1 Lehrstuhl für Genetik, Technische Universität München,
Wissenschaftszentrum Weihenstephan, Am Hochanger 8, 85350 Freising,
Germany
2 Bayerische Landesanstalt für Landwirtschaft, Institut für
Pflanzenbau und -züchtung, IPZ 1b, Am Gereuth 2, 85354 Freising,
Germany
3 Institut für Pathologie, GSF-Forschungszentrum für Umwelt und
Gesundheit GmbH, 85764 Neuherberg, Germany
Author for correspondence (e-mail:
ramon.torres{at}wzw.tum.de)
Accepted 5 July 2005
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SUMMARY |
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Key words: laterne, PINOID, ENHANCER OF PINOID, Embryo, Arabidopsis, Pattern formation, Auxin, PIN1, Organogenesis, Cotyledons
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Introduction |
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Aerial organs, e.g. leaves, are believed to be induced when local
(initially stochastic) concentrations of auxin form. This hormone is
transported in the epidermal layer towards the incipient organ primordium to
give rise to groups of cells that accumulate high concentrations of auxin at
its tip, which itself might produce auxin
(Benkova et al., 2003;
Ljung et al., 2001
). From
these sites, auxin is transported downwards through the vascular elements in
direction to the root. In the aerial organs, the directed auxin transport is
promoted by the PIN1 transport facilitator, which is located at apical sites
in the epidermis and at basal sites in the stele
(Gälweiler et al., 1998
;
Benkova et al., 2003
). Studies,
including microapplication experiments, suggest that a developing leaf
depletes local auxin pools and determines the spatial arrangement of the next
maximum (phyllotaxis) (Reinhardt et al.,
2003
). Whether auxin maxima are required for the initiation and/or
maintenance of cotyledon primordia remained to be determined.
The establishment of a comprehensive model for the pattern formation in the
Arabidopsis embryo has been hampered by the absence of
cotyledon-specific genes (Berleth and
Chatfield, 2002). Analyses of several Arabidopsis mutants
found in embryonic pattern screens (e.g.
Mayer et al., 1991
;
Scheres et al., 1995
) showed
that the generation of cotyledons is notoriously sensitive to disturbances in
diverse biological processes. For example, the reduction to complete
elimination of cotyledons occurs in gurke and
pepino/pasticcino2, which are thought to regulate cell proliferation
(Torres et al., 1996a
;
Haberer et al., 2002
;
Baud et al., 2004
). Mutations
in a number of genes related to auxin transport or sensing give rise to
seedlings with fused cotyledons or altered cotyledon numbers
(Okada et al., 1991
;
Berleth and Jürgens, 1993
;
Mayer et al., 1993
;
Bennett et al., 1995
;
Geldner et al., 2004
;
Friml et al., 2004
). A
deletion of the cotyledons occurs especially when two or more such mutants are
combined, as observed in quadruple mutants of pin-formed1, pin-formed3,
pin-formed4 and pin-formed7
(Friml et al., 2003
).
Recently, Furutani et al. (Furutani et
al., 2004
) have shown that the double mutant pin1 pid
results in
50% cotyledonless seedlings. In contrast to the above
mentioned genes, which affect a number of organs (or, which have pleiotropic
effects), laterne mutants are characterized by a specific and precise
deletion of the cotyledons.
The laterne phenotype is caused by a combination of two mutations, one in PINOID and the other in an unknown gene designated ENHANCER OF PINOID, and is characterized by a specific and precise deletion of the cotyledons. The detection of ENP uncovers a cotyledon specific genetic programme and provides a new gateway for understanding cotyledon development and the impact of auxin in the embryo apex.
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Materials and methods |
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Genetic analyses and mapping
The homozygous enp/enp line originated from the selfing of a line
carrying one pid-15 and at least one enp allele. As the
enp phenotype is subtle, the presence of enp/enp, in all
genotype combinations generated by conventional crosses, was confirmed by
crossing with pid-alleles and checking following generations for the
occurrence of laterne seeds (see Fig. S1 and Table S1 in the
supplementary material). Segregation analysis showed that enp
exhibits full penetrance (see Table S2 in the supplementary material). Generation of homozygous pid-15 enp stm-5 mutants was
performed by generating pid-15 enp stm-5/+ enp +
plants. These segregated only three classes of seedling phenotypes: wild type,
stm and laterne. This progeny was then subjected to analysis
by pyrosequencing, which scored for homo- or heterozygosity in both the
STM and the PINOID gene. We analysed 102 wild-type, 62
laterne and 41 stm seedlings or adult plants (the numbers do
not represent segregation as seedlings were processed as they grew).
Simultaneous homozygosity for pid-15 and stm-5 was detected
only in the fraction of laterne seedlings. In addition, pid-15 +
stm-5/pid-15 + + plants were generated, which produce seedlings with
either pinoid or stm-5 phenotypes (19/67 with stm
phenotype). Mapping of the ENP locus was carried out with CAPS and
the complete set of SSLP markers as described
(Lukowitz et al., 2000;
Haberer et al., 2002
) by using
F2 laterne plants (genotype pid-15 enp/pid-15 enp, but see
below). These had been generated by crosses of pid-15 enp/+
enp with the polymorphic ecotypes Col and Nd
(Erschadi et al., 2000
).
Primers were: 5'-GGACGTAGAATCTGAGAGCTC-3' and
5'-GGTCATCCGTTCCCAGGTAAAG-3' for G4539 (CAPS marker); and
5'-AATTTGGAGATTAGCTGGAAT-3' and
5'-CCATGTTGATGATAAGCACAA-3' for ciw7 (SSLP marker). The formula
p=1-
(1-x) was used for linkage calculation (x=ratio
of recombinant plants; p=calculated recombination frequency) correcting for
p-values greater than 10% using the Kosambi function. The linkage found was
18.9 cM (76/233 recombinants for G4539) and
9.9 cM (44/233
recombinants for ciw7). In rare cases, pid homozygous plants produce
leaky laterne seeds (see Table S3 in the supplementary material). However, the resulting differences to the genetic distance values given above
are negligible.
Microscopy
Semi-thin sections and whole mount analysis of embryos and seedlings were
carried out as previously described
(Haberer et al., 2002).
Photographs were taken using a ZEISS Axiophot 1 microscope with 35 mm in
system cameras (MC80 DX) or an adapted Kodak DCS760 system (with Digital Nikon
camera F5SLR) with corresponding software (Kodak Photo Desk DCS).
Epifluorescence microscopy on the same Axiophot used a HBO50 UV/Light-source
with an AHF filter system F41-017. Laser-scanning microscopy was performed on
a Zeiss LSM 510 META with an 488 nm Argon-Laser. The promotor GFP fusion
DR5rev::GFP and the translational fusion PIN1:GFP have been
previously described (Benkova et al.,
2003
; Friml et al.,
2003
).
Auxin transport measurements
Polar auxin transport was determined essentially as described
(Okada et al., 1991). Stem
segments (2.5 cm; 0.5 to 3.0 cm from the base) were inverted and placed in a
solution of 14C-IAA (0.1 µCi/ml) in 5 mM MES (pH 5.7)/1%
sucrose. After 24 hours the stem segments were dried on filter paper for 5
minutes and then analyzed after autoradiography for a minimum of 10 days using
a Storm 860 phosphoimager. For each stem segment 14C-IAA was
quantified in the basal 4 mm (see Table S4 in the supplementary material).
RT-PCR and (Pyro-)sequencing
RNA isolation, reverse transcription and PCR were performed according to
the supplier's instructions using a NucleoSpin-RNA Plant kit (Macherey-Nagel)
and a TaqMan kit (Applied Biosystems, Roche), respectively (Fig. S2).
PCR bands, generated from pid-15 and stm-5 DNA as template, were sequenced using the BigDye® Terminator v1.1 Cycle Sequencing Kit on an ABI prism sequencer according to the manufacturer's instructions. The data were analysed with the Lasergene Seq ManTM II programme by DNA STAR.
Pyrosequencing reactions were performed by the PSQ MA 96 system (Biotage, Sweden) using ThermoStart DNA Polymerase (ABGene, Germany) according to the manufacturer's protocols. Primers, designed using the Pyrosequencing Assay Design Software version 1.0.6., were as follows: 5'-CATGCGCGGAATTTGATTT-3'; Biotin-5'-CTTGACGACGGAAGAAGGAATC-3'; and 5'-GATCCGACTAAAAGACTTG-3' for PID/pid-15; 5'-CCCTAAAGAAGCTCGTCAACA-3'; Biotin-5'-AGTATGGATGCAAAAATCACAAA-3' and 5'-TGGCCTTACCCTTCG-3' for STM/stm-5.
In situ hybridisation analyses
In situ hybridization was essentially performed as described
(Schoof et al., 2000). Sense
probes were used as controls and wild-type expression patterns for all probes
were confirmed. Hybridisations were performed at 50°C with the
CUC2 probe and the WUS probe and at 55°C with the
ANT and the STM probe, respectively. We evaluated 69 embryos
(10/69 laterne) with CUC2, 96 embryos (23/96
laterne) with WUS, 40 embryos (11/40 laterne) with
ANT and 64 embryos (12/64 laterne) with STM
(numbers are not representative for segregation; embryos were selected
depending on quality and orientation). Templates for transcription were kindly
provided by K. Barton (merih5-clone with STM gene)
(Long et al., 1996
), D. Smyth
(ANT gene) (Elliott et al.,
1996
), M. Aida (CUC2 gene)
(Aida et al., 1999
) and T. Laux
(WUS gene) (Mayer et al.,
1998
).
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Results |
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|
The laterne phenotype is caused by two mutations: pinoid and enhancer of pinoid
ENHANCER OF PINOID was uncovered by outcrossing laterne
to Ler and other ecotypes. The resulting progeny lines segregated
either wild-type, laterne and/or a second seedling phenotype with
three cotyledons. These seedlings elaborated pin-like stems with abnormal
flowers (Fig. 4), reminiscent
of the mutants pinformed1 (pin1) and pinoid
(pid) (Okada et al.,
1991; Bennett et al.,
1995
). Complementation analyses with pin1 and
pid indicated that the observed mutation represents a new allele of
pinoid, (designated pid-15) harbouring a point mutation
changing G to E at position 380, a conserved amino acid residue of the
PINOID kinase. As outcrossing did not reveal an obvious third
phenotype, we suspected that a second gene behaving as a modifier, induced the
laterne phenotype in concert with pinoid. We termed this
modifier enhancer of pinoid (enp), as it strengthens the
pinoid seedling phenotype such that cotyledons are completely missing
instead of being supernumerary. Outcrossing led to the isolation of a line
that exhibits the genotype + enp/+ enp (`+' stands for
wild-type allele of PINOID). Seeing that enp mutants have an
almost negligible phenotype (see below), the presence of enp was
always scored in pid background. Accordingly, enp/ENP was
mapped by analysing laterne plants (see Materials and methods).
ENP maps to the lower arm of chromosome four, 9.9 cM south of ciw7.
As expected laterne plants also show linkage to second chromosome
markers due to the mutation in PINOID (not shown).
|
|
|
We tested, with respect to cotyledon formation, whether enp could
act as enhancer of loci other than pid, notably pin1, cuc1
and cuc2, as these mutants exhibit cotyledon defects partly similar
to those seen in pinoid mutants
(Okada et al., 1991;
Bennett et al., 1995
;
Aida et al., 1997
). In no case
did we recover laterne seeds from F1 plants that were heterozygous
for enp and one of these mutant loci. We conclude that during
embryogenesis enp acts as a specific enhancer of pid.
ENP is required in late adult stages
Analysis of homozygous and heterozygous enp alone, as well as all
heterozygous combinations of enp and different pinoid
alleles revealed mild but significant floral defects in adult plants. Most
notably fused organs and a variation in organ number were observed (Figs
4,
5). Ler exhibits (less
pronounced) divergence in organ numbers
(Fig. 5). Adult pid-15
enp and pid-2 enp homozygous plants elaborate stems with blind
ends. These mutants completely lack floral structures but occasionally
generate terminally stigmatic tissue (not shown). This enhancement of
pinoid floral defect by enp, however, depends on the genetic
background, as combinations of enp with pid-8 and
pid-9 originating from other backgrounds produce at least some,
though sterile, abnormal flowers (Figs
4,
5). This notion is supported by
outcrossing pid-15 enp (Ler background) to Col, which led to
(rare) laterne plants with few floral structures (not shown).
Considering different allele and background combinations, we found only two
consistent effects in homozygous enp pid double mutants: significant
reduction of sepals and sterility because of a reduction of gynoecia.
|
The position of PIN1 in epidermal cells of the laterne embryo apex is reversed
ENP could act on PINOID in a variety of different ways. We tested two
hypotheses: first, that it may affect on transcription; and second, that it
may affect on auxin transport. RT-PCR analysis revealed that pid
transcripts are still present in laterne seedlings (see Fig. S2 in
the supplementary material) showing that ENP does not regulate
PID transcription.
We tested net auxin flux as well as the polarity of auxin transport in both pid and laterne mutants. Auxin transport is not completely abolished in stems of pinoid plants (Bennet et al., 1995). Both pinoid and laterne showed a significant reduction in comparison with the wild type (Materials and methods; see Table S4 in the supplementary material). However, a significant difference in polar 14C-IAA transport between pinoid and laterne was not observed. Thus, enp, in pid homozygous background, does not further reduce auxin transport in stems.
We then assessed the polarity of auxin transport by analysing the cellular
position of PIN1 in the epidermis at the apex of wild-type, pid and
laterne embryos. Laser-scanning microscopy was carried out
predominantly on embryos at mid heart and torpedo stages, as clear polar
PIN1-position was difficult to discern in globular to early heart stages, in
both mutant and wild-type embryos (Fig.
6). All laterne embryos analysed (n>50)
showed a striking reversal of polar PIN1 position when compared with wild-type
(n>80) and pid embryos (n>50). Generally,
three or four cell rows of the apex of laterne embryos carry
detectable amounts of PIN1:GFP in the plasma membrane. Owing to the intense
signalling, we cannot exclude PIN1 localisation on the apical side of cells in
the upper rows. However, the predominant or exclusive position is clearly at
the lateral and basal sides of the cells in laterne, where it is
particularly well seen in the most basal cell rows
(Fig. 6A-C). Pronounced lateral
positioning of PIN1 is also found in the SAM region and increasingly towards
the tips of cotyledon primordia in wild-type
(Fig. 6D-F) and pid
embryos (Fig. 6G,H). However,
at the basal and mid region of wild-type cotyledon primordia, PIN1 is clearly
localised at the apical side of the cells
(Fig. 6D-F)
(Steinmann et al., 1999;
Benkova et al., 2003
).
Interestingly, although PIN1 changes its cellular position from apical to
basal in apices of adult pinoid mutants
(Friml et al., 2004
), the
situation is more complicated in cotyledon primordia of pid-15
homozygous embryos. We detected apical positioning as seen in wild-type but
frequently, even within the same primodia, we saw cells with basal
localisation (Fig. 6G,H).
|
Expression domains of meristem and organ specific genes in laterne embryos
The first morphological manifestation of the pid enp double
mutation becomes visible at the early heart stage (compare
Fig. 3 with Figs
8,
9). We carried out in situ
hybridisation analyses with genes controlling the organisation of the embryo
apex. Obvious alterations of gene expression were only observed in embryos
that could be identified as laterne by their morphology (i.e. from
triangular/early heart stage onwards). The analyses did not reveal conspicuous
deviations of gene expression from wild-type for + enp/+ enp
embryos.
In globular stage embryos, the transcription of STM displays a median stripe-like pattern indicating the anlagen of future shoot apical meristem (Fig. 8A,B). Later on STM is restricted to the central domain of this region (Fig. 8D,G). Alterations become visible in laterne from the triangular or early heart stage onwards (Fig. 8C,E), such that STM expands along the whole apical region (Fig. 8F,H). Interestingly, radial sections of this domain show that different embryos display a variability of expression, such that smaller regions with stronger and other with weaker signal strength appear (Fig. 8C,F,H).
|
CUC2 expression overlaps with STM in the globular embryo and forms later a `ring' separating shoot meristem and cotyledons (Fig. 8Q,R,T,U,W). Similar to ANT, the CUC2 localisation embraces the whole apical pole with patch-like patterns (Fig. 8V). In addition, it is sometimes also found in the centre (Fig. 8S,V,X). In wild-type as well as laterne, the expression patterns of ANT and CUC2 are partly overlapping in early stages and then separate in later stages. Expression of ANT, CUC2 and STM in tricotyledoneous pid-15 +/pid-15 + embryos, as well as the topology of the apical pole (not shown), was comparable with that in wild type (see Fig. S3 in the supplementary material; the domain of STM was slightly enlarged). Two GUS constructs suggest that other genes organising the topmost meristem region, such as KNAT2 and CUC3, exhibit similar alterations (see Fig. S4 in the supplementary material).
In wild-type the WUS domain initially embraces the internal (non-epidermal) cells in the upper half of the 16-cell stage. With progressing development, WUS is restricted to a few cells in L3 immediately neighboured to the vascular precursor cells of the central cylinder (Fig. 9A-C,E,G). We reasoned that in laterne, this cell group is localised in a region that morphologically displays wild-type organisation. In fact, in situ analysis shows that WUS expression is almost the same in laterne and wild-type embryos (Fig. 9).
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Discussion |
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The SAM in laterne mutants is enlarged and indented. Possibly, the
presence of cotyledons is required during embryogenesis to define and organise
the SAM properly (Torres Ruiz,
2004). This would be reminiscent of postembryonic development
where genes expressed in the adaxial and abaxial sides of leaves are thought
to influence SAM development (Siegfried et
al., 1999
; Sawa et al.,
1999
; McConnell et al.,
2001
; Kerstetter et al.,
2001
; Kumaran et al.,
2002
; Tsukaya,
2002
). Double mutant combinations of cuc1, cuc2 and
cuc3 genes, which develop one fused cotyledon and no SAM, suggested a
requirement of bilateral symmetry and cotyledon boundaries for SAM formation
(Aida et al., 1997
;
Aida et al., 1999
;
Vroemen et al., 2003
).
However, deletion of cotyledons causes loss of bilateral symmetry in
laterne but is not a prerequisite for SAM formation.
Dose effects indicate tight genetic interaction between ENHANCER OF PINOID and PINOID
The synergistic effect of the pid and enp mutations are
indicative of a genetic interaction during early embryogenesis. We detected
dose-dependent effects, which suggest an additional tight interaction at late
adult development. The homozygous enp adult phenotype is very subtle,
yet with addition of a single pid mutant allele the frequency and
expressivity of this phenotype, i.e. fused sepals, is greatly enhanced.
Similarly, a single enp mutant allele has an effect on the fertility
of pid mutants. Such dose effects might, for example, be due to
physical interaction of the participating gene products. However, ENP
(as inferred from its position) has not been detected as an interactor of PID,
in yeast-two-hybrid screens (Benjamins et
al., 2003). Therefore, further work will be necessary to clarify
the mode of interaction between these two genes.
|
STM activity in wild-type embryos functions to maintain SAM cells
in an undifferentiated state. The expanded STM domain in
laterne mutants might likewise act to maintain cells that would
normally give rise to cotyledons in an undifferentiated state. A comparable
observation has been made in pin1 pid double mutants, which
frequently lack cotyledons. Interestingly cotyledon development is partially
recovered in pin1 pid stm
(Furutani et al., 2004),
suggesting that a basic developmental machinery for cotyledon development was
suppressed in the double mutant. Similarly, in post-embryonic development,
simultaneous elimination of the competing activities of STM and
AS1 leads to (partial) meristem recovery
(Byrne et al., 2000
). The
triple mutant pid enp stm revealed that loss of STM function
can be (partly) overcome to produce rosette leaves on top of the apex. Note,
however, that in stm mutants, leaves occasionally emerge from the
hypocotyl (Barton and Poethig,
1993
). More importantly, the pid enp stm homozygous
mutant displays a laterne seedling phenotype. Thus action of
ENP cannot be bypassed, as shown in the STM PID PIN1
`pathway', to rescue the generation of cotyledons. Rather, this analysis
suggests that PIN1, PID and ultimately ENP partly control STM
expression. The molecular mechanism remains unclear but recently it has been
reported that, for example, PIN genes restrict expression of PLETHORA
genes, major determinants of root stem cell specification
(Blilou et al., 2005
).
ENP appears to exert its effect by specifically reverting the polarity of auxin transport in the pinoid background
The Ser/Thr kinase PINOID has recently been shown to control polar
targeting of the PIN1 auxin transport facilitator in plasma membranes of
epidermal cells of the inflorescence meristem. Loss-of-function pid
mutations result in basal, rather than apical, targeting of PIN1
(Friml et al., 2004). This
reverses auxin transport away from presumptive organ primordia and abolishes
the accumulation of auxin maxima, the reference points for organ formation
(Benkova et al., 2003
;
Reinhardt et al., 2000
;
Reinhardt et al., 2003
).
Consequently, pinoid mutants display abnormal or missing (floral)
organs and disturbed phyllotaxis (Bennett
et al., 1995
; Christensen et
al., 2000
; Benjamins et al.,
2001
; Friml et al.,
2003
; Reinhardt et al.,
2003
).
In line with observations regarding the importance of auxin for cotyledon
formation (e.g. Hadfi et al.,
1998), mutations in PID as well as in PIN1 cause
abnormal cotyledon numbers. Notably, these mutants do lead to cotyledon
abnormalities but not to loss of cotyledons (with rare exceptions). One
possibility to explain this is that redundant homologs mask cotyledon effects
of the single mutants. For example, root development is guided by the combined
action of several PIN genes; single mutants have relatively mild effects
(Friml et al., 2003
;
Blilou et al., 2005
).
Similarly, as PID belongs to a gene family with 23 members in
Arabidopsis (Friml et al.,
2004
), multiple PID genes could control cotyledon development. By
virtue of position and preliminary sequence data (we sequenced a
PID-like candidate gene residing in the mapped region), ENP
is not a PID (nor a PIN) homolog. However, if other members of these
families are recruited for cotyledon development, ENP could possibly
enhance more than one gene. Cloning of ENP and molecular screening
for interactors will clarify this question.
Although the impact of redundant genes on cotyledon development can still
not be excluded, analysis of PIN1 polarity very probably revealed how
enp enhances pid. Interestingly, and in contrast to adult
pinoid plants, pid embryos exhibit frequent but not complete
reversal of PIN1 positioning in the epidermis of the embryo apex. According to
the proposed models for organ formation
(Benkova et al., 2003), auxin
flux should be partly reversed but the net flux in the pid apex is
still directed towards the cotyledon tip. This disturbance is apparently
strong enough to cause mild cotyledon defects including an aberrant cotyledon
phyllotaxis. However, regarding the generation of cotyledons per se, either
auxin maxima are not required for organogenesis or auxin plays a role in
cotyledon development, at concentrations not sufficient to induce visible
DR5rev::GFP signals. The latter is supported by wild-type heart stage
embryos, which in our analysis only occasionally displayed weak auxin maxima.
This situation is reminiscent of the double root phenotypes of
topless, which only exhibit the root tip auxin maximum, required for
correct root pattern (Sabatini et al.,
1999
; Friml et al.,
2003
), in the `normal' basal root but not in the apical root
(Long et al., 2002
).
|
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ACKNOWLEDGMENTS |
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![]() |
Footnotes |
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Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/132/18/4063/DC1
* Present address: ALTANA Pharma AG, Byk-Gulden-Str. 2, 78467 Konstanz,
Germany
Present address: Institut für Toxikologie, GSF-Forschungszentrum
für Umwelt und Gesundheit GmbH, 85764 Neuherberg, Germany
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REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aida, M., Ishida, T., Fukaki, H., Fujisawa, H. and Tasaka,
M. (1997). Genes involved in organ separation in
Arabidopsis: an analysis of the cup-shaped cotyledon mutant.
Plant Cell 9,841
-857.
Aida, M., Ishida, T. and Tasaka, M. (1999).
Shoot apical meristem and cotyledon formation during Arabidopsis
embryogenesis: interaction among the CUP-SHAPED COTYLEDON and
SHOOT MERISTEMLESS genes. Development
126,1563
-1570.
Barton, M. K. and Poethig, R. S. (1993).
Formation of the shoot apical meristem in Arabidopsis thaliana: an
anlysis of development in the wild-type and in the shoot meristemless mutant.
Development 119,823
-831.
Baud, S., Bellec, Y., Miquel, M., Bellini, C., Caboche, M., Lepiniec, L., Faure, J. D. and Rochat, C. (2004). gurke and pasticcino3 mutants affected in embryo development are impaired in acetyl-CoA carboxylase. EMBO J. 5, 515-520.[CrossRef]
Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. and Offringa, R. (2001). The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128,4057 -4067.[Medline]
Benjamins, R., Ampudia, C. S., Hooykaas, P. J. and Offringa,
R. (2003). PINOID-mediated signaling involves calcium-binding
proteins. Plant Physiol.
132,1623
-1630.
Benkova, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertova, D., Jurgens, G. and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115,591 -602.[CrossRef][Medline]
Bennett, S. R. M., Alvarez, J., Bossinger, G. and Smyth, D. R. (1995). Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J. 8, 505-520.[CrossRef]
Berleth, T. and Jürgens, G. (1993). The
role of the monopteros gene in organising the basal body region of
the Arabidopsis embryo. Development
118,575
-587.
Berleth, T. and Chatfield, S. (2002). Embryogenesis: Pattern Formation from a Single Cell. In The Arabidopsis Book (ed. C. R. Somerville and E. M. Meyerowitz). Rockville, MD: American Society of Plant Biologists. doi/10.1199/tab.0051[CrossRef]
Blilou. I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J., Heidstra, R., Aida, M., Palme, K. and Scheres, B. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44.[CrossRef][Medline]
Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. and Simon, R. (2000). Dependence of the stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289,817 -819.
Byrne, M. E., Barley, R., Curtis, M., Arroyo, J. M., Dunham, M., Hudson, A. and Martienssen, R. A. (2000). Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408,967 -971.[CrossRef][Medline]
Christensen, S. K., Dagenais, N., Chory, J. and Weigel, D. (2000). Regulation of auxin response by the protein kinase PINOID. Cell 100,469 -478.[CrossRef][Medline]
Conway, L. J. and Poethig, R. S. (1997).
Mutations of Arabidopsis thaliana that transform leaves into
cotyledons. Proc. Natl. Acad. Sci. USA
94,10209
-10214.
Elliott, R. C., Betzner, A. S., Huttner, E., Oakes, M. P.,
Tucker, W. Q., Gerentes, D., Perez, P. and Smyth, D. R.
(1996). AINTEGUMENTA, an APETALA-2 like gene in
Arabidopsis with pleiotropic roles in ovule development and floral
organ growth. Plant Cell
8, 155-168.
Erschadi, S., Haberer, G., Schöniger, M. and Torres Ruiz, R. A. (2000). Estimating genetic diversity of Arabidopsis thaliana ecotypes with Amplified Fragment Length Polymorphisms (AFLP). Theor. Appl. Genet. 100,633 -640.[CrossRef]
Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R. and Jurgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426,147 -153.[CrossRef][Medline]
Friml, J., Yang, X., Michniewicz, M., Weijers Quint, A., Tietz,
O., Benjamins, R., Ouwerkerk, P. B. F., Ljung, K., Sandberg, G., Hooykaas, P.
J. J. et al. (2004). A PINOID-dependent binary
switch in apical-basal PIN polar targeting directs auxin efflux.
Science 306,862
-865.
Furutani, M., Vernoux, T., Traas, J., Kato, T., Tasaka, M. and
Aida, M. (2004). PIN-FORMED1 and PINOID
regulate boundary formation and cotyledon development in Arabidopsis
embryogenesis. Development
131,5021
-5030.
Gälweiler, L., Guan, C., Müller, A., Wisman, E.,
Mendgen, K., Yephremov, A. and Palme, K. (1998). Regulation
of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue.
Science 282,2226
-2230.
Geldner, N., Richter, S., Vieten, A., Marquardt, S.,
Torres-Ruiz, R. A., Mayer, U. and Jürgens, G. (2004).
Partial loss-of-function alleles reveal a role for GNOM in post-embryonic and
auxin-transport related development of Arabidopsis.Development 131,389
-400.
Haberer, G., Erschadi, S. and Torres Ruiz, R. A. (2002). The Arabidopsis gene PEPINO/PASTICINO2 is required for proliferation control of meristematic and non-meristematic cells and encodes a putative anti-phosphatatse. Dev. Genes Evol. 212,542 -550.[CrossRef][Medline]
Hadfi, K., Speth, V. and Neuhaus, G. (1998).
Auxin-induced developmental patterns in Brassica juncea embryos.
Development 125,879
-887.
Iwakawa, H., Ueno, Y., Semiarti, E., Onouchi, H., Kojima, S., Tsukaya, H., Hasebe, M., Soma, T., Ikezaki, M., Machida, C. and Machida, Y. (2002). The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol. 5,467 -478.[CrossRef]
Jürgens, G. (2001). Apical-basal pattern
formation in Arabidopsis embryogenesis. EMBO
J. 20,3609
-3616.
Kaplan, D. (1969). Seed development in Downingia. Phytomorphology 19,253 -278.
Kaplan, D. R. and Cooke, T. J. (1997).
Fundamental concepts in the embryogenesis of dicotyledons - a morphological
interpretation of embryo mutants. Plant Cell
9,1903
-1919.
Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. and Poethig, R. S. (2001). KANADI regulates organ polarity in Arabidopsis. Nature 411,706 -709.[CrossRef][Medline]
Klucher, K. M., Chow, H., Reiser, L. and Fischer, R. L.
(1996). The AINTEGUMENTA gene of Arabidopsis
required for ovule and female gametophyte development is related to the floral
homeotic gene APETALA2. Plant Cell
8, 137-153.
Kumaran, M. K., Bowman, J. L. and Sundaresan, V.
(2002). YABBY polarity genes mediate the repression of
KNOX homeobox genes in Arabidopsis. Plant
Cell 14,2761
-2770.
Ljung, K., Bhalerao, R. P. and Sandberg, G. (2001). Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J. 28,465 -474.[CrossRef][Medline]
Long, J. A. and Barton, M. K. (1998). The
development of apical embryonic pattern in Arabidopsis.Development 125,3027
-3035.
Long, J. A., Moan, E. I., Medford, J. I. and Barton, M. K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis.Nature 379,66 -69.[CrossRef][Medline]
Long, J. A., Woody, S., Poethig, S., Meyerowitz, E. M. and Barton, M. K. (2002). Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129,2297 -2306.
Lotan, T., Ohto, M., Yee, K. M., West, M. A. L., Lo, R., Kwong, R., Yamagishi, K., Fischer, R. L., Goldberg, R. B. and Harada, J. J. (1998). Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93,1195 -1205.[CrossRef][Medline]
Lukowitz, W., Gillmor, C. S. and Scheible, W. R.
(2000). Positional cloning in Arabidopsis. Why it feels
good to have a genome initiative working for you. Plant
Physiol. 123,795
-805.
Lynn, K., Fernandez, A., Aida, M., Sedbrook, J., Tasaka, M.,
Masson, P. and Barton, M. K. (1999). The
PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis
development and has overlapping functions with the ARGONAUTE gene.
Development 126,469
-481.
Mayer, K. F. X., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G. and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95,805 -815.[CrossRef][Medline]
Mayer, U., Torres Ruiz, R. A., Berleth, T., Misera, S. and Jürgens, G. (1991). Mutations affecting body organization in the Arabidopsis embryo. Nature 353,402 -407.[CrossRef]
Mayer, U., Büttner, G. and Jürgens, G.
(1993). Apical-basal pattern formation in the
Arabidopsis embryo: studies on the role of the GNOM gene.
Development 117,149
-162.
McConnell, J. R., Emery, J., Eshed, Y., Bao, N., Bowman, J. and Barton, M. K. (2001). Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411,709 -713.[CrossRef][Medline]
Meinke, D. W. (1992). A homeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science 258,1647 -1650.
Moussian, B., Schoof, H., Haecker, A., Jürgens, G. and
Laux, T. (1998). Role of the ZWILLE gene in the
regulation of central shoot meristem cell fate during Arabidopsis
embryogenesis. EMBO J.
17,1799
-1809.
Okada, K., Ueda, J., Komaki, M. K., Bell, C. J. and Shimura,
Y. (1991). Requirement of the auxin polar transport system in
early stages of Arabidopsis floral bud formation. Plant
Cell 3,677
-684.
Reinhardt, D., Mandel, T. and Kuhlemeier, C.
(2000). Auxin regulates the initiation and radial position of
plant lateral organs. Plant Cell
12,507
-518.
Reinhardt, D., Pesce, E. R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J. and Kuhlemeier, C. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426,255 -260.[CrossRef][Medline]
Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P. and Scheres, B. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99,463 -472.[CrossRef][Medline]
Sawa, S., Watanabe, K., Goto, K., Kanaya, E., Morita, E. H. and
Okada, K. (1999). FILAMENTOUS FLOWER, a meristem and
organ identity gene of Arabidopsis, encodes a protein with a zinc
finger and HMG-related domains. Genes Dev.
13,1079
-1088.
Scheres, B., Di Laurenzio, L., Willemsen, V., Hauser, M.-T.,
Janmaat, K., Weisbeek, P. and Benfey, P. (1995). Mutations
affecting the radial organisation of the Arabidopsis root display
specific defects throughout the embryonic axis.
Development, 121,53
-62.
Schoof, H., Lenhard, M., Haecker, A., Mayer, K. F. X., Jürgens, G. and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems is maintained between a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100,635 -644.[CrossRef][Medline]
Siegfried, K. R., Eshed, Y., Baum, S. F., Otsuga, D., Drews, G.
N. and Bowman, J. L. (1999). Members of the YABBY
gene family specify abaxial cell fate in Arabidopsis.Development 126,4117
-4128.
Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.
L., Paris, S., Gälweiler, L., Palme, K. and Jürgens, G.
(1999). Coordinated polar localization of auxin efflux carrier
PIN1 by GNOM ARF GEF. Science
286,316
-318.
Stone, S. L., Kwong, L. W., Yee, K. M., Pelletier, J., Lepiniec,
L., Fischer, R. L., Goldberg, R. B. and Harada, J. J. (2001).
LEAFY COTYLEDON2 encodes a B3 domain transcription factor that
induces embryo development. Proc. Natl. Acad. Sci. USA
98,11806
-11811.
Strasburger, E. (2002). Lehrbuch der Botanik, 35th edn. Berlin, Heidelberg: Spektrum Verlag.
Torres Ruiz, R. A. (2004). Polarity in Arabidopsis embryogenesis. In Polarity in Plants (ed. K. Lindsey), pp. 157-191. Oxford: Blackwell Publishers.
Torres Ruiz, R. A., Lohner, A. and Jürgens, G. (1996a). The GURKE gene is required for normal organization of the apical region in the Arabidopsis embryo. Plant J. 10,1005 -1016.[CrossRef][Medline]
Torres Ruiz, R. A., Fischer, T. and Haberer, G. (1996b). Genes involved in the elaboration of apical pattern and form in Arabidopsis thaliana: Genetic and molecular analysis. In Embryogenesis: The Generation of a Plant. (ed. E. Cummings and T. Wang), pp. 15-34. Oxford, UK: Bios Scientific Publishers.
Tsukaya, H. (2002). Leaf development. InThe Arabidopsis Book (ed. C. R. Somerville and E. M. Meyerowitz). Rockville, MD: American Society of Plant Biologists. doi/ 10.1199/tab.0072[CrossRef]
Vroemen, C. W., Mordhorst, A. P., Albrecht, C., Kwaaitaal, M. A.
and de Vries, S. C. (2003). The CUP-SHAPED
COTYLEDON3 gene is required for boundary and shoot meristem formation in
Arabidopsis. Plant Cell
15,1563
-1577.
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