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First published online 1 November 2006
doi: 10.1242/dev.02652
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1 Department of Molecular, Cellular and Developmental Biology, University of
Michigan, Ann Arbor, MI 48109-1048, USA.
2 Department of Biology, Yonsei University, Sinchon 134, Seoul 120-749,
Korea.
Author for correspondence (e-mail:
clarks{at}umich.edu)
Accepted 18 September 2006
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SUMMARY |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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Key words: Organogenesis, CLAVATA, Meristem, Differentiation, Arabidopsis
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INTRODUCTION |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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The homeodomain-containing transcription factor WUSCHEL (WUS) is necessary
and sufficient within the meristem to specify stem-cell identity. wus
mutations lead to the loss of shoot meristem stem cells, and WUS
overexpression gives rise to ectopic stem cells within the meristem
(Brand et al., 2002
;
Gallois et al., 2002;
Laux et al., 1996;
Lenhard et al., 2002;
Mayer et al., 1998;
Schoof et al., 2000).
WUS is expressed immediately basal to the stem cells in what is
termed as an `organizing center' (Mayer et
al., 1998).
The CLAVATA (CLV) signal transduction components CLV1, CLV2 and CLV3 act to
restrict the domain of WUS expression
(Brand et al., 2000;
Schoof et al., 2000).
CLV1 encodes a receptor-like kinase containing leucine-rich repeat
(LRR) motifs, CLV2 a LRR receptor-like protein and CLV3 a
small secreted polypeptide (Clark et al.,
1997; Fletcher et al.,
1999; Jeong et al.,
1999; Rojo et al.,
2002; Ni and Clark,
2006). Recent findings have shown that transient inactivation of
the CLV pathway leads to rapid alterations in the expression of meristem
regulators, consistent with earlier studies investigating the effect of
clv mutations on WUS expression
(Reddy and Meyerowitz, 2005).
Despite our improving understanding of the crucial biological role of this
signaling pathway in regulating stem-cell specification and differentiation,
no downstream signaling intermediates have been definitively identified.
The best candidate for a CLV signaling intermediate is the protein
phosphatase kinase-associated protein kinase (KAPP)
(Stone et al., 1994;
Stone et al., 1998;
Williams et al., 1997). KAPP
binds, among many receptor-kinases, to CLV1, and both overexpression and
cosuppression studies have suggested that KAPP plays a role in repressing CLV1
function (Stone et al., 1994;
Stone et al., 1998;
Williams et al., 1997).
However, neither a definitive genetic study nor a clear mechanism for KAPP
function has been reported.
Another potential source of signaling components are modifier mutants.
Previous studies have identified mutations in many genes that enhance or
suppress the phenotype of clv mutants and are potential candidates
for signaling intermediates, including SHOOTMERISTEMLESS, ULTRAPETALA,
REVOLUTA, PHABULOSA, PHAVOLUTA, CORONA, PERIANTHIA, and
WIGGUM/ENHANCED RESPONSE TO ABA 1
(Clark et al., 1996;
Fletcher, 2001;
Green et al., 2005;
Otsuga et al., 2001;
Prigge et al., 2005;
Running et al., 1998;
Running and Meyerowitz, 1996).
However, detailed analyses of all of these genes suggest that each acts
independently of the CLV signaling pathway.
Two additional genes that modify the clv phenotype when mutated
are POLTERGEIST (POL) and PLL1, which encode
related protein phosphatases. Mutations in either gene provide partial,
additive suppression of the stem-cell accumulation of clv mutants,
raising the possibility that these two genes act redundantly to promote
stem-cell identity (Song and Clark,
2005; Yu et al.,
2003; Yu et al.,
2000). However, the pol pll1 double mutant is seedling
lethal, complicating previous efforts to analyze these genes and their
potential role in CLV signaling.
In this study, we report a detailed analysis of POL, PLL1, WUS and CLV genetics. We overcome seedling lethality through grafting, and show interactions between mutations in these genes and their overexpression. All of our findings are consistent with a model in which POL and PLL1 act downstream of the CLV proteins, CLV signaling represses POL/PLL1 and POL/PLL1 are required for WUS expression.
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MATERIALS AND METHODS |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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; Yu et al.,
2003; Yu et al.,
2000). pol-6 pll1-1+ plants were isolated from
the F2 progeny obtained from the cross between pol-6 and
pll1-1, and, subsequently, pol-6 pll1-1 double mutants were
identified among the progeny of pol-6 pll1-1+ plants based
on polymerase chain reaction (PCR) genotyping, as described previously
(Song and Clark, 2005). Plants
were grown as described previously (Song
and Clark, 2005). When plants were grown in sterile conditions,
seeds were germinated on the half strength of MS media (Sigma) containing 1%
sucrose and 0.02% MES solidified with 0.6% agarose after imbibition at 4°C
for 2 days following sterilization.
pol pll1 seedlings 4-6 days after germination grown in sterile
condition were micro-grafted as described previously
(Turnbull et al., 2002). A
cotyledon shoulder region of a pol pll1 seedling was dissected with a
razor blade under a dissecting microscope and transferred on top of a
wild-type stock that was prepared by being cut at the hypocotyl region.
Whether a scion and a stock were positioned correctly along the axis was
examined under a dissecting microscope. Grafted plants were moved into soil
approximately 5 days after grafting.
Complementation of pol pll1 with PLL1 expression and antisense expression of PLL1
For the complementation of the seedling-lethal phenotype of pol-1
pll1-1 double mutants, the PLL1 cis-elements including 3.0 kb
promoter and 0.5 kb terminator were used for the expression of PLL1
cDNA. PLL1 cDNA fragment (Song
and Clark, 2005) digested with SmaI/SpeI was
first inserted into a pUC19 vector (digested with SmaI/XbaI)
and then the PLL1 promoter that was digested with
EcoRI/SmaI was inserted in front of the PLL1 cDNA.
Subsequently, the fused fragment was digested with
EcoRI/SalI and introduced into a pOCA28 vector
(Olszewski et al., 1988)
containing a PLL1 0.5 kb terminator (SalI/XhoI)
digested with EcoRI/SalI. pol-1 pll1-1/+ plants
were transformed with this construct as described previously
(Clough and Bent, 1998).
T1 plants displaying kanamycin resistance were screened and PCR
genotyped with PLL1c1/SynLB3 and PLL1c1/PLL1c2 primers to identify plants
containing both the pll1-1 T-DNA insertion and the transgene for
complementation (Song and Clark,
2005). Subsequently, their T2 progeny were PCR
genotyped to screen transgenic plants homozygous for pll1-1.
For the anti-sense expression of PLL1, a full-length cDNA
fragment, PCR amplified with PLL1-NSpe/PLL1-C primers (PLL1-NSpe,
5'-AACTAGTATGGGAAGTGGATTCTCCTCCT-3'); PLL1-C,
5'-CGCACTAGTTCAAAGATACTTTCCTGATGAC-3'), was introduced in reverse
orientation into a pCB302-3 binary vector containing cauliflower mosaic virus
(CaMV) 35S cis regulatory elements
(Xiang et al., 1999). This
transgene was introduced into pol-6 mutants.
Genetic interaction of POL/PLL1 with CLV, WUS and the P35S:CLV3 transgene
clv3-2 pol-6 pll1-1 triple mutants were screened among the progeny
of clv3-2 pol-6 pll1/+ that were identified from PCR genotyping among
the F2 progeny obtained from the cross between clv3-2
pol-6 and clv3-2 pll1 (Song
and Clark, 2005). The seedlings of the triple mutants were grown
in sterile conditions and grafted as described above, and their floral organ
numbers were counted. PER:PLL1 and
P35S:PLL1 transgenes
(Song and Clark, 2005) were
introduced into the clv1-1, clv1-11, clv2-1 and clv3-2
mutant backgrounds by crosses. The individual F2 progeny seed pools
segregating both clv and the transgene were selected, and their
phenotypes were examined. Scanning electron microscopy (SEM) analysis was
performed as described previously
(Diévart et al., 2003)
using plants at 10 days after germination.
The P35S:PLL1 transgene was introduced into the wus-1 mutant background by crosses. The individual F2 progeny segregating both wus-1 and P35S:PLL1 was examined to see whether P35S:PLL1 alters the floral phenotype of wus-1.
F1 plants were obtained from crosses between a transgenic plant
containing P35S:PLL1 and a transgenic plant containing
P35S:CLV3 (Brand et
al., 2000). Plants possessing both P35S:PLL1
and P35S:CLV3 were screened among the F1 plants
and their phenotypes were examined to see whether they displayed the
Wus- phenotype. To determine the presence of the
P35S:PLL1 and P35S:CLV3 transgenes,
PCR genotyping was performed using PLL1c1/PLL1c2 primers (PLL1c1,
5'-GTGTTTACTCGAAGAAGAGACGGA-3'; PLL1c2,
5'-GTGCTCGTTTTTTATTCTTGTTACTTC-3') and 35Sp1/CLV3r primers (35Sp1,
5'-GATGACGCACAATCCCACTA-3'; CLV3r,
5'-TCAAGGGAGCTGAAAGTTGTT-3'), respectively.
Expression of these genes was assessed using primers for PLL1 (PLL1c1/PLL1c2), CLV3 (CLV3f, 5'-ATGGATTCTAAAAGCTTTGTGCT-3'; CLV3r, 5'-TCAAGGGAGCTGAAAGTTGTT-3') and TUB (TUBf, 5'-AGAGGTTGACGAGCAGATGA-3'; TUBr, 5'-CCTCTTCTTCCTCCTCGTAC-3').
Expression pattern analyses of reporter genes
PWUS:GUS and PCLV3:GUS reporter
genes (Gross-Hardt et al.,
2002; Lenhard et al.,
2002) were introduced into mutant backgrounds by crosses. GUS
activity was examined in the plants, which were grown in sterile conditions,
at 10 days after germination, or in the inflorescence of grafted plants as
described previously (Sessions et al.,
1999). Tissues were incubated in the staining solution
overnight.
Complementation of pol pll1 by the ectopic expression of WUS
For ectopic WUS expression, the pOpL two-component
expression system was used (Moore et al.,
1998). APETALA1 (AP1)
(Hempel et al., 1998) and
ERECTA (ER) promoters
(Diévart et al., 2003)
were used to drive the expression of LhG4 (kindly provided by Michael
Prigge, University of Indiana, Indiana, USA). Several independent transgenic
lines were screened and crossed with transgenic plants expressing
pOp:WUS (Schoof et al.,
2000) (kindly provided by Thomas Laux) to examine the strength of
the promoter based on the phenotypes of F1 plants. F1
progeny obtained from the crosses between the selected AP1:LhG4 line
(or ER:LhG4 line) and pol-6 pll1-1/+ were crossed to
F1 progeny obtained from the crosses between pOp6:WUS and
pol-6 pll1-1/+. Among the resulting new progeny, pol pll1
plants were isolated, grafted and PCR genotyped using genespecific primers
(LhG4f/LhG4r for AP1:LhG4 and ER:LhG4; WUS-N/WUS-C for
pOp6:WUS) to test for the presence of both transgenes (LhG4f,
5'-TAACGTTATACGATGTCGCAGAG-3'; LhG4r,
5'-CCAATGCGACCAGATGCT-3'; WUS-N,
5'-CCCGGGGATGGAGCCGCCACAGCATCAG-3'; WUS-C,
5'-GGATCCCTAGTTCAGACGTAGCTCAAG-3'). AP1:LhG4 and
pOp6:WUS transgenes were introduced into the wus-1 mutant
background in a similar manner.
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RESULTS |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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). We
determined that pol pll1 lethality was largely the result of major
defects in basal embryo patterning, and that we could grow pol pll1
double-mutant tissue by grafting the apical portion of a pol-6 pll1-1
seedling onto the hypocotyl/root of a wild-type seedling
(Fig. 1A-E). Both
pol-6 and pll1-1 are T-DNA insertion alleles that are
putative nulls (Song and Clark,
2005). The pol pll1 tissues (Fig. 1F,G) growing in such grafted plants closely phenocopied wus mutants (Fig. 1I), with re-iterative termination of shoot apices during vegetative development. Eventually transitioning to flowering as wus mutants do, the pol pll1 grafted tissue (Fig. 1K,L) gave rise to inflorescence phenotypes similar to wus mutants (Fig. 1N), including flowers with reduced numbers of floral organs, presumably as a result of the loss of flower-meristem stem cells (compare Fig. 1P,Q with Fig. 1S). pol pll1 flowers lacked central carpels and developed reduced numbers of stamens, although the phenotype was slightly less severe than wus mutants (Fig. 2). The meristem-termination phenotypes were also observed, albeit less frequently, in pol/pol pll1/+ plants, in pol/pol plants with antisense expression of PLL1 and in pol/pol pll1/pll1 plants with incomplete complementation by PLL1 (Fig. 1U-Y). This indicates that these phenotypes are not related to the grafting technique used to generate pol pll1 tissue, but are a consequence of reduced POL/PLL1 activity.
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; Mayer et al.,
1998; Schoof et al.,
2000). The seedling lethality of pol pll1 mutants was
unaffected by the introduction of the putative null clv3-2 mutation.
The ratio between the viable plants and seedling-lethal plants in the progeny
of clv3-2 pol pll1/+ plants (79:31) and the progeny of clv3-2
pol/+ pll1 plants (54:19) did not vary significantly from 3:1
based on 
2 analysis. clv2-1 pol pll1, clv1-7 pol pll1
and clv1-1 pol pll1 triple mutants also exhibited seedling-lethal
phenotypes. To examine the post-embryonic phenotypes, clv3-2 pol pll1 mutants were grafted onto the wild-type hypocotyls. clv3-2 pol pll1 tissue developed in an identical fashion to pol pll1 double-mutant tissue during vegetative and inflorescence development (Fig. 1H,M). The mean number of organs developing in clv3-2 pol pll1 flowers was statistically indistinguishable from that of pol pll1 flowers (Fig. 1R, Fig. 2). These results indicate that pol pll1 is fully epistatic to clv3-2, indicating that POL/PLL1 act downstream of the CLV signaling pathway.
Alteration of stem-cell marker gene expression in pol pll1 mutants
To determine the nature of meristem defects in pol pll1 mutants,
we crossed pol pll1 to well-characterized transgenes in which the
CLV3 and WUS cis regulatory elements drive
ß-glucuronidase (GUS) expression (PCLV3:GUS and
PWUS:GUS) and monitored the expression of these key
meristem regulatory factors (Gross-Hardt
et al., 2002; Lenhard et al.,
2002). For PWUS:GUS, we observed a clear spot
of GUS activity at the shoot meristem in wild-type seedlings, but no signal at
all was observed in pol pll1 seedlings (data not shown). Around the
transition to flowering, when WUS becomes expressed in the many
wild-type flower meristems, we observed occasional punctate spots of
WUS expression in pol pll1 plants
(Fig. 3A-F). These spots
corresponded to expression in internal cell layers of what morphologically
appeared to be nascent meristems (Fig.
3C,F). When compared to PWUS:GUS expression in
wild-type plants, the spots in pol pll1 mutants appeared to
correspond to transient apices forming in leaf axils. These results suggest
that POL/PLL1 are required for the maintenance, but not the initiation, of
WUS expression. Because data indicate that CLV signaling is also
important for maintenance, but not initiation, of WUS expression,
these results are consistent with the hypothesis that POL/PLL1 functions
within the CLV pathway. If CLV signaling achieves repression of WUS
through the inhibition of POL/PLL1 activity, one would expect constitutive
inhibition of WUS in pol pll1 mutants after initiation.
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Ectopic WUS expression bypasses the requirement of POL/PLL1 for stem cells
To definitively test whether the loss of meristem activity in pol
pll1 mutants was the consequence of the loss of WUS expression
maintenance, we designed a transgene arrangement to determine if ectopic
WUS expression could bypass the requirement for POL/PLL1. We set
expression of WUS under the control of the flower-specific
APETALA1 (AP1) cis regulatory elements in a transactivation
system, in which AP1-driven WUS expression would only occur
in the progeny of plants carrying both the PAP1:LHG4
driver and the POP6:WUS responder
(Hempel et al., 1998;
Moore et al., 1998;
Schoof et al., 2000). In
wild-type plants with
PAP1:LHG4/POP6:WUS (hereafter referred
to as PAP1:WUS), flowers underwent extensive meristematic
proliferation and eventual carpeloid organ formation
(Fig. 4A). wus plants
with PAP1:WUS exhibited defective vegetative development
typical of wus mutants; however, upon flowering, these plants
developed vigorous meristem activity in each flower, giving rise to meristem
proliferation and carpeloid organ formation
(Fig. 4D). An identical
restoration of floral-meristem activity was observed when
PAP1:WUS was introduced into pol pll1 grafted
tissue, including extensive meristem proliferation and organogenesis
(Fig. 4B,C).
PAP1:WUS in pol pll1 tissue drove activation of
PCLV3, indicating the meristem-like nature of the
proliferations (Fig. 4E,F).
PAP1:WUS did not drive activation of
PWUS, suggesting that WUS is not under
autoregulatory control (Fig.
4G,H). A similar restoration of meristem activity in pol
pll1 mutants was observed when WUS expression was driven by the
cis regulatory elements for the receptor-kinase ERECTA (ER)
(Diévart et al., 2003;
Yokoyama et al., 1998). Using
the same transactivation transgene arrangement followed by grafting to
generate PER:WUS pol pll1 tissue, we observed restoration
of meristem proliferation that was less extensive than
PAP1:WUS and gave rise to more normal floral organs
(Fig. 4I,J). Thus, the loss of
pol pll1 meristem activity is directly attributable to the loss of
WUS expression maintenance, indicating that POL/PLL1 act through WUS
to promote stem-cell identity.
Ectopic PLL1 expression blocks differentiation in clv mutants
If POL/PLL1 are indeed targeted for negative regulation by CLV signaling,
one would predict that overexpressing POL/PLL1 would enhance clv
mutants, providing de-repression of excess POL/PLL1. Given the extensive gene
families for CLV1, CLV2 and CLV3
(Botella et al., 1997;
Sharma et al., 2003;
Shiu and Bleecker, 2001), and
evidence that clv1 and clv2 null alleles exhibit rather weak
phenotypes (Diévart et al.,
2003; Kayes and Clark,
1998), it is unclear whether any clv single mutant
represents a complete loss of signaling. We have previously shown that
PLL1 overexpression in an otherwise wild-type background gives rise
to weak Clv- phenotypes (Song
and Clark, 2005). Here, we drove PLL1 expression under
the control of both ER (PER) and the cauliflower
mosaic virus (CaMV) 35S (P35S) cis regulatory elements in
the clv2-1 and clv3-2 mutant backgrounds, and observed
dramatic enhancement of the Clv- phenotype
(Fig. 5). In many cases, the
transgenic plants simply produced meristem tissue at the shoot apex, with a
complete absence of organ formation over a long developmental window. Some
plants senesced and died without producing organs, whereas others developed
`escape' tissue, presumably as a result of transgene repression, that went on
to produce a small number of organs after a sustained period without
organogenesis (see Fig. S1 in the supplementary material). To determine
whether the overproliferating tissue was stem cell-like in nature, we
introduced PCLV3:GUS and PWUS:GUS
(Gross-Hardt et al., 2002;
Lenhard et al., 2002) into the
P35S:PLL1 clv3-2 background
(Fig. 5O,P). In both cases, we
observed GUS activity throughout the apex, with the strongest
PWUS:GUS signal in internal cell layers and the strongest
PCLV3:GUS signal in the overlying cells. The presence and
pattern of both meristem markers, as well as the morphology of these
structures, indicate that these accumulated cells are equivalent to the
central zone of a wild-type meristem, including stem cells in the top three
cell layers. This data also indicate that clv mutants have a partial
loss of differentiation that is further antagonized by the overexpression of
PLL1. This is consistent with both a detailed analysis of
clv mutants, as well as a recent study showing that inducible
downregulation of CLV3 leads to the rapid expansion of the
CLV3 expression domain (Reddy and
Meyerowitz, 2005). Indeed, it would be of interest to repeat this
sort of analysis in a PLL1 overexpression background, as
P35S:PLL1 clv3 results in a more complete loss of
differentiation than a clv3 single mutant.
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). Beyond this difference in leaf development,
P35S:PLL1 had no effect that we could detect on the
terminated vegetative or inflorescence meristems observed in wus
mutants (see Fig. S1 in the supplementary material). Similarly, within the
flowers, P35S:PLL1 had no statistically measurable effect
on the number of organs formed in wus flowers. Most importantly, no
increase in the number of stamens or carpels per flower as a result of
PLL1 overexpression was observed
(Fig. 6). wus is thus
fully epistatic to P35S:PLL1 within the meristem,
consistent with the hypothesis that PLL1 acts within the meristem by
regulating WUS.
Overexpression of CLV3 leads to shoot- and flower-meristem
termination, resulting in plants phenotypically similar to wus
mutants, albeit less severe (Brand et al.,
2000). If CLV signaling acts to repress POL/PLL1 activity, then
overexpression of PLL1 in the P35S:CLV3
background would be predicted to suppress, at least partially, the meristem
termination phenotype. Progeny from a cross between plants carrying the
P35S:CLV3 transgene and plants carrying the
P35S:PLL1 transgene were assayed for the shoot-meristem
termination phenotype and genotyped for the presence of the two transgenes.
Whereas every plant carrying P35S:CLV3 alone developed
terminated shoot meristems, 80% of the plants carrying both transgenes
developed normal shoot meristems (Table
1). Transgene expression analysis indicated that this was not the
result of suppression of the P35S:CLV3 transgene (see Fig.
S3 in the supplementary material).
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DISCUSSION |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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It is formally possible that POL/PLL1 act independently on WUS rather than acting as intermediates of CLV signaling, but this alternative hypothesis is not supported by the data. First, pol pll1 mutants do express WUS, albeit only in transient shoots. If POL/PLL1 and CLV were acting separately, one would expect the removal of CLV signaling to expand WUS expression, and hence alter phenotypes, in pol pll1 mutants. Therefore, this alternative hypothesis would predict that clv should suppress, to some extent, pol pll1 double-mutant phenotypes. This is especially true in the flower meristem, where we see transient WUS and CLV3 expression in pol pll1, and these mutants exhibit flower-meristem defects that are slightly weaker than wus. Even here, there is no effect of removing CLV signaling, as evidence by the full epistasis of pol pll1 to clv mutants. In addition, there is an incredible level of dosage sensitivity between CLV, POL/PLL1 and WUS in both loss- and gain-of-function situations, suggesting a common pathway.
CLV repression of POL/PLL1 is likely to be post-transcriptional, based on
both the broad expression of POL and PLL1 throughout the plant and within the
meristem (Yu et al., 2003;
Song and Clark, 2005), and on
the interaction of clv mutants with PLL1 overexpression.
This would be quite typical for receptor signaling intermediates.
Little is known about downstream targets of other receptor kinases.
POL/PLL1 share similarity in general pathway function with the BIN2 kinase in
BRI1 receptor kinase-mediated brassinosteroid signaling
(Li and Nam, 2002). POL/PLL1
and BIN2 appear to be negatively regulated by the corresponding receptor
kinase, and said repression allows for signaling to occur. In the case of BIN2
repression, brassinosteroid signaling occurs as the result of the loss of
BIN2-mediated phosphorylation and subsequent degradation of a set of
transcription factors (Wang et al.,
2002; Yin et al.,
2002; Zhao et al.,
2002). As with BIN2, the exact link between the POL/PLL1 and the
upstream receptor kinase remains unclear. Whether CLV1 directly modulates
POL/PLL1 activity and what are the targets of POL/PLL1 phosphatase activity
are crucial issues to pursue.
pol pll1 mutants have pleiotropic phenotypes, with evidence for
POL/PLL1 regulation of basal embryo development, of pedicel development and of
leaf vascular patterning (Song and Clark,
2005). These activities may represent the function of POL/PLL1
downstream of other receptor kinases. The redundant nature of many receptor
kinases may explain why the corresponding receptors have not yet been
identified (Cano-Delgado et al.,
2004; DeYoung et al.,
2006; Shpak et al.,
2004; Zhou et al.,
2004).
It is of interest to consider that the CLV1-related BAM receptors in
Arabidopsis may also utilize POL and related proteins as signaling
intermediates. bam mutant combinations exhibit many developmental
defects, including effects on leaf vascular patterning similar to those that
result from the overexpression of PLL1
(DeYoung et al., 2006;
Song and Clark, 2005), raising
the possibility that BAM receptors may regulate leaf development by signaling
through POL/PLL1 or related phosphatases. The observation that CLV1 can
replace BAM function during leaf, stem and floral-organ development suggest a
common signaling pathway in each of these different tissues
(DeYoung et al., 2006). Given
the large receptor-kinase gene family in Arabidopsis, it will be
crucial to test the association of specific receptors with potential
downstream intermediates.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/133/23/4691/DC1
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ACKNOWLEDGMENTS |
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Footnotes |
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REFERENCES |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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