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First published online 13 September 2006
doi: 10.1242/dev.02545
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Research Report |
Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK.
Author for correspondence (e-mail:
miltos.tsiantis{at}plants.ox.ac.uk)
Accepted 21 July 2006
SUMMARY
Leaf development in higher plants requires the specification of leaf initials at the flanks of a pluripotent structure termed the shoot apical meristem. In Arabidopsis, this process is facilitated by negative interactions between class I KNOTTED1-like homeobox (KNOX) and ASYMMETRIC LEAVES1 (AS1) transcription factors, such that KNOX proteins are confined to the meristem and AS1 to leaf initials. Sites of leaf inception are also defined by local accumulation of the hormone auxin; however, it is unknown how auxin and AS1 activities are integrated to control leaf development. Here, we show that auxin and AS1 pathways converge to repress expression of the KNOX gene BREVIPEDICELLUS (BP) and thus promote leaf fate. We also demonstrate that regulated auxin gradients control leaf shape in a KNOX-independent fashion and that inappropriate KNOX activity in leaves perturbs these gradients, hence altering leaf shape. We propose that regulatory interactions between auxin, AS1 and KNOX activities may both direct leaf initiation and sculpt leaf form.
Key words: KNOX, AS1, Auxin, AXR1, Leaf development
INTRODUCTION
Correct cell fate allocation in the Arabidopsis shoot depends upon
mutual repression between the AS1 Myb protein, which promotes leaf fate, and
class I KNOX transcription factors, which promote meristem activity
(Long et al., 1996
;
Ori et al., 2000;
Byrne et al., 2000;
Byrne et al., 2002). These
interactions result in the delimitation of AS1-expressing leaf founder cells
in the meristem. Leaf initials are also defined by local auxin maxima
generated by activity of the PINFORMED1 (PIN1) auxin efflux facilitator
protein (Benkova et al., 2003;
Reinhardt et al., 2003;
Heisler et al., 2005).
However, it is not known how the promotion of organ growth by auxin is
integrated with the cell fate allocation pathway defined by AS1/KNOX
proteins.
The disruption of mechanisms repressing KNOX expression in leaves
is associated with perturbations in leaf development and disruption in auxin
homeostasis (Tsiantis et al.,
1999; Scanlon et al.,
2002; Zgurski et al.,
2005), indicating that KNOX misexpression may perturb an
auxin-directed mechanism controlling leaf morphogenesis. However, whether
regulated auxin gradients sculpt leaf shape and how KNOX activity in leaves
may disrupt such auxin gradients is unclear.
Here, we investigate these questions by examining genetic interactions between components of the AS1/KNOX and auxin regulatory pathways in Arabidopsis. We show that auxin activity acts together with AS1 to repress expression of the KNOX gene BP and hence promote leaf development. We also provide evidence that local auxin maxima are required to initiate marginal serrations in the wild-type Arabidopsis leaf, indicating that auxin acts not only to define leaf inception at the meristem but also later in development to control leaf shape. We also show that ectopic BP expression in Arabidopsis leaves alters leaf shape, at least in part by perturbing these local auxin gradients that shape the leaf margin. Thus, the combined action of AS1 and auxin to repress BP expression in leaves plays a key role in safeguarding leaf fate and controlling leaf shape.
MATERIALS AND METHODS
Plant material and genetics
All mutant alleles and transgenic lines are listed in
Table 1. as1;axr1:
axr1 plants from the F2 generation of a cross between
axr1-12 and as1-1 homozygotes were self-pollinated to
generate F3 families that segregated as1;axr1 double mutants.
bp;axr1: bp plants from the F2 generation of a cross between
bp-9 and axr1-12 homozygotes were self-pollinated to
generate F3 families that segregated bp;axr1 double mutants. No
obvious difference in leaf phenotype was observed between axr1-12 and
bp-9;axr1-12 leaves by visual inspection of 50 single and double
mutants. bp;as1;axr1: as1;axr1 plants from the F2 generation of a
cross between as1-1;axr1-12 and bp-9;axr1-12 plants were
self-pollinated to generate F3 families that segregated bp;as1;axr1
triple mutants. axr1;BP::GUS: GUS-positive axr1 plants from
the F2 generation of a cross between axr1-3 and BP::GUS
homozygotes were self-pollinated to generate axr1;BP::GUS F3
families. as1;axr1;BP::GUS: axr1 plants from the F2
generation of a cross between axr1-3;BP::GUS and
as1-1;BP::GUS (Ori et al.,
2000) homozygotes were self-pollinated to generate F3 families
that segregated as1;axr1;BP::GUS double mutants.
as1;axr1;BP::GUS double mutants were also constructed with the
axr1-12 allele and showed an identical pattern of BP::GUS
expression to double mutants constructed with the axr1-3 allele.
pin1-6 double mutant combinations were generated by crossing
heterozygous plants with as1-1, bp-9 or blr-126 mutants.
as1, bp or blr plants from the F2 generation were
self-pollinated to generate respective F3 families that segregated
as1;pin1-6, bp;pin1-6 or blr;pin1-6 double mutants. We
excluded any effects of mixed backgrounds on the phenotypes by obtaining
similar results using pin1-En134, which was generated in the Col
ecotype, in crosses with as1-1 and bp-9. pid;bp: bp plants
from the F2 generation of a cross between a heterozygous pid-3 and
homozygous bp-9 plant were self-pollinated to generate F3 families
that segregated bp;pid double mutants. All reporter lines were
crossed into respective mutant or transgenic lines and expression analysis was
performed in segregating F3 families.
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Chemical treatments
1-N-naphthylphthalamic acid (NPA; Duchefa) was dissolved in dimethyl
sulfoxide (DMSO) to a stock concentration of 500 mM and added to Murishuge
Skoog (MS) medium to a final concentration of 5 or 10 µM.
2,3,5-Triiodobenzoic acid (TIBA; Sigma) was also dissolved in DMSO to a stock
concentration of 500 mM and added to MS medium to a final concentration of 20
µM. In all experiments, MS plates with the same concentration of DMSO were
used as controls.
Microscopy
SEM and confocal microscopy were carried out as previously described
(Bowman et al., 1991;
Running and Meyerowitz, 1995).
Seedlings for confocal microscopy were mounted and observed in water without
fixation using the 458 nm argon laser of a Zeiss LSM510 microscope.
Quantitative RT-PCR analysis
Total RNA (1 µg) extracted from mature leaf tissue was DNaseI treated
and used for cDNA synthesis with an oligo(dT) primer and Superscript reverse
transcriptase (Invitrogen). cDNA was amplified on the ABI PRISM 7300 Sequence
Detection System (Applied Biosystems). Amplification reactions were prepared
with the SYBR-Green PCR Master Kit (Applied Biosystems), according to
manufacturer's specifications, with 0.4 µM of primers and 10 µl of cDNA
per reaction. Each reaction was made in triplicate, and each experiment was
repeated three times. The efficiency of each set of primers and calculation of
the level of induction was determined according to Pfaffl
(Pfaffl, 2001). Error bars
represent the standard error calculated on experiment repetitions. Expression
levels were normalized with values obtained for the ORNITHINE
TRANSCARBAMILASE (OTC) gene, which was used as an internal
reference gene as described by Cnops et al.
(Cnops et al., 2004). Primers
are listed in Table 2.
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).
Tissue was fixed in 90% acetone at -20°C for one hour, washed briefly with
100 mM phosphate buffer, and stained overnight in freshly prepared 100 mM
sodium phosphate buffer with 10 mM sodium EDTA, 1 mM
5-bromo-4-chloro-3-indolyl-ß-D-glucuronic acid (Molecular Probes) and
ferrocyanide and ferricyanide salts (1 mM PIN1::GUS, 2 mM other GUS lines).
Reactions were terminated with 95% ethanol, and leaves were dissected, mounted
in 50% glycerol and viewed with dark-field microscopy.
Leaf silhouettes
Leaves were flattened onto clear adhesive, adhered to white paper and
digitally scanned.
RESULTS AND DISCUSSION
AXR1 acts alongside AS1 to exclude BP expression from leaves
To investigate whether AS1 and auxin act in the same or distinct pathways
to control leaf development, we examined genetic interactions between
as1 and axr1, which confers a primary defect in auxin
signalling (Lincoln et al.,
1990). AXR1 encodes a subunit of the RUB1 activating
enzyme that regulates the protein degradation activity of Skp1-Cullin-F box
complexes, primarily, but not exclusively, affecting auxin responses
(Leyser et al., 1993;
Pozo et al., 1998;
Gray et al., 2001;
Schwechheimer et al., 2002;
Xu et al., 2002). Leaf
phenotypes of the as1;axr1 double mutant were enhanced with respect
to either single mutant, with deeply lobed margins and ectopic stipules
present in the sinus of each lobe (arrowheads,
Fig. 1A-L). These novel
phenotypes observed in as1;axr1 double mutants, but not in either
single mutant, suggest that AS1 and auxin may act in overlapping pathways to
direct leaf development.
To investigate the basis of this genetic interaction, we examined whether
auxin signalling is required to repress KNOX expression in a manner
similar to AS1. We observed inappropriate expression of the KNOX gene
BP but not SHOOTMERISTEMLESS (STM) in axr1
mutant leaves, although the level of BP expression was substantially
higher in as1 than in axr1 leaves
(Fig. 1M). This ectopic
BP expression in axr1 leaves was not accompanied by a
reduction in AS1 transcripts (Fig.
1M), indicating that AXR1 is unlikely to repress BP by
promoting AS1 transcription. We observed a similar expression profile
of ectopic BP but not STM in leaves of a dominant
Aux/IAA17 mutant, axr3-1 (data not shown), suggesting that
regulation of BP by AXR1 probably reflects SCF activity related to
auxin, rather than other signalling pathways. Notably, ectopic expression of
BP in the axr1 leaf is not responsible for the mild leaf
phenotypes that distinguish axr1 from wild type
(Lincoln et al., 1990), as
bp;axr1 double mutant leaves appeared identical to axr1
single mutants (Fig.
1C,J,N,P).
To determine whether the convergence of AS1 and AXR1 activities on BP regulation might account for the novel phenotypes observed in as1;axr1 double mutants, we examined the pattern of BP expression in axr1, as1 and as1;axr1 leaves. Although BP::GUS was absent from wild-type leaves (Fig. 1R), expression was observed in the serration tips of axr1 leaves (Fig. 1S), and in the petiole, midvein and serration tips of as1 leaves (Fig. 1T). However, the pattern of BP::GUS expression in as1;axr1 double mutant leaves was different than that of either single mutant, being sharply localised to margin cells in the sinus of every lobe from an early stage in leaf development (arrows, Fig. 1U,V), correlating with the ectopic initiation of stipules. These results indicate that both AS1 and auxin signalling are required to exclude BP expression from leaves, and that, in their absence, BP is misexpressed at the leaf margin. To test whether this novel pattern of BP expression observed in as1;axr1 leaves is responsible for the ectopic initiation of stipules, we analysed as1;axr1;bp triple mutants. Ectopic stipules observed in cauline leaves of as1;axr1 double mutants, but not in as1 or axr1 single mutants, were not found in as1;axr1;bp triple mutants (Fig. 1W-Y, n=20 triple mutant leaves), indicating that their initiation is likely to depend on BP activity.
|
), nor does
loss of BP function suppress the as1 mutant phenotype
(Byrne et al., 2002). By
contrast, in as1;axr1 double mutants, ectopic stipules initiate at
the sites of ectopic BP expression, and loss of BP function
suppresses this phenotype. These observations suggest that, in as1
mutant leaves, the inability of ectopic BP expression to elicit
ectopic stipule initiation reflects the additional repression of BP
by AXR1. As previously suggested, the ectopic initiation of stipules may
reflect the formation of ectopic meristem-leaf boundaries within the leaf,
because normal stipule formation occurs at the boundary between initiating
leaves and the shoot apical meristem (SAM)
(Ori et al., 2000). Notably,
as1;axr1;bp triple mutant leaves do not revert to wild type, but
rather to an as1-like morphology
(Fig. 1O,Q), possibly because
of the effects of additional KNOX genes misexpressed in as1
or because AS1 also regulates KNOX-independent pathways to promote leaf
development.
PIN1 acts with AS1 to repress BP and promote lateral organ development
To test whether polar transport of auxin at the shoot apex acts in concert
with AS1 to promote leaf development, we analysed pin1;as1 double
mutants. The auxin efflux facilitator PIN1 transports auxin in the epidermis
towards leaf initial cells that then act as auxin sinks, and this local
accumulation of auxin triggers organ initiation
(Benkova et al., 2003;
Reinhardt et al., 2003;
Heisler et al., 2005). Strong
pin1 mutants with impaired auxin transport, therefore, initiate a
reduced number of leaves and no flowers
(Okada et al., 1991). However,
pin1;as1 double mutants initiate significantly fewer leaves than do
pin1 single mutants (Fig.
2A-E, Student's t-test,
P=2.4x10-3), demonstrating that AS1 and PIN1
function redundantly to promote leaf development.
To test whether PIN1 promotes lateral organ development by regulating
BP, we analysed pin1;bp double mutants, predicting that
those aspects of the pin1 phenotype that are BP dependent will be
suppressed. We observed that the failure of pin1 mutants to initiate
both leaves and flowers is partially rescued in these double mutants
(Fig. 2F-H,J,K, Student's
t-test, P=0.025; see also Fig. S1 in the supplementary
material, Student's t-test, P=0.0025), indicating that PIN1
activity in lateral organ formation involves the repression of BP activity. BP
can act as a dimer with a related homeobox protein, BELLRINGER (BLR)/PENNYWISE
(Byrne et al., 2003;
Smith and Hake, 2003), and the
flower initiation defects of pin1 were also suppressed in
blr;pin1 double mutants (Fig.
2G,I,J,L), indicating that PIN1-mediated auxin action to promote
lateral organ initiation is antagonised by both BLR and BP activities.
Antagonistic actions of BP towards auxin-mediated organogenesis were also
observed in double mutants between bp and pinoid
(pid) (Bennett et al.,
1995; Benjamins et al.,
2001), in which organ initiation defects of pid mutants
were partially suppressed (Fig.
2M, Student's t-test,
P=2.1442x10-6).
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PIN1 regulates leaf margin development
Our results suggest that auxin and AS1 activities promote leaf fate, in
part by excluding meristem-expressed BP transcripts from leaves.
Previous work has shown that aberrant leaf development resulting from
inappropriate KNOX expression is associated with reduced polar auxin
transport and altered auxin distribution
(Tsiantis et al., 1999;
Scanlon et al., 2002;
Zgurski et al., 2005). Thus,
regulated auxin transport may be an important determinant of leaf shape. To
investigate whether PIN1-directed auxin flux controls leaf shape, we compared
the margin configuration of pin1 and wild-type leaves. Whereas
wild-type (Col ecotype) rosette leaves have a serrated margin
(Fig. 3A), pin1-En134
mutants (Col ecotype) have a smooth margin
(Fig. 3B), indicating that PIN1
activity promotes the development of leaf marginal serrations, hence
determining leaf shape. This effect of loss of PIN1 function on the
leaf margin is independent of the ectopic BP expression observed in
pin1 leaves, as the margins of bp;pin double mutant leaves
are indistinguishable from those of pin1 single mutants (data not
shown).
|
), we
assayed DR5rev::GFP and PIN1:GFP expression in wild-type leaf
margins. DR5rev::GFP was localised in the tips of initiating
serrations (Fig. 3C), and polar
expression of PIN1:GFP in the epidermis indicated that these auxin maxima may
be generated by PIN1-directed auxin efflux (arrowheads
Fig. 3D). This observation
suggests that aspects of the mechanism whereby PIN1-dependent auxin activity
gradients trigger leaf initiation at the SAM may be recapitulated within the
Arabidopsis leaf to determine the shape of the leaf margin. These
local auxin maxima correlated with epidermal convergence points of PIN1
polarity in the leaf margin have recently been shown to control vein
positioning (Scarpella et al.,
2006), suggesting that a common auxin-mediated mechanism may
underlie patterning of leaf venation and elaboration of leaf shape. To further test whether local auxin activity gradients active in the developing leaf margin are required to initiate serrations, we perturbed these gradients by growing wild-type plants (Col ecotype) on NPA. Compared with the serrated leaf margin of plants grown on MS medium (Fig. 3E), a smoother leaf margin developed when these plants were grown on MS medium supplemented with NPA (Fig. 3F). Local auxin activity gradients and polar localisation of PIN1:GFP in margin cells of plants grown on MS medium (arrowheads, Fig. 3G) were abolished in NPA-grown plants and pin1 mutants (Fig. 3H,I, see also Fig. S2 in the supplementary material), demonstrating that these local gradients of auxin activity, generated by PIN1 polarity, are required for the development of a serrated wild-type leaf margin.
To test whether auxin activity in the developing leaf margin responds to
ectopic KNOX expression, we examined PIN1::GUS and
DR5::GUS expression in wild-type and 35S::BP leaves. In
comparison with wild-type leaves (Fig.
4A,C), PIN1::GUS and DR5::GUS expression was
repressed in the distal lamina and concentrated in developing lobes of
35S::BP leaves (Fig.
4B,D). Therefore, KNOX exclusion from leaves is required to
establish the wild-type pattern of auxin activity gradients and PIN1
expression in leaves. To further examine whether PIN1 localisation in the leaf
margin is altered in response to ectopic KNOX activity, we assayed PIN1:GFP
expression during the development of wild-type and dissected leaves that
result from ectopically expressing BP under the control of the
FILAMENTOUS FLOWER (FIL) promoter
(Hay and Tsiantis, 2006).
PIN1:GFP expression maxima were observed at sites of developing serrations
along the wild-type leaf margin (arrow Fig.
4E), and were shifted basipetally as new serrations were initiated
(arrow Fig. 4F). PIN1:GFP
expression in initiating leaflets of FIL>>BP leaves was
indistinguishable from that of wild type; however, expression persisted as
leaflets developed in FIL>>BP leaves (arrows
Fig. 4G), suggesting that KNOX
activity in the leaf prevents the normal basipetal displacement of PIN1:GFP
expression maxima, correlating with prolonged localised growth and leaflet
formation. BP-induced alterations in PIN1:GFP expression were mirrored by
similar alterations in expression of the AINTEGUMENTA (ANT)
gene (arrows, Fig. 4H-J), which
promotes growth in Arabidopsis lateral organs
(Krizek, 1999;
Mizukami and Fischer, 2000;
Grandjean et al., 2004). These
observations suggest that auxin-mediated reorganisation of growth at the leaf
margins underpins leaflet formation in FIL>>BP leaves.
To test whether perturbation of such auxin activity gradients contributes to KNOX-dependent alterations in leaf shape, we analysed leaflet formation in FIL>>BP plants grown on MS medium (Fig. 4K) or MS medium supplemented with NPA. Strikingly, we observed that NPA treatment completely blocked leaflet initiation (Fig. 4L; a similar suppression of lobe initiation by NPA treatment was observed in 35S::BP plants, data not shown), and prevented the generation of PIN1-directed auxin maxima in the leaf margin (Fig. 4M and data not shown). The smooth margin formed in both wild-type and FIL>>BP plants as a result of NPA treatment indicates that local auxin maxima generated by polar auxin transport may stimulate the localised growth required for development of both a wild-type serrated margin, when BP is absent from the leaf, and a dissected leaf margin, when BP is ectopically expressed in the leaf. Thus, although auxin activity gradients acting in the leaf margin to control leaf shape are sensitive to ectopic BP activity, their effects on leaf shape are mediated by factors that remain unknown.
|
),
and the characterization of downstream targets of BP, will help to distinguish
between these two possibilities that are not mutually exclusive. The partial
recovery of organ initiation defects of pin1 and pid mutants
in bp;pin1 and bp;pid double mutants is reminiscent of the
suppression of cotyledon boundary formation and the growth defects of
pin1;pid double mutants in stm;pin;pid triple mutants
(Furutani et al., 2004). These
genetic interactions may indicate that the antagonism between KNOX and auxin
activities operates in multiple contexts throughout Arabidopsis
development to promote organ initiation and the associated elaboration of
organ boundaries. Taken together, these observations highlight the modular
nature of auxin action, and emphasize the significance of identifying factors
that contextualise auxin action in distinct tissues at different developmental
stages and possibly at various auxin concentrations
(Ljung et al., 2001;
Xu et al., 2006). For example,
the auxin response factors (ARF) ETTIN/ARF3 and ARF4 act with KANADI proteins
to facilitate axial patterning of lateral organs
(Pekker et al., 2005);
therefore, it will be interesting to determine whether the same or different
transcriptional components mediate the repression of BP by auxin. Conclusions
Our results establish two novel points about developmental patterning in
plants. First, we show that auxin activity, directed by PIN1-dependent fluxes,
is required together with AS1 to repress BP expression and promote
leaf development. Secondly, we show that PIN1 activity is required later in
leaf development to control leaf shape by regulating the initiation of
marginal serrations (Fig. 4N).
Ectopic KNOX expression in leaves perturbs these PIN1-dependent local
gradients of auxin activity, resulting in lobe or leaflet outgrowth. Both KNOX
activity in leaves and auxin signalling are involved in the development of
dissected leaf forms in nature (Bharathan
et al., 2002; Wang et al.,
2005; Hay and Tsiantis,
2006); therefore, it is possible that the differential regulation
of auxin activity gradients by KNOX proteins mediates natural variation in
leaf form.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/133/20/3955/DC1
ACKNOWLEDGMENTS
We thank O. Leyser, A. Hudson, Y. Eshed and S. Hake for critical reading of the manuscript. We thank J. Friml for PIN1:GFP and DR5rev::GFP seeds, O. Leyser for axr1-12 seeds, Y. Mizukami for ANT::GFP seeds, B. Scheres and I. Blilou for pin1En134 seeds, J. Traas for pin1-6 seeds, W. Werr for STM::GUS seeds, S. Hake and N. Ori for bp-9 and 35S::BP seeds, J. Craft for FIL>>BP lines, and Y. Eshed and J. Bowman for FIL::LhG4 seeds. We also thank J. Baker for photography, I. Moore for assistance with confocal microscopy and the Arabidopsis Biological Resource Center for seeds. M.T. receives support from the BBSRC and the Gatsby Charitable foundation. A.H. is the recipient of a University of Oxford Glasstone Research Fellowship and a Balliol College Junior Research Fellowship. M.B. is the recipient of a Bodossakis Foundation Award. This work was also funded by an EU MECHPLANT project.
Footnotes
* These authors contributed equally to this work 
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