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First published online 24 July 2008
doi: 10.1242/dev.023648
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Research Report |
1 Faculty of Biology, Schaenzlestrasse 1, University of Freiburg, D-79104
Freiburg, Germany.
2 Developmental Genetics, Centre for Molecular Biology of Plants, University of
Tübingen, D-72076 Tübingen, Germany.
* Author for correspondence (e-mail: laux{at}biologie.uni-freiburg.de)
Accepted 4 July 2008
SUMMARY
Stem cells are maintained in an undifferentiated state by signals from their microenvironment, the stem cell niche. Despite its central role for organogenesis throughout the plant's life, little is known about how niche development is regulated in the Arabidopsis embryo. Here we show that, in the absence of functional ZWILLE (ZLL), which is a member of the ARGONAUTE (AGO) family, stem cell-specific expression of the signal peptide gene CLAVATA3 (CLV3) is not maintained despite increased levels of the homeodomain transcription factor WUSCHEL (WUS), which is expressed in the organising centre (OC) of the niche and normally promotes stem cell identity. Tissue-specific expression indicates that ZLL acts to maintain the stem cells from the neighbouring vascular primordium, providing direct evidence for a non-cell-autonomous mechanism. Furthermore, mutant and marker gene analyses suggest that during shoot meristem formation, ZLL functions in a similar manner but in a sequential order with its close homologue AGO1, which mediates RNA interference. Thus, WUS-dependent OC signalling to the stem cells is promoted by AGO1 and subsequently maintained by a provascular ZLL-dependent signalling pathway.
Key words: Arabidopsis embryogenesis, Meristem, Stem cell niche, ZWILLE (PINHEAD; AGO10)
INTRODUCTION
Stem cells are located in specialised microenvironments, stem cell niches,
where signals from the neighbouring cells maintain them in a pluripotent
state. This principle was recognised several decades ago in animals and plants
(Schofield, 1978
;
Stewart and Dermen, 1970), but
only recently have the regulatory mechanisms started to be unravelled.
In the wild-type Arabidopsis shoot meristem, three layers of stem
cells are located at the very tip and give rise to all shoot organs formed in
a plant's life. They are maintained in an undifferentiated state by signals
that depend upon expression of the homeodomain transcription factor WUSCHEL
(WUS) in a small underlying cell group termed the organising centre (OC)
(Mayer et al., 1998). The stem
cells in turn express CLAVATA3 (CLV3), a signal peptide that acts to restrict
WUS transcription via the CLV1/CLV2 receptor kinase signalling
cascade (Brand et al., 2000;
Schoof et al., 2000). This
feedback loop between the OC and stem cells provides a mechanism to control
the size of the stem cell pool. Additional pathways have been identified that
work in parallel to the WUS/CLV3 loop in regulating stem cell identity
(Brand et al., 2002;
Lenhard et al., 2002;
McConnell et al., 2001;
Prigge et al., 2005;
Vroemen et al., 2003). Several
studies suggest that during postembryonic development, tissues surrounding the
meristem also provide important information for shoot meristem maintenance
(reviewed by Tucker and Laux,
2007), including the internal (L3) cell layers
(Stuurman et al., 2002;
Szymkowiak and Sussex, 1992)
and the adaxial sides of leaf primordia
(McConnell et al., 2001;
Waites et al., 1998).
Furthermore, the sites of shoot meristem regeneration in tissue culture
(Brossard, 1979;
Projetti and Chriqui, 1986),
in sunflower hybrids (Chiappetta et al.,
2006), or after KNOTTED-LIKE HOMEOBOX (KNOX;
also known as KNATM-TAIR) overexpression
(Chuck et al., 1996;
Nishimura et al., 2000),
correlate with the position of vascular cells. However, the underlying
mechanism remains elusive.
Little is known about how the shoot meristem stem cells are formed in the
embryo. After separation of protoderm and inner cells, the onset of
WUS expression in four sub-epidermal apical cells of the 16-cell
embryo, which after several asymmetric cell divisions give rise to the OC
(Laux et al., 2004), is the
first indication of stem cell niche development during Arabidopsis
embryogenesis. At the same stage, the cells below the OC precursor cells start
to elongate and form the vascular primordium
(Jürgens and Mayer, 1994;
Mansfield and Briarty, 1991).
The shoot meristem stem cells, however, cannot be distinguished before the
middle stages of embryogenesis, when expression of CLV3 is detected
(Fletcher et al., 1999).
Mutagenesis screens identified the ARGONAUTE (AGO) family member
ZWILLE (ZLL; also known as PINHEAD and
AGO10) as a factor involved in shoot meristem development
(Lynn et al., 1999;
Moussian et al., 1998). AGO
proteins have been revealed as central components of RNA-induced silencing
complexes (RISC) in animals and plants, where they bind small RNA molecules to
target messenger RNAs for degradation, translational inhibition, or genomic
DNA for methylation (reviewed by Peters
and Meister, 2007; Vazquez,
2006). zll mutant embryos form terminally differentiated
cells and organs instead of shoot meristem stem cells
(Lynn et al., 1999;
Moussian et al., 1998), but
the mechanism underlying the function of the ZLL gene has remained
unclear. Notably, meristems formed postembryonically can give rise to fertile
plants with indeterminate inflorescences, indicating that ZLL is
specifically required for embryonic shoot meristem development.
In this study we provide direct evidence that during embryonic patterning, ZLL acts from the emerging vascular primordium to mediate WUS function and maintain shoot meristem stem cells in an undifferentiated state, thereby indicating the presence of a novel signalling pathway downstream of ZLL.
MATERIALS AND METHODS
Plant work
Plants were grown as described previously
(Laux et al., 1996). The
zll-1, zll-15 (Moussian et al.,
1998) and ago1-8
(Newman et al., 2002) mutants
are in the Landsberg erecta (Ler) background and
ago1-1 (Bohmert et al.,
1998) is in the Columbia background. The respective wild-type
plants were used as controls. Transgenic ago1-1 lines were
backcrossed to Ler and showed the same effect as the original
Columbia lines.
|
) with
CFP. For the pZLL:YFP-ZLL gene, a modified YFP
sequence lacking a stop codon was inserted immediately prior to, and in frame
with, the ZLL coding sequence in the context of an 8 kb genomic
fragment. The ZLL promoter was then replaced with the ARR5, AS1,
AS2 and ATHB8 promoters (sequences of primers used to amplify
these promoters are available upon request) to generate tissue-specific
expression constructs. The gWUS-GFP3 transgene contains a
3xGFP gene inserted immediately prior to the stop codon of a 15 kb
BamHI genomic fragment of WUS. For ectopic WUS
expression with the pOpL two-component system
(Moore et al., 1998), the
ATRPS5A promoter (Weijers et al.,
2001) was fused to the synthetic transcription factor gene
LhG4, transformed into plants as the driver line, and crossed to an
effector line carrying the pOp:WUS(69.3) construct
(Schoof et al., 2000). F1
progeny carrying both transgenes were germinated on 1/2 MS media and scored
for phenotype at 4 and 11 days post-germination. All plasmids were introduced
into Agrobacterium tumefaciens strain GV3101 [pMP90
(Koncz and Schell, 1986)] and
transformed into plants using the floral dip method
(Clough and Bent, 1998).
Microscopy and image analysis
Embryos were dissected from ovules on slides using fine-tip syringes in 10%
glycerol and viewed on an Axioscope fluorescence microscope (Zeiss). Embryos
were stained with DAPI (1 mg/mL) for 5 minutes and mounted in 50% glycerol in
1xPBS. Images were captured using Axiovision 4.4 software (Zeiss) and
figures were generated using Photoshop 7.0 (Adobe).
RESULTS AND DISCUSSION
Histological sections of zll embryos revealed no abnormalities in
stem cell development until late stages of embryogenesis, when the cells at
the stem cell position, unlike the small pluripotent stem cells in the wild
type, enlarge and become vacuolated, indicating their differentiation. This
defect is incompletely penetrant in all known zll alleles, and even
in the strongest alleles only 90% of the seedlings lack functional stem cells,
whereas the remaining seedlings are indistinguishable from wild type. To study
how ZLL affects stem cell development in the embryo, we analysed
expression of the shoot meristem stem cell marker pCLV3:GFP-ER
(Lenhard and Laux, 2003). No
difference was observed in the pCLV3:GFP-ER expression pattern
between zll-1 and wild-type embryos from the earliest detection at
transition stage until the early torpedo stage
(Fig. 1, compare A,B with D,E;
see Table S1 in the supplementary material), suggesting that ZLL does
not have a discernable role in the establishment of CLV3 expression.
However, from torpedo stage onwards, when pCLV3:GFP-ER extended into
the three layers of stem cells in wild type
(Fig. 1B,C), in the majority of
zll-1 embryos the intensity and number of cells expressing
pCLV3:GFP-ER gradually decreased
(Fig. 1E,F; see Table S1 in the
supplementary material). The frequency of embryos showing strongly reduced or
no pCLV3:GFP-ER expression correlates closely with the frequency of
zll-1 seedlings lacking the shoot meristem (compare Table S1 with
Table S6 in the supplementary material). This suggests that ZLL activity is
required to maintain stem cells of the embryonic shoot meristem, but not to
initiate them.
In previous studies, ZLL mRNA was detected throughout the embryo
at early globular stage and subsequently became restricted to the vasculature
and, at lower levels, to the shoot meristem and the adaxial sides of the
cotyledons (Lynn et al., 1999;
Moussian et al., 1998). By
contrast, using anti-ZLL antibodies, ZLL protein was only detectable in the
vascular primordium of whole-mount embryos
(Moussian et al., 2003). To
clarify this discrepancy, we constructed an YFP-ZLL fusion protein that
rescued the zll-1 mutant phenotype (see Table S2 in the supplementary
material) when expressed from the ZLL promoter. YFP-ZLL fusion
protein was first detected in all cells of the proembryo between the 2-cell
(Fig. 2A) and 8-cell stages.
During subsequent stages, YFP-ZLL became restricted to the emerging vascular
primordium (Fig. 2B) and the
adaxial domain of the cotyledons (Fig.
2C,D), but was barely detectable in the shoot meristem until
maturity, when expression there increased (see Fig. S1 in the supplementary
material). Thus, YFP-ZLL localisation closely mimicked the ZLL mRNA
expression pattern, indicating that all cells where mRNA is detected also
produce ZLL protein. It is plausible that the failure to detect ZLL protein in
the shoot apex and the adaxial cotyledons in previous studies was due to the
lower sensitivity of whole-mount immunodetection in this experiment.
Based on this dynamic expression pattern, the shoot meristem,
(Moussian et al., 1998), the
adaxial side of the cotyledons (Lynn et
al., 1999; Newman et al.,
2002), and the vasculature
(Moussian et al., 2003) have
been discussed as potential sites of ZLL function in embryonic stem cell
development. To clarify this, we first compared pZLL:YFP-ZLL
expression with that of the stem cell niche markers
gWUS-GFP3 and pCLV3:CFP-ER during all relevant
stages of embryogenesis. At the early globular stage, the
gWUS-GFP3-expressing OC precursor cells were completely
encompassed by strong YFP-ZLL expression
(Fig. 2B). However, from the
transition stage until late torpedo, when abnormal differentiation of stem
cells in zll-1 embryos is observed, YFP-ZLL was barely detectable in
either the OC or stem cells (Fig.
2C-E). To determine where ZLL is necessary for meristem
development, the YFP-ZLL fusion protein was expressed using different promoter
sequences at specific embryo stages and in specific embryonic regions
overlapping with the endogenous ZLL expression pattern
(Fig. 3). The expression
pattern of each transgene was verified by localisation of the YFP signal, and
function was assayed by rescue of shoot meristem stem cells in the
zll-1 mutant (Fig. 3;
see Table S2 in the supplementary material). Notably, ZLL expression
in the stem cells via the CLV3 promoter
(Fig. 3D-F) and in adaxial
tissues of the cotyledons via the ASYMMETRIC LEAVES 2 (AS2)
(Iwakawa et al., 2002)
promoter (Fig. 3G-I) was unable
to rescue stem cell development in zll-1 embryos. By contrast,
expression of YFP-ZLL restricted to the vascular primordium
(Fig. 3J-L) from the
Arabidopsis HOMEOBOX GENE 8 (ATHB8)
(Baima et al., 1995) promoter
did rescue stem cell maintenance. Importantly, co-expression with the
gWUS-GFP3 or pCLV3:CFP-ER reporter genes
demonstrated that pATHB8:YFP-ZLL expression does not overlap at any
stage in embryo development with the cells that give rise to the shoot
meristem stem cell niche (Fig.
2F). Thus, ZLL function in the vascular primordium appears to be
sufficient for stem cell niche development, indicating a non-cell-autonomous
function, whereas its expression in the stem cells and adaxial sides of the
cotyledons is neither required nor sufficient for stem cell maintenance.
Notably, expression of YFP-ZLL in the vascular primordium of the
embryo axis from the ARABIDOPSIS RESPONSE REGULATOR 5 (ARR5)
(D'Agostino et al., 2000)
promoter (Fig. 3M-O), or in the
apical parts of the embryo (including the vascular primordium of the
cotyledons) via the ASYMMETRIC LEAVES 1 (AS1)
(Byrne et al., 2000) promoter
(Fig. 3P-R), led to a complete
rescue of the zll-1 phenotype. Since both expression domains overlap
only in the provascular cells that lie immediately underneath the stem cell
niche, these cells might have a specific role in stem cell maintenance.
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).
ATRPS5A directs expression predominantly to basal parts of the young
embryo, to the whole embryo until torpedo stage and thereafter mainly to the
meristem and cotyledons, at levels indistinguishable between wild type and
zll (see Fig. S3 in the supplementary material).
ATRPS5A>>WUS expression in a wild-type background led to stunted
growth, ectopic outgrowths on the hypocotyl
(Fig. 4H) and seedling
lethality in the majority of cases (see Table S5 in the supplementary
material), consistent with disturbed organ differentiation as reported
previously (Brand et al., 2002;
Gallois et al., 2002;
Lenhard et al., 2002). These
effects were suppressed by the zll-1 mutation
(Fig. 4, compare H with J; see
Table S5 in the supplementary material), despite similarly high levels of
WUS mRNA accumulation compared with the wild-type background (see
Fig. S3 in the supplementary material), indicating that ZLL is
necessary also for ectopic WUS function in the embryo. Taken together, these results suggest that ZLL-dependant signalling from the vascular primordium maintains stem cells during embryogenesis by potentiating WUS signalling from the OC to the stem cells. Since expansion of the WUS domain coincided closely with the stages when pCLV3:GFP-ER expression began to decrease, it is plausible that the failure to maintain CLV3 function in zll embryos might in turn account for derepression of WUS transcription.
Because previous studies showed that the ZLL and AGO1
genes share overlapping function during early embryogenesis
(Lynn et al., 1999), we
investigated whether AGO1 might also have a function in potentiating WUS
signalling. Since double mutants between strong zll and ago
alleles are embryo lethal, we generated zll mutants with partially
altered levels of AGO1 activity, similar to previous studies that
considered flower and leaf development
(Lynn et al., 1999). By
reducing AGO1 gene dosage to one functional copy, we found that stem
cell defects in weak zll-15 mutants were enhanced to the severity of
the null allele zll-1 without any other obvious effect on seedling
development. In the complementary experiment, an increase of AGO1
gene dosage to three copies reduced the severity of stem cell defects in
zll-1 (see Table S6 in the supplementary material).
Consistent with these data, ago1-1 embryos showed defects in gWUS-GFP3 expression similar to those observed in zll-1. The majority of homozygous ago1-1 embryos showed an expanded and disorganised domain of gWUS-GFP3 expression from as early as the transition to heart stage (see Fig. S4A and Table S7 in the supplementary material), and by maturity the domain was much broader than in segregating wild-type siblings (see Fig. S4B-D in the supplementary material). Unlike zll-1, however, most ago1-1 embryos failed to initiate pCLV3:GFP-ER expression at the correct stage (see Fig. S4E and Table S8 in the supplementary material), despite strong expression of gWUS-GFP3. Only at later stages of embryogenesis (see Fig. S4F and Table S8 in the supplementary material) did ago1-1 embryos gradually recover pCLV3:GFP-ER expression to wild-type-like levels (see Fig. S4G,H and Table S8 in the supplementary material), coinciding with the approximate stage when ZLL becomes required for meristem maintenance. Therefore, whereas both ZLL and AGO1 appear to be required for normal expression of WUS, their affects on CLV3 expression appear to be temporally separated. One plausible model is that AGO1 and ZLL act sequentially in stem cell development, with AGO1 being essential for initiation of the stem cell programme until heart/torpedo stage and ZLL for its maintenance during embryo maturation. In future studies it will be intriguing to determine whether AGO1, like ZLL, is a component of non-cell-autonomous signalling from provascular tissues during embryogenesis. Notably, ago1 mutants display pleiotropic effects and are sometimes seedling lethal, indicating that AGO1 has additional functions that cannot be rescued by late ZLL expression.
Taken together, our results provide direct evidence that the vascular
primordium, which is one of the first discernable tissues to form in the
developing Arabidopsis embryo, plays an instructive role during
embryonic stem cell development. This function is mediated by a
ZLL-dependent signalling pathway, which, based on homology to AGO1
and recent studies of ZLL (Brodersen et
al., 2008), is consistent with a role for small RNAs in this
process. Since pATHB8:YFP-ZLL signal was not detectable outside of
the provascular tissues during embryogenesis, it is likely that ZLL itself
does not move and thus might be involved in the production or the transmission
of a signal to the stem cell niche. The nature of this signal is currently
elusive, but its central role in early vascular function makes the
phytohormone auxin a plausible candidate to be tested in the future. As a
consequence of this vascular-borne signal, WUS signalling from the OC
is enabled to maintain the stem cells in an undifferentiated state. This could
involve modulation of WUS function in the OC cells, or an effect on
the competence of stem cells to respond to the WUS-dependent signal.
Further studies aimed at elucidating the precise mechanism of ZLL function are
necessary to distinguish between these models.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/135/17/2839/DC1
ACKNOWLEDGMENTS
We thank Minako Ueda, Ivo Rieu, other members of the Laux laboratory and Dominique Chriqui for critical comments and discussions; Philipp Graf, Yuval Eshed and Herve Vaucheret for constructs and seeds; and Nikolai Adamski, Nico Lindau and Matthias Blender for technical assistance. This work was supported by grants from the Deutsche Forschungsgemeinschaft and the BMBF (T.L.), the Landesgraduiertenförderung Baden-Württemberg (A.H.), and an EMBO long-term fellowship (M.R.T.).
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