1 National Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant
Physiology and Ecology, Shanghai Institute for Biological Sciences, Chinese
Academy of Sciences, 300 Fenglin Road, Shanghai 200032, China
2 College of Life Science and Biotechnology, Shanghai Jiao Tong University, 1954
Hua Shan Road, Shanghai 200030, China
3 College of Life Sciences, Fudan University, 220 Han Dan Road, Shanghai 200433,
China
4 College of Life Sciences, East China Normal University, 3663 North Zhongshan
Road, Shanghai 200062, China
* Author for correspondence (e-mail: hhuang{at}iris.sipp.ac.cn)
Accepted 21 May 2003
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SUMMARY |
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Key words: Adaxial-abaxial axis, Arabidopsis thaliana, ASYMMETRIC LEAVES1, ASYMMETRIC LEAVES2, ERECTA, Polarity formation
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INTRODUCTION |
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In Arabidopsis, the PHABULOSA (PHB) and
PHAVOLUTA (PHV) genes, together with a closely related gene,
REVOLUTA (REV), encode members of a
homeodomain/leucine-zipper (HD-ZIP) family of proteins. Semi-dominant
gain-of-function mutations in either PHB or PHV result in
the transformation of abaxial leaf tissues into adaxial ones
(McConnell and Barton, 1998;
McConnell et al., 2001
).
Phenotypes in loss-of-function rev mutants could be interpreted as a
partial loss of adaxial identity (Talbert
et al., 1995
; Otsuga et al.,
2001
). It was suggested that these genes are required for
promoting the adaxial cell fate in lateral organs
(McConnell and Barton, 1998
;
McConnell et al., 2001
). In
addition, YABBY and KANADI (KAN) genes are
expressed in the abaxial face of lateral organs and specify the abaxial cell
identity in Arabidopsis (Chen et
al., 1999
; Sawa et al.,
1999a
; Sawa et al.,
1999b
; Eshed et al.,
1999
; Eshed et al.,
2001
; Kerstetter et al.,
2001
). Members of the YABBY and KAN gene
families are candidate abaxial-promoting factors because mutations in these
genes cause abnormality in the specification of the abaxial fate
(Siegfried et al., 1999
;
Eshed et al., 2001
;
Kerstetter et al., 2001
;
Bowman et al., 2002
).
Other key regulators of leaf polarity include a group of functional
homologs: PHANTASTICA (PHAN) in Antirrhinum, ROUGH
SHEATH2 (RS2) in maize and ASYMMETRIC LEAVES1
(AS1) in Arabidopsis
(Waites and Hudson, 1995;
Schneeberger et al., 1998
;
Serrano-Cartagena et al.,
1999
). PHAN, RS2 and AS1 all encode MYB-domain
containing putative transcription factors, with a high degree of sequence
similarity among them (Waites et al.,
1998
; Timmermans et al.,
1999
; Tsiantis et al.,
1999
; Byrne et al.,
2000
; Sun et al.,
2002
). In situ hybridization and immunolocalization experiments
demonstrated that transcripts or proteins of members in the class 1
KNOX (knotted-like homeobox) gene family are ectopically accumulated
in leaves of phan, rs2 and as1 mutants
(Waites et al., 1998
;
Timmermans et al., 1999
;
Tsiantis et al., 1999
;
Byrne et al., 2000
). These
results suggest that PHAN, RS2 and AS1 act to down-regulate KNOX
genes in leaf initials, or these genes might initiate a process by which
KNOX gene expression is epigenetically repressed.
Furthermore, mutations in the Arabidopsis AS2 gene, another
important gene in leaf development, cause very similar phenotypes to those of
as1 mutants (Serrano-Cartagena et
al., 1999; Ori et al.,
2000
; Sun et al.,
2000
; Semiarti et al.,
2001
). In addition, as2 mutants show increased
accumulation of KNOX transcripts in leaves
(Semiarti et al., 2001
),
similar to that in as1 mutants
(Byrne et al., 2000
). It was
proposed that the AS1 and AS2 genes function in the same
regulatory pathway (Serrano-Cartagena et
al., 1999
; Byrne et al.,
2002
; Xu et al.,
2002
). AS2 has been cloned recently and the gene encodes
a protein with a leucine-zipper motif
(Iwakawa et al., 2002
;
Xu et al., 2002
). AS2
is expressed in almost all of the above ground portion of the wild-type plant
except the stem (Iwakawa et al.,
2002
; Xu et al.,
2002
).
Although the isolation and characterization of the AS1 and
AS2 genes have provided important insights into the mechanisms that
control the establishment of polarity during leaf development, they also
raised further questions. First, what is the molecular basis for AS1 and AS2
action? Do they form a complex if they function in the same regulatory
pathway? Second, do AS1 and AS2 also regulate leaf polarity
in the adaxial-abaxial axis, in addition to their roles in proximodistality
and mediolaterality in leaves (Byrne et
al., 2000; Tsiantis,
2001
)? Finally, are there any other genes required for leaf
polarity formation in the AS1 and AS2 regulatory
pathways?
To address these questions, we previously isolated and characterized new
as1 and as2 alleles in the Landsberg erecta
(Ler) genetic background (Sun et
al., 2000; Sun et al.,
2002
; Xu et al.,
2002
). Unlike other as1 and as2 alleles in the
Columbia, ER and En-D backgrounds, the alleles in the Ler background
showed a novel leaf phenotype: in some rosette leaves the petiole is attached
to the under surface of the leaf lamina. We referred to this structure as a
lotus-leaf. Here, we further characterize the lotus-leaf defects and
demonstrate that the primary AS1 and AS2 functions in the
establishment of leaf polarity are the regulation of adaxial-abaxial axis. We
also provide evidence that ER function acts in the AS1-AS2
pathway to regulate polarity formation during leaf development. We report a
physical interaction between AS1 and AS2 proteins in vitro and in yeast. Based
on these results as well as the phenotypes of 35S::AS1 and
35S::AS2 transgenic plants, we propose a model of AS1, AS2
and ER actions in leaf polarity formation.
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MATERIALS AND METHODS |
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Yeast two-hybrid assay
The cDNA fragments encoding the entire AS1 and AS2 predicted proteins were
amplified using polymerase chain reaction (PCR) and cloned into the
NdeI and BamHI restriction sites of the MATCHMAKER
two-hybrid vectors pGADT7 and pGBKT7 (Clontech, USA), to generate pGADT7-AS1,
pGBKT7-AS1, pGADT7-AS2 and pGBKT7-AS2, respectively. The PCR primers were as
follows: 5'-gccatATGAAAGAGCGTCAACGTTGG-3' and
5'-gtggatccTTAT CAGGGGCGGTCTAATCTG-3' (for AS1), and
5'-gccatATGGCATCTTCTTCAACAAAC-3' and
5'-gtggatccTTATCAAGACGGATCAACAGTAC-3' (for AS2). In each of the
above primer sequences, the lowercase letters represent additional nucleotides
to introduce restriction sites. All PCR fragments were verified by
sequencing.
Construct combinations pGADT7-AS1/pGBKT7-AS2 and pGADT7-AS2/pGBKT7-AS1 were co-transformed into the yeast strain AH109, and transformants were selected for growth on media lacking tryptophan and leucine. The interaction between the AS1 and AS2 proteins was tested by growth of the transformants on media lacking histidine and adenine, indicating expression of the reporter genes HIS3 and ADE2. Analysis of the relative ß-galactosidase activity was as described in the Yeast Handbook (Clontech, USA).
Enzyme-linked immunosorbent assay
For synthesis and purification of recombinant AS1 and AS2 proteins, cDNAs
containing the entire coding regions of these two proteins were amplified by
PCR. The amplified AS1 cDNA was cloned into the vector pET-14b
(Novagen, USA) by using the NdeI and BamHI sites to yield
His-AS1, and the AS2 cDNA was cloned into the vector pGEX-4T1 (Pharmacia, USA)
by using the BamHI and SalI sites to result in GST-AS2. The
PCR primers for the AS1 amplification were
5'-gccatATGAAAGAGCGTCAACGTTGG-3' and
5'-gtggatccTTATCAGGGGCGGTCTAATCTG-3', and those for the
AS2 amplification were
5'-caggatccATGGCATCTTCTTCAACAAAC-3' and
5'-cagtcgacTTATCAAGACGGATCAACAGTAC-3'. In each of above sequences
the lowercase letters represent additional nucleotides to introduce
restriction sites. All constructs were verified by sequencing. Production and
purification of His-AS1 and GST-AS2 fusion proteins were according to the
manufactures' recommended protocols (Novagen and Pharmacia, USA). The
resultant proteins were analyzed by SDS-PAGE before enzyme-linked
immunosorbent assay (ELISA) experiments. ELISA was performed by coating wells
of microtiter plates (Nunc., USA) with the GST-AS2, followed by addition of
the His-AS1 at different concentrations to the coated wells. The retained
His-AS1 was determined by incubation with a primary antibody against the His
tag (Sigma, USA), at 4°C overnight. Then the second antibody, a
POD-conjugated anti-mouse antibody (Sigma, USA), and the substrate
3,3',5,5'-tetramethylbenzidine (TMB) were added. The reaction was
examined by recording the absorbance at 655 nm, using a 450 Microplate Reader
(Bio-Rad, USA).
Reverse transcription-polymerase chain reaction
For reverse transcription-polymerase chain reaction (RT-PCR), total RNA was
extracted as described previously (Huang
et al., 1995). After treatment with DNase (Promega, USA),
complementary DNA was synthesized using a reverse transcription kit (Promega,
USA). PCR reactions were performed with KNAT1 gene-specific primers
(5'-TGTCAGAGTCCCATTCAC-3' and
5'-GCAACGAGAGGTTGTTATT-3'), which span the exon3/exon5 region. PCR
products were examined by separating on a 1.0% agarose gel.
Construction of transgenic plants
The overexpression construct 35S::AS1 was constructed previously
(Sun et al., 2002). For
overexpression of the AS2 gene, a 0.6 kb genomic DNA containing the
entire AS2 coding region was PCR-amplified from the Ler
plants and sequenced. This DNA fragment was then inserted into a binary T-DNA
vector pMON530 (Monsanto, USA), downstream of a 35S promoter. The constructs
35S::AS1 and 35S::AS2 were introduced into the Ler,
as1-101 and as2-101 plants by Agrobacterium-mediated
transformation. Ten 35S::AS1/Ler, thirty-two
35S::AS2/Ler, five 35S::AS1/as2-101 and
fifteen 35S::AS2/as1-101 transgenic lines were obtained.
Gene overexpression was verified by RT-PCR from the
35S::AS1/Ler and the 35S::AS2/Ler
transgenic lines that were used for phenotypic analysis in this work (data not
shown), and primers used in the PCR experiment were described previously
(Xu et al., 2002
).
35S::AS1/as2-101 and 35S::AS2/as1-101
transgenic lines were verified by PCR using a forward 35S primer
(5'-GCTCCTACAAATGCCATCA-3') and reverse primers
(5'-ttgaattcCATTACAAGTTACAAC-3' for the AS1 and
5'-GTTTTCTCATCACCAAGCG-3' for the AS2). Phenotypes of the
transgenic lines were consistent among progeny from each transformation.
Histology and microscopy
Fresh leaves and whole seedlings of wild-type and mutant plants were
examined using a SZH10 dissecting microscope (Olympus, Japan), and photos were
taken using a Nikon E995 digital camera (Nikon, Japan). Preparation of thin
section specimens and scanning electron microscopy (SEM) were as described
previously (Chen et al., 2000),
using the first pair of rosette leaves.
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RESULTS |
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ER function is involved in the leaf polarity formation
The as1 and as2 mutants were identified and first
characterized several decades ago (Redei,
1965). However, the lotus-leaf phenotype was not reported from
previous analyses of the as1 and as2 alleles
(Redei, 1965
;
Serrano-Cartagena et al.,
1999
; Byrne et al.,
2000
; Ori et al.,
2000
; Semiarti et al.,
2001
). Previously, we reported the observation of lotus-leaves in
newly isolated as1 alleles in the Ler background
(Sun et al., 2002
). We also
compared as2 alleles in different genetic backgrounds, and found that
only those in the Ler background produced lotus-leaves at relatively
high frequencies (Xu et al.,
2002
). These results indicate that the lotus-leaf phenotype is
likely to be sensitive to the genetic background. Ler carries a
mutated ER gene. To determine whether the lotus-leaf morphology is
associated with the er mutation, we crossed as2-101
(Ler) with a wild-type Landsberg ER (Lan) plant. Since the
er mutation causes distinctive morphologies from those of the
ER (Lan), it is easy to score the F2 as2-101 er
and as2-101 ER plants for the lotus-leaf phenotype. Our data showed
that the as2-101 er plants had a much higher frequency of
lotus-leaves than that in the as2-101 ER plants
(Table 1), indicating that
ER function is indeed involved in the leaf polarity
establishment.
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To examine AS1 and AS2 functions in leaf polarity along the proximodistal axis, we further analyzed adaxial epidermal identity in the as1, as2 and 35S::AS2/Ler leaves. Fig. 4A,B shows the adaxial epidermis in the proximal part of a Ler lamina. There were two distinctive cell types: elongated cells of the midvein and the relatively uniform epidermal cells that covered most of the lamina. The equivalent region of the as2 leaf epidermis (Fig. 4D,E) contained only one type of cell that was long and narrow in shape. These cells resembled the epidermal cells on the margin of Ler petiole (Fig. 4C, arrowhead), and were very similar to the epidermal cells on the adaxial side of the as2 petiole (Fig. 4F), consistent with the results from transverse sections (Fig. 2). Epidermal patterns in the as1 mutant were very similar to those in the as2 mutant (data not shown). In comparison, 35S::AS2/Ler petioles contained the uniformly shaped epidermal cells (white arrowhead) and elongated midvein-like cells (black arrowhead, Fig. 4G,H). This type of cell is usually positioned in the more distal region in the Ler lamina. In the more proximal portion of the petiole, epidermal cells were mosaic with a mixture of adaxial- and abaxial-type cells (Fig. 4I). This abnormal proximodistal differentiation, however, was not seen in the 35S::AS1/Ler plants (data not shown). These results indicate that the AS1 and AS2 functions are also required for promotion of cell fate along the proximodistal axis.
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DISCUSSION |
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Of the three axes of leaves, establishment of adaxial-abaxial polarity is
the primary and most essential process for leaf development. It was previously
proposed that the establishment of adaxial-abaxial polarity is a requirement
for proper lamina growth (Sussex,
1954; Sussex,
1955
). as1 and as2 mutant plants and
35S::AS2/Ler transgenic plants all have needle-like leaves,
however, the features of these organs are totally different. The needle-like
structure in as1 and as2 is due to a reduction in adaxial
differentiation, whereas that in the 35S::AS2/Ler transgenic
plants shows only the adaxial epidermis. Moreover, the Arabidopsis
semidominant mutant phb-1d also has needle-like structures, which
were thought to be adaxialized organs
(McConnell and Barton, 1998
;
McConnell et al., 2001
). The
epidermal pattern of needle-like leaves in 35S::AS2/Ler
transgenic plants is very similar to that of needle-like organs in
phb-1d, indicating the needle-like leaves in
35S::AS2/Ler transgenic plants may also be adaxialized
organs. Needle-like leaves cannot develop further to form laminae, regardless
of their adaxialized or abaxialized nature. This is consistent with the
proposal of Sussex that proper establishment of adaxial-abaxial polarity is
required for lamina development (Sussex,
1954
; Sussex,
1955
).
Interestingly, the lotus-leaf in as1 and as2 mutants is
also very similar to the trumpet-shaped leaves in the phb-1d mutant
(McConnell and Barton, 1998).
However, the inside and outside cell identities in lotus-leaves and
trumpet-shaped leaves is reversed (data not shown)
(McConnell and Barton, 1998
).
Cells with adaxial identity are on the inside surface of the as1/as2
lotus-leaf, while such cells are on the outside surface of the phb-1d
trumpet-shaped leaf. The analysis of leaf phenotypes in
35S::AS2/Ler transgenic plants, especially needle-like
structures in the as2 mutants and the 35S::AS2/Ler
transgenic plants further supports the hypothesis that the primary function of
AS2 is related to the promotion of the adaxial cell differentiation.
Since AS1 associates with AS2, and the as1 mutant also showed
lotus-leaves and needle-like leaves (Sun
et al., 2002
) (data not shown), it is possible that AS1
also functions as an adaxial promoting factor in leaf polarity formation. Our
recent results using RT-PCR showed that expression of the PHB gene
was enhanced in the 35S::AS1/Ler and
35S::AS2/Ler transgenic plants, and expression of the
FILAMENTOUS FLOWER (FIL), a member in the YABBY
family, was promoted in the as1-101 and as2-101 mutant
plants (L.X., H. Li and H.H., unpublished). These results suggest that the
AS1 and AS2 are genetically upstream to the PHB and
FIL genes in the regulation of leaf polarity.
ER function in the AS1-AS2 pathway for leaf
polarity
We previously demonstrated that lotus-leaves appeared at a much higher
frequency in as1 and as2 mutants in the Ler
background than that in any other genetic backgrounds analyzed
(Sun et al., 2002;
Xu et al., 2002
). Although
genomes from different Arabidopsis ecotypes contain polymorphisms, a
major difference between Ler and other Arabidopsis strains
is that Ler carries a mutated form of the ER gene. This
mutation confers plants with a compact inflorescence, blunt fruits, and short
petioles (Torii et al., 1996
).
In this work, we provide direct evidence that the higher frequency of
lotus-leaves in as2 mutant was caused by the er mutation.
Therefore, both AS1 and AS2 (possibly the AS1-AS2 complex), as well as ER
contribute to the leaf polarity formation. The ER gene encodes a
receptor protein kinase with extracellular leucine-rich repeats
(Torii et al., 1996
). It is
widely expected that ER regulates signaling in plant development.
The Arabidopsis bp mutant carries mutated KNAT1 and
ER genes. It was proposed that ER functions redundantly with
KNAT1 to regulate plant architecture and stem differentiation
(Douglas et al., 2002;
Venglat et al., 2002
).
Although AS1-AS2 and ER also seem to be redundant in the
promotion of the adaxial cell fate, similar to the KNAT1 and
ER pair in the bp mutant, we hypothesize that
AS1-AS2 and ER may play different roles in the establishment
of leaf polarity. First, we have observed that as2 mutations in
genetic backgrounds other than Ler also showed lotus-leaves, although
at much lower frequencies (Xu et al.,
2002
). In addition, petioles of the first pair of rosette leaves
in all as2 alleles, regardless of genetic backgrounds, contain a
radially symmetric portion. Although petioles of as1-1 plants in the
mixed Col/Ler background did not show even the radially symmetric
portion, petioles in as1-1 and plants with the other as1 and
as2 alleles all reflect a same defect. These observations indicate
that the AS1 and AS2 functions, but not the ER
function, are primarily necessary for the normal adaxial-abaxial polarity in
leaves. Second, the length of the radially symmetric portion in as1
er (data not shown) and as2 er was highly variable: from fully
expanded leaves to needle-like leaves. Nevertheless, as2 ER showed
very few lotus-leaves and less variable portions of radially symmetric
petioles, and as1 ER did not contained any radially symmetric
position. These observations suggest that the ER function may reduce
the sensitivity of plant cells to yet unknown internal or environmental
signals for leaf development.
Function of the AS1-AS2 complex
Arabidopsis as1 and as2 mutants have very similar leaf
morphology (Redei, 1965;
Serrano-Cartagena et al.,
1999
; Sun et al.,
2000
). Both mutants also show misexpression of the class 1
KNOX genes (Byrne et al.,
2000
; Ori et al.,
2000
; Semiarti et al.,
2001
; Byrne et al.,
2002
) and suppression of the LATERAL ORGAN BOUNDARIES
(LOB) gene (Shuai et al.,
2002
). All these suggest that these two genes function in the same
regulatory pathway. In this work, we provided direct genetic evidence showing
a requirement of the AS1 and AS2 functions together in the
leaf development: 35S::AS1/as2 and 35S::AS2/as1 transgenic
plants demonstrated only the as1- or as2-like leaf
phenotypes, which are markedly different from those in the corresponding
35S::AS1/Ler and 35S::AS2/Ler plants. To
explore the underlying molecular mechanisms of AS1 and AS2
actions in leaf development, we previously examined AS1 expression in
the as2 mutant and AS2 expression in the as1 mutant
to determine if these two genes are regulated by each other. There were no
obvious changes in either AS1 or AS2 transcripts when one
gene was expressed in the other mutant background
(Xu et al., 2002
), suggesting
that the direct transcriptional regulation of one by the other is not
likely.
In this work, we tested the possibility of protein-protein interactions between AS1 and AS2. We showed that AS1 and AS2 can indeed associate together both in vitro and in yeast cells. These results suggest that AS1 and AS2 may form a complex to regulate their downstream genes during leaf development.
This regulatory model is similar to that with products of floral organ
identity genes APETALA3 (AP3) and PISTILATA
(PI) in Arabidopsis. AP3 and PI can associate to form a
complex, and mutation in either AP3 or PI results in very
similar floral phenotypes (Jack et al.,
1992; Goto and Meyerowitz,
1994
).
Although as1 and as2 have comparable defects in leaf
development, transgenic plants carrying 35S::AS1/Ler and
35S::AS2/Ler exhibited dramatically different phenotypes,
not only morphologically but also at the molecular level, such as the
suppression of KNAT1 expression. One possibility is that the AS1 and
AS2 proteins are not present at similar levels in wild-type plants. The AS1
protein may be more abundant than AS2, such that the increase of AS2 dosage
results in the formation of more functional AS1-AS2 complexes. Another
possibility is that the different phenotypes are caused by the endogenous gene
expression pattern. AS1 is expressed throughout the leaf, a pattern
similar to that of the 35S-driven gene expression in leaves. The same
expression pattern of the AS1 gene may not generate altered
phenotypes. AS2 is expressed only adaxially as reported in the
embryonic cotyledons (Iwakawa et al.,
2002), and therefore ectopic AS2 expression under the
control of the 35S promoter may cause dramatic phenotypic
changes.
It is known that both AS1 and AS2 are needed to
down-regulate class 1 KNOX genes, because loss-of-function mutations
in AS1 and AS2 result in the ectopic expression of
KNOX genes in leaves (Byrne et
al., 2000; Semiarti et al.,
2001
). Based on the analyses of 35S::AS1/Ler and
35S::AS2/Ler transgenic plants, only the AS2
ectopic overexpression suppressed KNAT1 expression in the
inflorescence and generated bp-like phenotypes. This phenomenon can
also be accounted for by the less abundant AS2 dosage and (or) the strict AS2
distribution in wild-type inflorescence failing to form enough complexes to
suppress KNAT1, although the AS1 appears in the same-stage
inflorescence (Byrne et al.,
2000
).
A proposed genetic model for AS1, AS2 and
ER actions in leaves
Based on the AS1 and AS2 expression patterns
(Byrne et al., 2000;
Iwakawa et al., 2002
) and the
results in this work, we propose a model of AS1, AS2 and ER
actions in the establishment of leaf polarity
(Fig. 9). AS1 and AS2 can bind
each other (evidence from the yeast two-hybrid assays and the in vitro protein
binding experiment). The AS1-AS2 complex may efficiently suppress
KNAT1 expression in leaves (KNAT1 was expressed ectopically
in the as1 and as2 leaves, but was repressed in wild-type
leaves). The AS1-AS2 complex can efficiently promote adaxial leaf identity
(the as1 and as2 single mutants both showed defective
epidermal cells on the adaxial surface, indicating that the independent
AS1 and AS2 functions cannot normally promote the adaxial
identity; and evidence also from 35S::AS2/as1-101 plants as
they failed to reproduce the phenotypes of 35S::AS2/Ler
plants, which had adaxialized leaves). The ER function is required
for promoting adaxial-abaxial polarity formation in the AS1-AS2 regulatory
pathway (as1 ER and as2 ER plants show much weaker
adaxial-abaxial defects of leaves than as1 er and as2 er
plants, respectively), however the exact involvement of ER action in
this pathway remain to be elucidated.
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ACKNOWLEDGMENTS |
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