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First published online 27 February 2008
doi: 10.1242/dev.017913
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National Laboratory of Plant Molecular Genetics, Shanghai Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai 200032, People's Republic of China.
Author for correspondence (e-mail:
hhuang{at}sippe.ac.cn)
Accepted 30 January 2008
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SUMMARY |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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Key words: Arabidopsis, ASYMMETRIC LEAVES1/2, Leaf development, Polarity establishment, Ribosomal proteins
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INTRODUCTION |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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; Sussex,
1955) and elaborated recently by Reinhardt et al.
(Reinhardt et al., 2005)
provide important information that the establishment of the adaxial-abaxial
axis is crucial for subsequent leaf development.
An increasing number of genes that regulate leaf adaxial-abaxial polarity
have been identified and characterized extensively. Three members in the class
III HD-ZIP family, PHABULOSA (PHB), PHAVOLUTA
(PHV) and REVOLUTA (REV), specify adaxial fate and
are expressed in the adaxial domain of leaves
(McConnell and Barton, 1998;
McConnell et al., 2001;
Emery et al., 2003;
Zhong and Ye, 2004).
Transcripts of these three genes are the targets of microRNA165 and 166
(miR165/166) (Rhoades et al.,
2002; Tang et al.,
2003). Two other genes, ASYMMETRIC LEAVES1 (AS1)
and AS2, have also been considered to promote the adaxial identity of
leaves by positively regulating PHB, PHV and REV
(Lin et al., 2003;
Xu et al., 2003). More
recently, AS1/AS2 were found to repress miR165/166 so that PHB,
PHV and REV transcripts may be stabilized
(Li et al., 2005;
Fu et al., 2007;
Ueno et al., 2007). Recently,
genes functioning in the trans-acting siRNA pathway have been uncovered that
facilitate adaxial cell fate of leaves, including RNA-DEPENDENT RNA
POLYMERASE6 (RDR6), SUPPRESSOR OF GENE SILENCING3
(SGS3), ZIPPY (ZIP) and DICER-LIKE4
(DCL4) (Peragine et al.,
2004; Li et al.,
2005; Garcia et al.,
2006; Xu et al.,
2006).
In addition to the adaxial promoting components, several genes are required
for leaf abaxial identity, including members of the KANADI (KAN) and YABBY
(YAB) families (Sawa et al.,
1999; Siegfried et al.,
1999; Eshed et al.,
2001; Kerstetter et al.,
2001). KAN genes antagonize class III HD-ZIP genes
(Emery et al., 2003), while
the YABs are downstream genes of KAN
(Eshed et al., 2004).
Furthermore, two auxin response factor genes, AUXIN RESPONSE FACTOR3
(ARF3/ETT) and ARF4, promote abaxial identity
(Pekker et al., 2005).
ARF3 and ARF4 transcripts are the targets of a small RNA,
termed tasiR-ARF (Allen et al.,
2005). Finally, loss of function in 26S proteasome subunit genes
results in plants with abaxialized leaves, suggesting that post-translational
regulation is required for the normal leaf polarity
(Huang et al., 2006).
Here, we implicate a new class of genes, the ribosomal large subunit
protein encoding genes, in leaf polarity establishment. In animals, functions
of the ribosomal proteins have been investigated extensively, and defects in
these proteins can cause various kinds of diseases
(Bilanges and Stokoe, 2007;
Idol et al., 2007;
Scheper et al., 2007) and
developmental abnormalities (Oliver et
al., 2004; Uechi et al.,
2006; Marygold et al.,
2007). Compared with those in animals, only a few ribosomal
proteins in plants have been characterized. POINTED FIRST LEAVES1
(PFL1) and PFL2 encode the PRS18 and PRS13 ribosomal small
subunit proteins, respectively, playing roles in leaf development
(Van Lijsebettens et al.,
1994; Ito et al.,
2000). A semi-dominant mutation of the Arabidopsis
MINUTE-LIKE1 gene, which encodes an additional ribosomal small subunit
RPS5, led to early embryonic developmental defects by disrupting cell division
(Weijers et al., 2001).
Finally, loss of function in the SHORT VALVE1 (STV1) gene,
which encodes a ribosomal large subunit protein RPL24B, resulted in the
apical-basal patterning defect of gynoecium by influencing ARF3
translation (Nishimura et al.,
2005). All these results indicate that ribosomal proteins are
widely involved in different plant developmental processes.
In the present study, we report characterizations of two ribosomal large subunit genes, RPL28A and RPL5A, both of which play important roles in specifying leaf adaxial identity. Moreover, we found that other two ribosomal protein genes, STV1 and RPL5B, also have this function in leaf pattern formation, indicating that specific ribosomal functions are required for proper leaf patterning. In addition, we present detailed analyses of genetic interactions between the ribosomal pathway and other genetic pathways during leaf polarity formation.
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MATERIALS AND METHODS |
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SUMMARY
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MATERIALS AND METHODS
RESULTS
DISCUSSION
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; Sun et al.,
2002; Xu et al.,
2002; Li et al.,
2005). For generation of as2 enhancers, about 8000
as2-101 seeds (Ler) were ethyl methanesulfonate mutagenized
(0.15%), and the seeds from 2749 individual M2 lines were screened. Two
as2 enhancer mutants, ae5-1 and ae6-1, were
obtained, which were backcrossed to wild-type Ler three times before
detailed phenotypic analyses. Seeds of ae5-2 (SALK_138179),
ae6-2 (SALK_089798), rpl5b (SALK_010121) and arf4-2
(SALK_070506) were obtained from the ABRC (Ohio State University, Columbus,
OH, USA). Seeds of rev-9, kan1-2/kan1-2 kan2-1/+ were provided by J.
Bowman (University of California, Davis). Seeds of stv1-1 and
ett-3 were from K. Okada
(Nishimura et al., 2005) and
P. Zambryski (University of California, Berkeley), respectively. Plant growth
was carried out according to our previous conditions
(Chen et al., 2000).
RT-PCR
RNA extraction was performed as described previously
(Xu et al., 2003) with leaves
from 25-day-old seedlings, and reverse transcription was performed with 1
µg total RNA using a kit (Fermentas, Vilnius, Lithuania). PCR was performed
with the following gene-specific primers:
5'-ATGGCGACAGTTCCAGGAC-3' and
5'-TTAAGCTTGTCTGTTTCTTTG-3' for RPL28A;
5'-TGTGAACACAAAAGCTGAGTG-3' and
5'-CAACCAAGACAAGAACAAGTAC-3' for RPL5A; and
5'-TGGCATCA(T/C)ACTTTCTACAA-3' and
5'-CCACCACT(G/A/T)AGCACAATGTT-3' for ACTIN. PCR was
performed according to our previous methods
(Li et al., 2005).
In situ hybridization and microscopy
In situ hybridization was performed according to a previously described
method (Long and Barton, 1998)
using 14-day-old seedlings. FIL and REV probe preparations
were according to our previous methods (Li
et al., 2005). AE5 and AE6 probes were made from
cDNA clones containing sequences from exon 4 of AE5 and exon 7 of
AE6, respectively. Microscopic analyses were performed according to
the previously described methods (Chen et
al., 2000; Sun et al.,
2002).
For confocal laser-scanning microscopy, the YFP-RPL28A and
YFP-RPL5A fusions were first constructed. The YFP-RPL28A and
YFP-RPL5A fragments were then subcloned into vector pER8
(Zuo et al., 2000), resulting
in pER8-YFP-RPL28A and pER8-YFP-RPL5A, respectively. These
two constructs were introduced into wild-type Col-0 plants by
Agrobacterium- mediated transformation, and the 10-day-old seedlings
of the transgenic T1 plants were used for observation after pretreatment with
4 µM estradiol for 3 hours. Specimens were viewed with an LSM510
laser-scanning confocal microscope (Zeiss, Jena, Germany) at a wavelength of
514 nm (YFP).
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RESULTS |
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SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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To identify the AE5 and AE6 genes, we carried out
map-based cloning by crossing ae5-1 as2-101 and ae6-1
as2-101 to wild-type Col-0 plants. Using about 2000 recombinant
chromosomes each, we mapped AE5 and AE6 to the lower arm of
chromosome 2 and the upper arm of chromosome 3 in a less than 30 kb region,
respectively (Fig. 1A,B). We
sequenced coding regions of all putative genes in the ae5 region and
identified a gene containing a G-to-A substitution in the second exon,
resulting in a premature stop codon (Fig.
1A). This gene (At2g19730) encodes RPL28A, a protein in the large
subunit of the ribosome. We then analyzed the ae6 mapping region and
found another ribosomal protein coding gene (At3g25520), RPL5A
(Fig. 1B). Although sequencing
of the RPL5A-coding region did not show any change in the nucleotide
sequence, the expression level of the RPL5A gene was dramatically
reduced (see Fig. S1 in the supplementary material). Subsequent analyses
revealed that the 3' region of the gene was disrupted by an
Arabidopsis transposon Tag1
(Tsay et al., 1993), which may
cause mRNA instability of this gene (see Fig. S1 in the supplementary
material).
To further confirm by complementation that we had identified the correct genes, we transformed the ae5-1 as2-101 mutant with a complementation construct containing 1.3 kb of the RPL28A gene plus 1.9 kb and 1.1 kb of its 5' and 3' regions (see Fig. S2A in the supplementary material). We also transformed the ae6-1 as2-101 mutant with a construct containing 1.8 kb of the RPL5A gene together with 1.9 kb and 0.8 kb of the 5' and 3' regions (supplementary material Fig. S2B). A total of 20 and 25 transgenic lines, respectively, were obtained, of which all plants showed only as2-101 single mutant phenotypes (see Fig. S2C-F in the supplementary material), indicating that RPL28A and RPL5A indeed correspond to the enhanced as2 phenotypes in the ae5-1 as2-101 and ae6-1 as2-101 mutant plants.
RT-PCR revealed that AE5 and AE6 were expressed in all plant tissues examined (Fig. 1C). In situ hybridization using the gene-specific sequence as probes showed that AE5 and AE6 transcripts were detected throughout the embryo (Fig. 1D,E) and leaf primordia (Fig. 1F,G) at earlier developmental stages. The same expression pattern was also detected in the reproductive organs, with the hybridization signals being throughout the inflorescence meristem, floral primordia and four types of young floral organs (Fig. 1H). The in situ hybridization experiments were performed with two types of negative controls: (1) sense probes (Fig. 1I); and (2) an insertional ae6-2 allele (Fig. 1J; for identification of ae6-2, see Fig. S3 in the supplementary material). These results indicate that RPL28A and RPL5A are new regulators of leaf polarity despite their expression throughout leaf primordia.
Mutations of ae5 and ae6 affect leaf adaxial-abaxial polarity
To understand the functions of AE5 and AE6 in leaf
development, we analyzed phenotypes of ae5/6 as1 and ae5/6
as2 mutants, as well as ae5 and ae6 single mutants.
Compared with wild-type (Fig.
2A) and as2-101 (Fig.
2B) plants, both ae5-1 as2-101
(Fig. 2D) and ae6-1
as2-101 (Fig. 2E)
displayed an increased number of lotus- and needle-like leaves
(Table 1). Of these two double
mutants, the ae5-1 as2-101 phenotypes appeared even more severe with
almost all true leaves being needle-like in a proportion of the seedlings
(Fig. 2D). Although most first
two leaves in the ae6-1 as2-101 mutant were expanded, the adaxial
surface of the leaves was rough (Fig.
2E). For the single mutants, ae6-1 had a phenotype
similar to that of wild-type plants (Fig.
2G), whereas the early appearing leaves of ae5-1 were
slightly longer and all leaves were pale green
(Fig. 2F).
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To determine the anatomical basis of the pale green leaves of ae5-1 and ae6-2 mutants, we analyzed their lamina structure by transverse sectioning. In wild-type Ler (Fig. 3G) and Col-0 (Fig. 3H) plants, four distinct cell types in the lamina of expanded leaves are recognizable along the adaxial-abaxial axis: adaxial epidermis, palisade mesophyll, spongy mesophyll and abaxial epidermis. Of the two types of mesophyll cells, the adaxially located palisade cells are usually tightly arranged, whereas the abaxially positioned spongy cells are loosely arranged with intercellular spaces (Fig. 3G,H, arrows). However, in the ae5-1 and ae6-2 leaves, numerous intercellular spaces occurred in the adaxial palisade region (Fig. 3I,J, arrowheads), reflecting a disrupted leaf adaxial-abaxial axis. These results also suggest that the less tightly arranged palisade cells at least partially contribute to the pale green color of the ae5-1 and ae6-2 leaves.
Compared with the inflorescences in wild-type plants (Fig. 3K), those from some ae5-1 (Fig. 3L,M) and ae6-2 (data not shown) plants were abnormal. The inflorescence of some ae5-1 plants terminated early, by producing several secondary inflorescences (Fig. 3L). In wild-type plants, a secondary inflorescence is usually associated with a cauline leaf at its proximal end (Fig. 3K), whereas in ae5-1 plants a proportion of secondary inflorescences lacked a subtending cauline leaf (Fig. 3M, arrowhead). Occasionally, some cauline leaves in ae5-1 (Fig. 3N) and ae6-2 (data not shown) formed ectopic outgrowths on their abaxial distal parts. All these results indicate that RPL28A and RPL5A are involved in multiple plant developmental processes.
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To obtain molecular evidence for the RPL28A and RPL5A function in
specifying leaf polarity, we examined by in situ hybridization the expression
pattern of two marker genes, FIL and REV. In wild-type
plants, FIL is usually expressed on the abaxial side of leaves
(Siegfried et al., 1999)
(Fig. 5A), and this pattern was
also observed in ae5-1 leaves
(Fig. 5B). FIL
expression appeared to be extended towards the adaxial side in some young
leaves in as2-101 (Fig.
5C, arrowheads), and was further expanded throughout some
needle-like leaf primordia of ae5-1 as2-101
(Fig. 5D, arrows; see Fig. S5
in the supplementary material). REV is known to be expressed in the
adaxial domain of leaf primordia as well as in the vascular tissue of
developing leaves (Eshed et al.,
2001) (Fig. 5E).
Although the REV expression pattern did not show obvious changes
between the wild type (Fig.
5E), ae5-1 (Fig.
5F) and as2-101 (Fig.
5G), the normal REV expression pattern was not apparent
in leaf primordia of ae5-1 as2-101
(Fig. 5H). In addition, the
REV signal was markedly reduced in the primordia of the double
mutant, whereas in vascular bundles the REV expression level appeared
close to that in the wild-type primordia
(Fig. 5H; see Fig. S5 in the
supplementary material). These results indicate that ribosomal proteins are
required genetically for regulation of the key leaf polarity-controlling genes
during leaf patterning.
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)
(Fig. 6E), but ae5-1
rdr6-3 demonstrated more severe defects in leaf polarity, with many
lotus- and needle-like leaves (Fig.
6F, arrowheads). The vascular pattern through the blade-petiole
junction region in rdr6-3 (Fig.
6G) was similar to that of wild-type plant
(Fig. 4J), whereas that in
ae5-1 rdr6-3 (Fig. 6H)
was apparently abaxilized, with a phloem-surrounding-xylem structure.
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), with narrow and dark green rosette leaves and ectopic
outgrowths on the abaxial leaf side (Fig.
6I,K). Interestingly, on abaxial surfaces of the ae5-1 ett-3
arf4-2 (Fig. 6J,M,N) and
ae6-2 ett-3 arf4-2 (data not show) triple mutant leaves, the number
of the outgrowths was dramatically decreased. The ae5-1 kan1-2 kan2-1
triple mutant only had two very narrow leaves, with other leaves being
arrested at their earlier developmental stages
(Fig. 6L). Similarly, the
number of the outgrowths on abaxial surfaces of the two ae5-1 kan1-2
kan2-1 leaves was also reduced (Fig.
6L, inset), when compared with those of kan1-2 kan2-1
(Fig. 6K, inset,
Fig. 6O). The reduction of the
outgrowth numbers in the triple mutants was also accompanied by the impaired
severity of outgrowth shapes (see Fig. S4 in the supplementary material).
These results indicate that RPL28A and RPL5A may genetically
interact with the KAN1/2 and ARF3/4 pathways to regulate
leaf polarity.
Leaf polarity defects in stv1 as2 and rpl5b as2 double mutants
To determine whether other ribosomal subunit genes also participate in leaf
patterning, we constructed stv1 as2 and rpl5b as2 double
mutants. STV1 encodes a ribosomal large subunit protein RPL24B
(Nishimura et al., 2005).
Although stv1-1 (Fig.
7A) and rpl5b (Fig.
7E; for identification of rpl5b, see supplementary
material Fig. S3) both produced pale green leaves, the epidermal cell patterns
appeared normal (see Fig. S4 in the supplementary material). By contrast,
stv1-1 as2-1 and rpl5b as2-1 double mutant plants
demonstrated very severe phenotypes with most rosette leaves being needle-like
(Fig. 7B,F). These needle-like
leaves were covered with rectangular-shaped cells or abaxial-type cells
(Fig. 7C,G, arrowheads).
Similar to those in the ae5-1 as2-101 double mutant
(Fig. 4L), the vascular pattern
of these leaves indicated that they were abaxialized
(Fig, 7D,H).
As RPL5B is a duplicated copy of RPL5A (AE6) in the Arabidopsis genome, we were interested in determining whether the ae6 rpl5b double mutant would more severely affect leaf polarity. Interestingly, the double heterozygote (ae6-2/+ rpl5b/+) exhibited a phenotype similar to that of ae6-2 or rpl5b single mutant, with pale green leaves (see Fig. S6 in the supplementary material). However, plants with genotypes ae6-2/ae6-2 rpl5b/rpl5b, ae6-2/+ rpl5b/rpl5b, or ae6-2/ae6-2 rpl5b/+ were not found in the F2 progeny of the ae6-2 and rpl5b cross (see Fig. S6 in the supplementary material). Taken together, the enhanced as2 phenotypes by other ribosomal large subunit gene mutations indicate that the entire ribosomal activity may be required for normal leaf polarity establishment.
Subcellular localization of RPL28A and RPL5A
We next examined the subcellular localization of RPL28A and RPL5A by
generating YELLOW FLUORESCENT PROTEIN (YFP)-RPL28A
and -RPL5A fusions under the control of an estradiol-inducible
promoter. These two constructs were introduced into wild-type Ler, ae5-1
as2-101 and ae6-1 as2-101 mutant plants, respectively, and the
double mutant phenotypes could be rescued (data not shown), indicating that
YFP-RPL28A and YFP-RPL5A are biologically active. In the root tissue of
wild-type Ler plants, YFP-RPL28A
(Fig. 8A-C) and YFP-RPL5A (data
not shown) were both located in the nuclei and cytoplasm. In addition to the
strong YFP signals in the nucleolus, YFP-RPL28A
(Fig. 8D-F) and YFP-RPL5A
(Fig. 8G-I) were also present
in the nucleoplasm. These results indicate that the ribosomal large subunit
proteins in plants possess a similar subcellular localization pattern to those
in animals (Claussen et al.,
1999).
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). Unlike
other leaf adaxial-promoting factors, the severe ae5 and ae6
alleles exhibited a defective phenotype with almost all leaves being pale
green in color, and this type of leaves was also observed in stv1-1
and rpl5b single mutants. This phenotype was caused, at least in
part, by the ectopic intercellular spaces, which should be normally located in
the abaxial spongy mesophyll layer of the wild-type leaves but are present in
the adaxial palisade layer of the mutant ones. In addition, double mutants
combining as1/as2 with ribosomal protein gene mutations can cause
severe defects in the adaxial-abaxial leaf polarity. Our data strongly suggest
that ribosomal proteins are a new type of regulator in leaf polarity
establishment.
The translational function of the ribosome is required for leaf polarity establishment
The ribosome is composed of two subunits, a large subunit and a small
subunit, both of which are formed by ribosomal proteins and rRNAs. The
Arabidopsis genome contains 227 genes encoding 80 ribosomal proteins,
48 and 32 of which are on the large and small subunits, respectively
(Carroll et al., 2007). By
interacting with different rRNAs at specific regions, they form different
active sites required for the ribosomal function
(Ramakrishnan, 2002). In
animals, ribosomal proteins are involved in either specific or nonspecific
developmental processes (Bilanges and
Stokoe, 2007; Ishijima et al.,
1998; Idol et al.,
2007; Marygold et al.,
2007; Oliver et al.,
2004; Uechi et al.,
2006). For example, knockdown of some ribosomal protein genes in
zebrafish resulted in a spectrum of developmental defects with varying degrees
of abnormality in the brain, body trunk, eyes and ears
(Uechi et al., 2006). In
Drosophila, 88 genes that encode cytoplasmic ribosomal proteins were
characterized, 64 of them were found to correspond to the similar dominant
`Minute' phenotypes (Marygold et al.,
2007). Some ribosomal proteins or protein complexes with specific
functions were also documented: RPL22 and RPL7 function in transcription
repression (Ni et al., 2006);
RPL5, RPL11 and RPL23 act in inhibition of protein ubiquitination and
degradation (Arva et al., 2005;
Dai and Lu, 2004;
Dai et al., 2004); and RPL11 is
involved in reduction of histone H4 acetylation
(Dai et al., 2007).
The functions of four Arabidopsis ribosomal proteins have been
characterized and the corresponding mutants pfl1/rps18
(Van Lijsebettens et al.,
1994), pfl2/rps13
(Ito et al., 2000),
aml1/rps5 (Weijers et
al., 2001) and stv1/rpl24
(Nishimura et al., 2005) all
exhibited pleiotropic developmental defects. However, it was also observed
that a loss of functions in different ribosomal protein genes affecting
specific developmental processes. For example, STV1 (RPL24)
regulates apical-basal patterning of the gynoecium
(Nishimura et al., 2005). We
propose that regulation of the leaf adaxial-abaxial polarity requires a
conserved translational function of the Arabidopsis ribosome. First,
although RPL28A, RPL5A, RPL5B and RPL24B are all large subunit proteins,
according to data from yeast (Spahn et
al., 2001) and bacteria
(Korostelev et al., 2006;
Selmer et al., 2006), these
four proteins are located in three distinct sites on the large subunit,
whereas plants with mutations in each of these genes suffer similar
adaxial-abaxial polarity defects. Second, pfl2/rps13 and
pfl1/rps18 also display either pale green leaves
(Van Lijsebettens et al.,
1994) or the defective mesophyll pattern
(Ito et al., 2000), similar to
that in the large subunit mutants ae5, ae6, stv1 and rbl5b.
Finally, the double heterozygous plant (ae6/+ rpl5b/+) exhibited the
pale-green leaf phenotype (see Fig. S6 in the supplementary material). These
data suggest that a partial loss of the ribosome function may cause some
similar leaf polarity defects. As the ribosome is known to be the conserved
machinery of translation in all organisms, the regulation of leaf polarity at
the translational level must be very important.
Roles of the ribosome in the regulatory network in leaf patterning
The molecular mechanism of how ribosomal proteins regulate leaf
polarity-controlling genes is not yet clear. One possibility is that the
ribosome may genetically promote the HD-ZIP III mediated pathway in
the adaxial domain of leaves. We have two lines of evidence to support this
idea: (1) ae5-1 can enhance a weak rev allele,
rev-9; and (2) accumulation of REV transcripts were reduced
in ae5 as2 and ae6 as2 double mutants. In addition,
AS1/AS2 are known to regulate PHB, PHV and REV
positively in leaves (Lin et al.,
2003; Fu et al.,
2007; Ueno et al.,
2007), and as1/as2 phenotypes could be enhanced
in the ribosomal protein gene mutation backgrounds.
Another possibility is that the ribosome may genetically repress
ARF3/4, KAN or their downstream genes. This hypothesis is
supported by the observation that ae5 ett arf4 and ae6 ett
arf4 triple mutants dramatically suppress an ett arf4 phenotype
in which outgrowths are formed on the abaxial leaf side. In addition, ae5
kan1 kan2 also exhibited the reduction of the outgrowth numbers. It was
proposed that juxtaposition of adaxial and abaxial domain is required for
lamina outgrowth (Waites and Hudson,
1995), and adaxial and abaxial characteristics on the same abaxial
side of the kan1 kan2 leaves might cause the formation of ectopic
outgrowths (Eshed et al.,
2004). Based on this proposal, it is possible that the balanced
juxtaposition of the adaxial and abaxial cell patches on the same leaf side
may be crucial for the outgrowth formation. The addition of ae5 or
ae6 mutation in the ett arf4 and kan1 kan2
backgrounds may alter the original juxtaposition balance by promoting abaxial
leaf characteristics, and therefore repressed the outgrowth phenotype.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/135/7/1325/DC1
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ACKNOWLEDGMENTS |
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Footnotes |
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DISCUSSION
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