on both sides of their first leaf were considered as fil yab3 kan2 kan1/+.
Isolation of Solanum tuberosum YABBY gene
Total mRNA was extracted from vegetative shoot tips using the RNeasy kit
(Qiagen). First strand cDNA was generated using reverse transcriptase and an
oligo(dT) primer. Two degenerate primers targeting the zinc finger domain
(5' GTIACIGTIMGITGYGGICAYTG 3') and the YABBY domain (5'
GCCCARTTYTTIGCIGC 3') were used to amplify Solanum tuberosum
partial cDNA sequences. Products were cut from the gel and TA cloned using the
TOPO TA cloning kit (Invitrogen). Phylogenetic analysis including a
translation of the sequence obtained from S. tuberosum and the A.
thaliana YABBY gene amino acid sequences indicate S. tuberosum
YABBY1 (GenBank accession no. AY495968) is orthologous to
FIL/YAB3.
Microscopy
SEM, tissue clearing, GUS staining and in situ hybridization were carried
out according to the methods of Eshed et al.
(Eshed et al., 1999) and Emery
et al. (Emery et al., 2003
).
KAN1, KAN2, KAN3, FIL, PHV and PHB probes were generated by
linearizing cDNA plasmids and synthesizing DIG-labeled antisense RNA using T7
RNA polymerase. Histological analyses were carried out as described by Eshed
et al. (Eshed et al., 1999
) for
kan1 kan2 and Emery et al. (Emery
et al., 2003
) for kan1 kan2 kan3.
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Results |
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Polar anatomical and expression pattern features of kan1 kan2 and kan1 kan2 kan3 seedlings
Anatomical differences along the abaxial/adaxial (ab/ad) axis of
Arabidopsis leaves are evident shortly after leaf initiation.
Wild-type leaves have distinct dense columnar palisade mesophyll cells on the
adaxial side (Fig. 2A-C). The
abaxial spongy mesophyll cells appear more cubic and intercelluar air spaces
gradually became more prevalent. The distinct layers of mesophyll are
maintained by predominantly anticlinal cell divisions
(Fig. 2C). In contrast, leaf
primordia of kan1 kan2 and kan1 kan2 kan3 seedlings were
nearly radial (Fig. 2E,H), and
only later displayed signs of polar anatomical features
(Fig. 2F,I). Cells on the
abaxial side of kan1 kan2 leaf primordia maintained a densely
cytoplasmic appearance for a prolonged time, and periclinal divisions were
common (Fig. 2F). As a
consequence, kan1 kan2 leaves were 10-20 cells across, compared to
only six cell layers in wild type. The excess cell divisions were not
distributed equally, resulting in localized outgrowths on the abaxial side
(Fig. 2F). Unlike those of the
double mutant, leaves of the triple mutant remained radial until much later in
development and did not exhibit the ectopic abaxial periclinal divisions
characteristic of kan1 kan2 leaves
(Fig. 2I).
|
|
Effects of uniform KANADI expression
When KANADI was expressed uniformly throughout leaf primordia, such as in
AS1>>KAN2 plants, the leaves that developed were radialized and
abaxialized (Fig. 3E)
(Eshed et al., 2001). To
further test the relationships between KANADI and YABBY or PHB, we examined
their expression patterns in these plants. While PHB was localized to
the adaxial regions of wild-type leaves
(Fig. 3D), no PHB
expression was detected in AS1>>KAN2 leaves, and a low level of
PHB expression was still present in the apical meristem
(Fig. 3G). In contrast,
FIL expression was detected throughout young AS1>>KAN2
leaf primordia (Fig. 3I).
However, unlike wild-type leaves in which FIL expression is
maintained in the marginal abaxial regions
(Fig. 3H), FIL
expression in AS1>>KAN2 was transient, only being detected in
one leaf per apex (Fig. 3I).
Thus, even though AS1>>KAN2 leaves were abaxialized,
FIL expression was ephemeral. We conclude that KANADI can induce
uniform FIL expression in organ primordia, but that lack of
maintenance of FIL expression correlates with the limited extent of
lamina formation.
The abaxial leaf outgrowths have symmetric blade characteristics
Unlike kan1 kan2 floral organs, which can largely be viewed as
adaxialized, the blade outgrowths on the abaxial side of leaves represent a
novel phenotype. To address their nature, anatomical, morphological and
molecular characterizations were carried out. The outgrowths appeared first in
a row on the lower third of the leaf, with additional outgrowths continuing to
initiate and expand for as long as the leaf differentiates
(Fig. 1G-H,
Fig. 4A). The epidermis of
these outgrowths in mature leaves had a high density of stomata interspersed
amongst long rectangular cells similar to those found typically at leaf
margins. In wild-type seedlings, the unique leaf marginal cells exhibited
specific GUS staining in the enhancer trap marker line YJ158
(Fig. 4B). The outgrowths of
kan1 kan2 young leaves showed GUS expression of this marker
throughout their circumference (Fig.
4C), suggesting acquisition of radial blade identity.
|
Similar amphicribral vascular arrangement has been found in the abaxialized
radial leaves of Antirrhinum phantastica mutants
(Waites and Hudson, 1995) and
the abaxialized cotyledons of the phb phv rev triple mutant
(Emery et al., 2003
). An
opposite, amphivasal arrangement was found in adaxialized phb-1d/+
leaves, where a cluster of phloem tissue is surrounded by a ring of xylem
(McConnell and Barton, 1998
).
Combined with the formation of leaf-margin-specific cell types around the
blade outgrowths, the outgrowths can be viewed as ectopic filamentous leaves,
consisting primarily of marginal circumference and abaxial internal tissues.
These observations are consistent with the ectopic boundaries of FIL
expression detected in these outgrowths as they temporally persist beyond the
normal abaxial FIL expression
(Fig. 4J) and are associated
with prolonged cell divisions (Fig.
2F). Earlier in leaf development, FIL expression appeared
to be at highest levels in the region in which outgrowths will soon develop,
and at lower levels throughout the abaxial regions of the majority of the leaf
(Fig. 4K).
Residual apolar morphology and abaxial outgrowths of kan1 kan2 leaves are dependent upon YABBY activity
Since the blade-like outgrowths were associated with strong and localized
FIL expression, we tested whether FIL is required for their
formation. While kan1 kan2 fil leaves still developed outgrowths,
their formation was reduced and delayed (not shown). However, when the
activity of YAB3, which is molecularly and functionally redundant
with FIL (Siegfried et al.,
1999; Kumaran et al.,
2002
) is also compromised, leaves of quadruple mutants, kan1
kan2 fil yab3, exhibited almost no traces of focal outgrowths. The two
different quadruple mutant genotypes, kan1-2 kan2-1 fil-8 yab3-2 or
kan1-2 kan2-1 fil-5 yab3-1, exhibited similar phenotypes; the first
two leaves appeared nearly radial, with trichomes, which are normally found
only adaxially on the first few leaves, present around their entire
circumference (Fig. 5A). The
quadruple mutant plants were greatly reduced in overall size, and organ
expansion was severely decreased. Subsequently produced leaves lacked a clear
plane of blade symmetry and expanded at random orientations, resulting in
short and thick structures (Fig.
5B,I). As in phb-1d homozygotes, the quadruple mutant
plants lacked stipules entirely, a feature seen in fil yab3 mutants
as well (Fig. 5A,B). Unlike the
abaxial epidermal surface of kan1 kan2 cotyledons, which has a clear
abaxial appearance, the abaxial epidermis of the quadruply mutant cotyledons
and leaves resembled those of the wild-type adaxial epidermis
(Fig. 5C-E). In the quadruple
mutant all floral organs except carpels were completely radialized, reduced in
number and lacked defining cell types (Fig.
5F). Overall, these flowers closely resembled those of severely
adaxialized plants homozygous for phb-1d
(Fig. 5K).
|
The YABBY genes were previously suggested to promote abaxial cell fate on the basis of their expression pattern and gain-of-function alleles. Yet, the loss-of-function phenotypes in either fil or fil yab3 mutant backgrounds do not provide clear support for this assumption, as replacement of abaxial cell types by adaxial ones is limited. For example, trichomes were not found on the abaxial surfaces of fil yab3 leaves until the 5th or 6th leaf as in wild type (Fig. 5L inset). However, when KANADI activity is partially compromised the role of the YABBYs as promoters of abaxial identity is revealed. Although kan1-2/+ kan2-1 plants resembled wild type, fil-5 yab3-1 kan1-2/+ kan2-1 plants had short and narrow leaves, with trichomes on both sides of the first produced leaves (Fig. 5L).
Previous analyses of mutations of genes involved in establishing the ab/ad
axis suggested an association between this axis and proper development along
the proximodistal axis (Waites and Hudson,
1995). While no clear morphological markers define the
Arabidopsis proximodistal axis beyond petiole and blade tissues,
neither the kan1 kan2 nor the fil yab3 plants have leaves
that grow to the normal length. Leaves of the quadruple mutants only grew to
20% of the normal length of wild-type leaves, similar in size to homozygous
phb1-d leaves (Fig.
5M), corroborating the concept that proper establishment of
adaxial-abaxial and proximodistal axes are related.
Other YABBY associated lamina growth
SPLAYED (SYD) encodes a SWI/SNF homolog required for
proper B class gene expression during flower development
(Wagner and Meyerowitz, 2002).
In a screen for genetic enhancers of gym kan1 mutations, we
identified two alleles of syd that in the gym kan1 syd
triple mutants resulted in ovules developing from the abaxial regions of the
carpels (Eshed et al., 2001
).
To examine whether syd enhances other aspects of the kanadi
mutant phenotype, we constructed the kan1-2 kan2-1 syd-2 triple
mutant. The leaves of kan1 kan2 syd were radially symmetric and
lacked outgrowths (Fig. 6A).
Consistent with their adaxialized appearance, PHB was expressed
throughout the developing leaves (Fig.
6B). FIL expression was greatly reduced in this
background (Fig. 6C-D). Thus,
the suppression of abaxial outgrowths by syd mutations in a kan1
kan2 background is associated with a loss of YABBY gene expression in
this background.
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Discussion |
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While fil yab3 double mutants do not exhibit a conspicuous loss of
polarity with respect to differentiation of leaf tissues
(Siegfried et al., 1999;
Kumaran et al., 2002
), we show
that FIL and YAB3 contribute to polar differentiation of
tissues in the leaf when in the context of a kan1/+ kan2 background.
Trichomes develop on the abaxial sides of the first leaves in fil yab3
kan1/+ kan2 plants, but not in kan1/+ kan2 plants, indicating
that FIL/YAB3 contribute to the differentiation of cell
types on the abaxial sides of these leaves. Thus, these loss-of-function
phenotypes are consistent with the hypothesis, based on gain-of-function
alelles, that YABBY gene activity promotes abaxial cell fates
(Sawa et al., 1999
;
Siegfried et al., 1999
).
Association of polar YABBY activity with lamina expansion
The establishment of polarity is required for lamina expansion, a critical
process in the development of nearly all lateral organs. Based on elegant
genetic and classic dissection experiments it has been proposed that a
juxtaposition of adaxial and abaxial domains is required for lamina
development (Sussex, 1955;
Waites and Hudson, 1995
).
Several lines of evidence lead us to propose that a major component of the
genetic program directing lamina expansion in leaves is the activity of
members of the YABBY gene family. As outlined below, YABBY gene expression is
correlated with lamina expansion in several different contexts, ectopic YABBY
gene expression leads to ectopic growth, and loss of YABBY gene activity
results in a loss of lamina expansion.
YABBY gene expression patterns mirror distributions of cytoplasmically
dense cells competent to undergo cell division. In Arabidopsis, FIL
and YAB3 are initially expressed throughout the abaxial regions of
leaves, and later, expression becomes restricted to the laminar marginal
domains as the central abaxial domain differentiates into vacuolated cells.
Expression ceases in a basipetal manner, paralleling the differentiation of
leaf cells and preceding the progression in cell division distributions
(Donnelly et al., 1999;
Sawa et al., 1999
;
Siegfried et al., 1999
;
Kumaran et al., 2002
). In
Solanum tuberosum, the correlation with densely cytoplasmic cells is
readily observed, as YABBY expression becomes restricted to the marginal
domains of the abaxial-adaxial boundary. Given that the YABBY-expressing cells
represent a two dimensional sheet of cells, originally throughout the leaf,
but then becoming restricted to two marginal regions of the differentiating
leaf, it would follow that lamina expansion along the proximodistal axis would
also be coupled to establishment of the abaxial-adaxial axis. Thus, in each of
these cases YABBY gene expression patterns are consistent with activity being
linked to lamina expansion.
The reduction in lamina growth, most markedly in the floral organs of
fil yab3 plants is also consistent with YABBY gene activity
contributing to lamina expansion
(Siegfried et al., 1999). Some
lamina expansion does occur in fil yab3 leaves, but this limited
lamina development may be due to two other members of the YABBY gene family,
YAB2 and YAB5, which are expressed in leaves
(Siegfried et al., 1999
).
Characterization of plants lacking all YABBY activity will be required to
address whether YABBY activity is absolutely required for leaf lamina
development. The outer integument is a lateral organ in which expression of
only a single YABBY gene family member, INNER NO OUTER (INO)
has been detected (Villanueva et al.,
1999
). In this case, INO is expressed in the abaxial cell
layer of the outer integument
(Balasubramanian and Schneitz,
2002
; Meister et al.,
2002
) and loss of INO activity results in a complete loss
of lamina expansion of the outer integument. Thus, loss-of-function alleles of
YABBY gene family members are also consistent with a role of YABBY gene
expression promoting lamina expansion.
The model of leaf blade development by Waites and Hudson
(Waites and Hudson, 1995)
proposed that juxtaposition of abaxial and adaxial domains is required for
lamina outgrowth. Leaves of kan1 kan2 plants are mosaic, having both
ectopic adaxial and abaxial characteristics. Young leaf primordia in the
double mutant are nearly radial, with spatially expanded expression domains of
adaxial promoting genes (Eshed et al.,
2001
). Laminar expansion in these leaves occurs largely as a
result of the low level of properly localized YABBY genes since this expansion
is lost in the kan1 kan2 fil yab3 quadruple mutant. However, as
kan1 kan2 leaves differentiate, reactivation of YABBY genes occurs
within specific abaxial foci by a presently unexplained mechanism. These foci
develop as blade-like outgrowths with abaxial fates based on anatomical
characters and vascular organization. YABBY activity is required for lamina
expansion associated with the focal outgrowths since this growth disappears in
the kan1 kan2 fil yab3 background, providing positive evidence that
YABBY activity can induce lamina expansion.
In kan1 kan2 leaves, three levels of YABBY gene expression are evident: the adaxial domain has no expression, the abaxial domain has low levels, and the abaxial foci have high levels. Lamina expansion is correlated with the boundaries between each of these expression domains, suggesting that relative levels, rather than absolute levels, of YABBY activity could be responsible for the blade growth in these leaves. The abnormal thickness of kan1 kan2 leaves can also be seen in a context of prolonged boundaries of YABBY gene expression leading to continued periclinal cell divisions in the abaxial regions of developing leaves. Such boundaries still exist even in kan1 kan2 fil yab3 quadruple mutants, as reflected by FIL expression, and therefore thickness of these leaves could also be attributable to residual YABBY activity, possibly mediated by YAB2 and YAB5. However, when no boundaries (as assayed by FIL) are present, such as in phb-1d, and kan1 kan2 syd leaves, abnormal leaf thickness is not present.
In a phb-1d background, radial adaxialized leaves are produced and
FIL is not expressed at detectable levels in the leaves
(Siegfried et al., 1999).
Thus, loss of YABBY activity is associated with loss of lamina expansion in
this background. In contrast to the adaxialized leaves of the above genotypes,
AS1>>KAN2 plants produce radial abaxialized leaves. If YABBY
activity was solely associated with abaxial cell type specification, one might
expect YABBY gene expression to be prominent. However, in
AS1>>KAN2 leaves FIL expression is transient,
consistent with the lack of lamina expansion in this genotype. YABBY gene
family expression does not necessarily have to be localized to the abaxial
domain to effect lamina expansion. For example, in phb-1d
heterozygotes, peltate leaves, in which cells with abaxial identity are inside
the cup, commonly develop (McConnell and
Barton, 1998
). In this case, YABBY gene expression is associated
with expansion of the cup and is located at the tip of the developing leaf
rather than the abaxial domain (Siegfried
et al., 1999
). Perhaps more remarkably, FIL is expressed
adaxially in petal loss pistallata second whorl floral organs that
are morphologically inverted (Siegfried et
al., 1999
; Griffith et al.,
1999
). As these organs display normal blade expansion, YABBY gene
expression can still exert its role in lamina expansion as long as expression
remains polar.
Thus, in each case examined, YABBY gene activity is associated with regions of lamina expansion, and is necessary in at least some contexts to promote lamina development. In these cases it appears that it is a boundary of YABBY gene activity that is associated with lamina formation. Unlike many genes whose products will promote growth per se, via cell division or cell expansion, we suggest that boundaries of YABBY activity act to promote cell division indirectly in regions spanning both sides of the boundary. This would imply that YABBY activity is signaling between domains, and consistent with this hypothesis ectopic expression of FIL or YAB3 results in dramatic non-autonomous phenotypic effects (Y.E. and J.L.B., unpublished observations). Determination of whether YABBY gene activity is sufficient to induce lamina expansion will require the analysis of genetic chimeric plants in which sectors of YABBY gene expression are produced in fields of cells lacking YABBY activity.
Boundaries and organizers
The proposal that boundaries of YABBY gene expression act as mediators of
zones of lamina expansion has elements in common with the paradigm of
boundaries acting as organizing centers in animal development
(Lawrence and Struhl, 1996;
Basler, 2000
;
Irvine and Rauskolb, 2001
). In
such a developmental paradigm an initial polarity leads to asymmetric
short-range signaling creating a third type of cell at or near the boundary
that produces long-range organizing signals that pattern the differentiation
of surrounding tissues. Such systems provide a powerful mechanism to generate
complex patterns from an initial simple asymmetry. While no signaling
molecules that pattern differentiation within developing leaves have yet been
identified, boundaries of YABBY gene activity appear to promote organ growth
in adjacent cells and thus acting as a focus for lamina formation.
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ACKNOWLEDGMENTS |
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Footnotes |
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Present address: US Patent Office, Washington DC (S.F.B.), USA
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