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First published online 27 February 2008
doi: 10.1242/dev.016469
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1 Department of Crop Genetics, John Innes Centre, Norwich NR4 7UH, UK.
2 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Author for correspondence (e-mail:
mary.byrne{at}bbsrc.ac.uk)
Accepted 3 January 2008
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SUMMARY |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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Key words: Ribosomal protein, Leaf polarity, ASYMMETRIC LEAVES1, PIGGYBACK, Arabidopsis
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INTRODUCTION |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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;
Kidner and Timmermans, 2007).
Several transcription factor families are involved in establishing adaxial and
abaxial fates. One such family is the class III homeodomain-leucine zipper
(HD-ZIPIII) genes, which includes PHABULOSA (PHB),
PHAVOLUTA (PHV) and REVOLUTA (REV)
(Byrne, 2006;
McConnell et al., 2001;
Otsuga et al., 2001;
Talbert et al., 1995;
Zhong and Ye, 1999). These
genes are all expressed throughout incipient primordia and later become
localised to the adaxial side of primordia
(Emery et al., 2003;
McConnell et al., 2001;
Otsuga et al., 2001;
Prigge et al., 2005;
Talbert et al., 1995;
Zhong and Ye, 1999). Combined
mutations in PHB, PHV and REV reduce adaxial fate, whereas
dominant mutations in the HD-ZIPIII genes show replacement of abaxial tissue
by adaxial tissue (Emery et al.,
2003; McConnell et al.,
2001; Ochando et al.,
2006; Prigge et al.,
2005; Zhong and Ye,
2004). HD-ZIPIII genes have a mutually antagonistic relationship
with KANADI genes, which encode GARP putative transcription factors
(Eshed et al., 1999;
Eshed et al., 2001;
Izhaki and Bowman, 2007;
Kerstetter et al., 2001).
KANADI genes are expressed abaxially in a pattern complementary to HD-ZIPIII
gene expression. Loss of two or more KANADI genes results in polarity defects,
and reduced abaxial fate is associated with ectopic outgrowths on the abaxial
side of leaves (Eshed et al.,
2004; Izhaki and Bowman,
2007).
One additional component of the leaf dorsoventral patterning network is the
MYB domain transcription factor ASYMMETRIC LEAVES1 (AS1).
Loss of function of the AS1 orthologue in Antirrhinum,
tobacco, tomato and pea results in adaxial defects, ranging from patches of
abaxial cells on the adaxial side of the leaf to leaves that are radial due to
complete loss of adaxial fate (Kim et al.,
2003; McHale and Koning,
2004; Tattersall et al.,
2005; Waites and Hudson,
1995; Waites et al.,
1998). By contrast, mutations in AS1 in
Arabidopsis have only subtle polarity defects
(Byrne et al., 2000;
Ori et al., 2000;
Xu et al., 2003). One
possibility is that AS1 in Arabidopsis contributes to leaf
polarity redundantly with other factors
(Byrne et al., 2000;
Garcia et al., 2006;
Huang et al., 2006;
Ueno et al., 2007).
We have isolated three enhancers of as1, called
PIGGYBACK1 (PGY1), PGY2 and PGY3, all of
which have a similar phenotype and condition ectopic leaf lamina outgrowths on
the adaxial side of the as1 leaf. We refer to this phenotype as a
`piggyback' phenotype, as ectopic outgrowths resemble epiphyllous structures
found on the adaxial side of the leaf of the `piggyback begonia' (Begonia
hispida var. cucullifera)
(Maier and Sattler, 1977).
Here, we describe the as1 pgy phenotype, and demonstrate that
AS1 and PGY1 independently promote dorsoventral polarity.
AS1 has minor interactions with the HD-ZIPIII-KANADI pathway, whereas
genetic interactions position PGY1 as an integral component of this
pathway. PGY1, PGY2 and PGY3 genes encode cytoplasmic large
subunit ribosomal proteins, L10a, L9 and L5. We propose that leaf-patterning
mechanisms involving the HD-ZIPIII-KANADI pathway include ribosome-mediated
translational regulation.
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MATERIALS AND METHODS |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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). All
pgy alleles segregate as single recessive loci. Mutants were
backcrossed to Landsberg erecta (Ler) twice before genetic
analysis. pgy2-2 was a GABI-Kat (128H07) T-DNA insertion line
(Rosso et al., 2003).
rev-6 was obtained from the Arabidopsis Biological Resource Centre
(ABRC). kan1-2 and kan2-1 were obtained from John Bowman.
All genetic interactions were in a Ler background. Plants were grown
either in soil or on Murashige and Skoog media at 22°C with a day length
of 16 hours.
Genetics
pgy genes were cloned using Ler x Columbia F2
mapping populations. For complementation a 2.1 kb genomic fragment
encompassing At2g27530, a 5 kb genomic fragment encompassing At1g33140 and a
3.5 kb genomic fragment encompassing At3g25520 were cloned into the binary
vector pMDC123 (Curtis and Grossniklaus,
2003) and transformed into pgy1-1/pgy1-1 as1/+, pgy2-1/pgy2-1
as1/+ and pgy3-1/pgy3-1 as1/+ plants, respectively, using
standard agrobacterium-mediated transformation
(Clough and Bent, 1998). For
each complementation construct, basta resistant plants with an as1
phenotype were confirmed as as1 pgy homozygotes.
as1-1 rev-6 was analysed in the F3 generation of the cross as1-1 x rev-6. In the F2 generation of this cross as1-1 rev-6 segregated at 1:15. pgy1-1 rev-6 were obtained from the F3 generation of the cross pgy1-1 x rev-6. Progeny from pgy1-1 rev-6/+ individuals segregated 1:3 pgy1-1 rev-6 mutants. as1-1 pgy1-1 rev-6 triple mutants were analysed in the F4 generation of the cross as1-1 pgy1-1 x as1-1 rev-6, after selfing as1-1 pgy1-1 rev-6/+ F3 plants. Segregation of as1-1 pgy1-1 rev-6 in this F4 generation was 1:3. as1-1 kan1-2 and pgy1-1 kan1-2 were obtained from the F3 generation of the respective crosses as1-1 x kan1-2 and pgy1-1 x kan1-2. as1-1 pgy1-1 kan1-2 triple mutants were identified in the F4 generation after selfing as1-1 pgy1-1 kan1-2/+ F3 plants from the cross of kan1-2 x as1-1 pgy1-1. Segregation of as1-1 pgy1-1 kan1-2 in this F4 generation was 1:3. Double and triple mutant combinations of as1-1, pgy1-1 and kan2-1 were generated in an identical manner. as1-1 kan1-2 kan2-1 or kan2-1/+, pgy1-1 kan1-2 kan2-1 or kan2-1/+ and as1-1 pgy1-1 kan1-2 kan2-1 or kan2-1/+ were analysed in the F3 and F4 generations of the respective crosses as1-1 x kan1-2 kan2-1/+, pgy1-1 x kan1-2 kan2-1/+ and as1-1 pgy1-1 x kan1-2 kan2-1/+. In progeny from as1-1 pgy1-1 kan1-2/+ kan2-1/+, plants with a suppressed as1-1 pgy1-1 phenotype segregated 6:10 and plants with a kan double mutant phenotype segregated 1:15. Combinations of pgy mutants in the as1-1 background were generated from the crosses of as1-1 pgy1-1 x as1-1 pgy2-1, and as1-1 pgy1-1 pgy2-1 x as1-1 pgy3-1. The genotype of all combinatorial mutants was confirmed either by sequencing or by CAPS analysis using allele-specific polymorphisms as listed in Table 1.
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) showed that all the designed primers bind with the same
efficiency to template. PCR reactions were performed using an Opticon
real-time PCR instrument (MJ Research). The PCR programme started at 94°C
for 2 minutes, followed by 40 cycles of 94°C (15 seconds), 60°C (30
seconds), 72°C (1 minute) and 76°C (1 second). Melting curves were
recorded from 65°C to 95°C, reading every 0.5°C. Quantification of
gene expression was carried out using the method of Livak and Schmittgen
(Livak and Schmittgen, 2001).
Results were normalised to that of ACTIN2.
In situ hybridisation
Non-radioactive in situ hybridisations were performed as previously
described (Long et al., 1996)
using 10-day-old seedlings. For the PGY probes, gene-specific
fragments were amplified using gene specific primers (see
Table 1) and cloned into the
vector pGEM-Teasy (Promega). Antisense and sense probes were transcribed with
SP6 or T7 polymerase following linearisation of the clone plasmid.
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).
For SEM analysis of as1 pgy1 rev mutants, tissue was fixed in 3%
glutaraldehyde and dehydrated through an ethanol series, before critical point
drying using a Watford Polaron and sputter coating with gold (Agar High
Resolution Sputter Coater). Samples were viewed using a Gemini Supra 55 VP SEM
under high vacuum with a beam accelerating voltage of 3 kV. For analysis of
leaf vasculature, tissue was fixed in 3% glutaraldehyde, dehydrated through an
ethanol series to 100% ethanol and embedded in JB4 resin (Agar Scientific).
Embedded tissue was sectioned at 3 µm and subsequently stained with 0.02%
Toluidine Blue. Images were obtained using a Nikon E800 microscope. Leaf 6 of
28-day-old plants was used for vascular sections. |
RESULTS |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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pgy1, pgy2 and pgy3 single mutants had a subtle phenotype compared with wild type, with formation of slightly pointed leaves and more prominent marginal serrations (Fig. 1A). Often these phenotypes were visible only early in development of rosette leaves. In contrast to single mutants, rosette leaves of as1 pgy1, as1 pgy2 and as1 pgy3 mutants were distinct from as1, and formed narrower, elongate leaves with adaxial ectopic lamina (Fig. 1B,C). Ectopic outgrowths were typically formed in the proximal region of late rosette leaves; however, the penetrance of this phenotype was environmentally conditioned, and in extreme cases ectopic outgrowths were formed on most rosette and cauline leaves. To determine the relationship between PGY genes we generated as1 pgy1 pgy2, as1 pgy2 pgy3 and as1 pgy1 pgy3 triple mutants and the as1 pgy1 pgy2 pgy3 quadruple mutant. Although the frequency of outgrowths was slightly increased in plants with multiple pgy mutations, leaf phenotypes were similar to as1 pgy double mutants, indicating that all three PGY genes contribute to the same developmental pathway (Fig. 1D and see Fig. S1 in the supplementary material). To further understand the developmental defect in these mutants we selected pgy1 for more detailed characterisation.
Initiation and development of ectopic leaf lamina in as1 pgy1 mutants
We analysed the developmental progression of as1 pgy1 outgrowths
using SEM. The proximal and adaxial regions of immature late rosette leaves
were examined. In wild-type leaves, larger cubical cells of the midvein are
evident in the medial region of the leaf, whereas smaller, less regular cells
of the lamina are in lateral regions (Fig.
2A). At a similar stage of development, cells in the midvein and
lamina regions of as1 leaves could be distinguished. These cells were
similar to wild type (Fig. 2B).
Early in development of as1 pgy1 mutant leaves, the adaxial surface
was characterised by the appearance of dome-shaped structures
(Fig. 2C) that developed into
radial, peg-like structures (Fig.
2D,E). Outgrowths subsequently became bifacial and leaf-like. One
side of fully mature outgrowths was trichome dense and dark green, similar to
the adaxial epidermis of wild-type leaves, whereas the opposing side of
outgrowths had very few trichomes and was pale green, similar to the abaxial
epidermis of wild-type leaves (Fig.
1C and Fig. 2F).
These epidermal features of mature outgrowths are consistent with the
establishment of dorsoventral polarity. Interestingly, the polarity of
outgrowths was always oriented with the adaxial side facing the distal tip of
the leaf and the abaxial side facing the proximal base of the leaf and the
meristem (Fig. 2F).
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; Lin et al.,
2003; McConnell and Barton,
1998; Waites and Hudson,
1995). Analysis of the adaxial surface of as1 pgy1
mutants did not reveal epidermal features suggestive of patches of abaxial
tissue on the adaxial side of the leaf
(Fig. 2). Another marker of
leaf-tissue polarity is vascular patterning. In Arabidopsis, leaf
vascular bundles develop dorsoventral polarity with xylem tissue in an adaxial
position above abaxial phloem (Fig.
3A). We used this anatomical feature to further investigate the
leaf defect in as1 pgy1. Transverse sections of leaf midveins of
as1 and pgy1 single mutants displayed a vascular pattern
similar to wild type (Fig.
3B,C). However, in the as1 pgy1 double mutants, sections
of the midvein had a disorganised and sometimes radial vascular pattern, with
phloem surrounding xylem (Fig.
3D). Radialisation of the vasculature occurred in regions of the
leaf below outgrowths. Both the ectopic outgrowths from the adaxial leaf
surface and the radial vascular pattern were consistent with defects in
adaxial fate in as1 pgy1 leaves.
rev enhances the as1 pgy1 leaf polarity defect
The dorsoventral polarity defect in as1 pgy1 leaves may occur
either through loss of adaxial fate or gain of abaxial fate. HD-ZIPIII family
genes PHB, PHV and REV act redundantly in specification of
leaf adaxial fate (Emery et al.,
2003; Prigge et al.,
2005). Loss of REV function results in formation of
longer and narrower leaves compared with wild type. rev mutants also
exhibit reduced lateral shoot meristem formation, a reduction in floral
meristem activity and vascular patterning defects
(Otsuga et al., 2001;
Talbert et al., 1995;
Zhong and Ye, 1999). To
determine whether PGY1 interacts with an HD-ZIPIII pathway, we
examined genetic interactions between as1, pgy1 and rev.
Double mutants, as1 rev and pgy1 rev, and the as1 pgy1
rev triple mutant were generated and leaf development in these mutant
combinations was compared with as1 and as1 pgy1.
pgy1 did not dramatically affect rev leaves, although
pgy1 rev double mutants had narrower leaves compared with
rev (Fig. 4A,B).
Rosette leaves of as1 rev mutants were more elongate and narrower
compared with as1 single mutants, and the leaf adaxial surface of
as1 rev was more rippled than that of as1
(Fig. 4C,D). In these respects
as1 rev leaves were similar to those of as1 pgy1. However,
as1 rev mutants did not develop ectopic outgrowths. By contrast,
as1 pgy1 rev triple mutants had a leaf phenotype more severe than
that of as1 pgy1, with formation of radial leaf-like structures
(Fig. 4E,F), suggesting a more
severe loss of adaxial fate. The as1 pgy1 rev phenotype indicates
that all three genes act to regulate leaf adaxial fate. However, REV,
PHB and PHV transcript levels were not significantly altered in
pgy1 or as1 pgy1 mutants, indicating that PGY1 does
not regulate transcription of these genes
(Fig. 6K). In contrast to a
previous report (Fu et al.,
2007), we found transcript levels of these three HD-ZIPIII genes
were also not significantly altered in as1 relative to wild type
(Fig. 6K).
pgy1 enhances rev inflorescence defects
In addition to leaf defects, rev mutants had a pronounced effect
on lateral meristem function, with fewer axillary meristems and abnormal
flowers (Fig. 5A,B).
Inflorescences of rev single mutants produce wild-type flowers, as
well as flowers with a reduced complement of inner whorl organs. Additionally,
rev floral meristems may fail to produce a flower, instead only
forming a terminal filamentous structure
(Otsuga et al., 2001;
Talbert et al., 1995).
Although the leaf phenotype of rev was only slightly modified by
pgy1, the inflorescence and flowers of rev were
significantly altered by pgy1. pgy1 rev inflorescences initially
formed one or two fertile flowers. Subsequent floral meristems only gave rise
to a terminal filamentous organ or did not produce organs
(Fig. 5C,D). The pgy1
enhancement of rev was similar to phv and phb/+
enhancement of rev. rev phv, rev phb/+ and rev phv phb/+
mutants initially produce several fertile flowers and subsequent floral
meristems mostly form a single radial organ
(Prigge et al., 2005). rev
phb phv/+ floral meristems also produce filamentous structures as with
pgy1 rev mutants (Fig.
5E,F). These interactions further support the suggestion that both
PGY1 and REV are together required for organ patterning.
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;
Eshed et al., 2004;
Kerstetter et al., 2001). To
further understand the interaction of PGY1 with the HD-ZIPIII-KANADI
dorsoventral patterning pathway we generated the as1 kan1 and
pgy1 kan1 double mutants and the as1 pgy1 kan1 triple
mutant. as1 kan1 leaves were only slightly different from those of
as1, being less rolled under at the margins
(Fig. 6A,B). The leaf phenotype
of pgy1 is subtle and no significant changes were apparent in the
pgy1 kan1 double mutants (data not shown). In contrast to as1
kan1, the as1 pgy1 kan1 triple mutant displayed significant
suppression of the as1 pgy1 phenotype. In the vegetative rosette,
as1 pgy1 kan1 leaves did not have the narrow, elongated shape of
as1 pgy1 leaves, and the triple mutant had a phenotype more like that
of as1 (Fig. 6D,E),
indicating that the suppression of the as1 pgy1 phenotype by
kan1 is mainly the effect of an interaction between pgy1 and
kan1. As with kan1, the as1 pgy1 phenotype was also
suppressed by kan2 (data not shown).
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; Izhaki and
Bowman, 2007). Therefore we tested if a dosage effect would have
consequences on as1 and as1 pgy1 mutants. We generated
as1 kan1 kan2/+ and as1 pgy1 kan1 kan2/+ combinatorial
mutants. Leaves of as1 kan1 kan2/+ were similar to those of as1
kan1, showing only mild suppression of as1
(Fig. 6A-C). By contrast, the
suppression of as1 pgy1 was more pronounced in as1 pgy1 kan1
kan2/+ mutants relative to as1 pgy1 kan1, with leaves broader
and rounder, and developing only few outgrowths
(Fig. 6D-F). These interactions
suggest an underlying dosage effect of KANADI function on pgy1.
Consistent with these genetic interactions, expression of KAN1 and
KAN2 was not significantly altered in as1 or pgy1,
whereas both KAN1 and KAN2 were slightly upregulated in
as1 pgy1 (Fig. 6K).
The suppression of the as1 pgy1 phenotype by kan mutations
suggest that ectopic expression of KANADI genes is a cause of the ectopic
outgrowths on the adaxial side of as1 pgy1 leaves.
To further test dose effects of kan mutants on as1 pgy1,
we generated as1 kan1 kan2 and pgy1 kan1 kan2 triple
mutants, as well as the as1 pgy1 kan1 kan2 quadruple mutant. Leaves
of as1 kan1 kan2 were more severely affected and smaller in size than
those of kan1 kan2, but otherwise had features of kan1 kan2
leaves (Fig. 6H)
(Ha et al., 2007). pgy1
kan1 kan2 leaves were indistinguishable from kan1 kan2 leaves
(Fig. 6I). In the as1 pgy1
kan1 kan2 quadruple mutant leaves had abaxial outgrowths as in kan1
kan2 (Fig. 6J). These
phenotypes indicate that neither AS1 nor PGY1 are required
for the severe adaxialised leaf phenotypes resulting from loss of both
kan1 and kan2. In the as1 pgy1 kan1 kan2 quadruple
mutants, outgrowths were often limited to the abaxial side of the leaves,
consistent with KAN requirement for the as1 pgy1
phenotype.
pgy1 suppresses kan gynoecium defects
KANADI genes repress HD-ZIPIII genes and kan mutant phenotypes are
in part due to ectopic HD-ZIPIII gene expression
(Eshed et al., 2001;
Izhaki and Bowman, 2007).
Genetic interactions indicate that PGY1 functions together with
REV in organ patterning and that pgy1 may enhance
rev through effects on other HD-ZIPIII genes. However, pgy1
does not suppress the strong leaf defect of kan1 kan2 mutants. To
further explore the relationship between AS1, PGY1 and KANADI genes,
we tested whether as1 and pgy1 could suppress other
kan mutant phenotypes. The kan1 kan2 double mutant has
dramatic effects on gynoecium development, with proliferation of ectopic
septum and ovules on the abaxial sides of the carpels
(Eshed et al., 2001). As with
the kan1 kan2 mutant, the combination of kan1 kan2/+ also
displayed gynoecium defects, with ectopic septum and style tissues between the
fused carpels, and an increase in apical style and stigma size
(Fig. 7F). In as1 kan1
kan2/+ mutants, gynoecia were smaller, but otherwise similar to those of
kan1 kan2/+ (Fig. 7G).
In pgy1 kan1 kan2/+ mutants, the characteristic silique phenotype of
kan1 kan2/+ (Fig.
7B,F) was suppressed by pgy1
(Fig. 7D,H). The siliques were
more elongated in pgy1 kan1 kan2/+ compared with kan1
kan2/+, and their morphology was similar to wild type
(Fig. 7A,E) except for
occasional ectopic style tissue along the abaxial replum
(Fig. 7H). pgy1 kan1
kan2/+ are fertile, whereas kan1 kan2/+ gynoecium defects result
in greatly reduced fertility. Therefore PGY1, but not AS1,
is required for the kan1 kan2/+ gynoecium phenotype.
PGY genes encode ribosomal proteins
PGY1, PGY2 and PGY3 were identified by positional
cloning, and all three genes were found to encode cytoplasmic large subunit
ribosomal proteins (Fig. 8A).
pgy1-1 had a base pair change resulting in a premature stop codon in
At2g27530. A second independent allele of pgy1, designated
pgy1-2, also had a base pair change resulting in a premature stop
codon in At2g27530. The as1 pgy1-2 mutant phenotype was the same as
as1 pgy1-1. This gene encodes ribosomal protein L10a, which is a
member of the L1p/L10e family, involved in binding and release of deacylated
tRNA from the E site of the ribosome
(Nikulin et al., 2003;
Yusupov et al., 2001). A point
mutation in pgy2-1 resulted in a splicing defect in At1g33140,
whereas an insertion mutant allele, pgy2-2, failed to accumulate
significant levels of transcript (see Fig. S2A in the supplementary material).
As with as1 pgy2-1 mutants, as1 pgy2-2 mutants formed
adaxial ectopic outgrowths. PGY2 encodes ribosomal protein L9, which
is a member of the L6p/L9e family. This ribosomal protein is located at the
base of the stalk protuberance, in a region important for
translation-initiation-factor binding (Ban
et al., 1999). A point mutation in pgy3-1 resulted in an
amino acid change in the protein encoded by At3g25520, which encodes ribosomal
protein L5. This ribosomal protein is a member of the L18p/L5e family.
L18p/L5e binds the 5S RNA and is involved in anchoring of peptidyl-tRNA during
translation (Meskauskas and Dinman,
2001).
|
). The
relatively subtle phenotype of pgy mutants may be due to redundancy
between ribosomal proteins in Arabidopsis,or PGY genes may
not have a role in global translation due to tissue-specific expression. To
test for possible differential expression between the PGY ribosomal
protein family members, we analysed expression in shoot tissues using RT-PCR.
All of these ribosomal protein genes were ubiquitously expressed in the shoot
(see Fig. S2B in the supplementary material). To investigate PGY
function in leaf development further, we analysed the mRNA expression pattern
of PGY1, PGY2 and PGY3 using in situ hybridisation. All
three PGY genes were expressed throughout the vegetative meristem and
in young organ primordia. In older organ primordia, expression was most
prominent in adaxial cells and in the margins of developing leaves
(Fig. 8B-D and see Fig. S3 in
the supplementary material). These high levels of expression are coincident
with small cytoplasmically dense cells. PGY genes, therefore, do not
appear to regulate organ patterning through tissue-specific expression. |
DISCUSSION |
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|
TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES |
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Development of ectopic leaves
Establishment of dorsoventral polarity in incipient leaf primordia requires
specification of both adaxial and abaxial domains. In a model in which leaf
outgrowth is promoted by juxtaposition of these two domains it might be
expected that an ectopic patch of one fate within the field of the other would
form a continuous boundary, and lamina outgrowth at this boundary would
surround the circumference of the ectopic patch. This appears to be the case
in Antirrhinum, where mutations in the AS1 orthologue
PHANTASTICA (PHAN) result in lamina surrounding ectopic
patches of abaxial tissue (Waites and
Hudson, 1995). Likewise, in tobacco plants with reduced
PHAN function, adaxial ectopic lamina outgrowth is contiguous along a
boundary of tissue with reduced adaxial fate
(McHale and Koning, 2004).
Ectopic lamina outgrowths in maize dorsoventral polarity mutants are also most
often formed as a continuum along an adaxial-abaxial boundary
(Evans, 2007;
Juarez et al., 2004a;
Juarez et al., 2004b;
Schichnes et al., 1997;
Timmermans et al., 1998). As
in these examples, outgrowths in as1 pgy1 mutants could result from
small patches of abaxial cells on the adaxial side of the leaf. However, in
as1 pgy1 mutants there was no clear evidence of abaxial cell types on
the adaxial epidermis of the leaf. One possibility is that ectopic abaxial
patches in subepidermal layers, such as in the vasculature, recapitulate an
adaxial-abaxial boundary for ectopic outgrowth.
An alternative, but not exclusive, possibility is that as1 pgy1
outgrowths are the result of establishment of a new proximodistal axis of
growth. Two of the earliest signatures of leaf primordia initiation are
downregulation of class I KNOX genes and formation of a localised auxin maxima
in the peripheral region of the meristem
(Heisler et al., 2005;
Jackson et al., 1994;
Reinhardt et al., 2000;
Reinhardt et al., 2003). In
addition, auxin has been implicated in the formation of ectopic outgrowths on
the hypocotyls of kan1 kan2 kan4 mutants
(Izhaki and Bowman, 2007).
Ectopic outgrowths in as1 pgy1 mutants may, likewise, initiate at
sites of a localised auxin maximum, possibly established through interactions
between patterns of ectopic KNOX expression, conferred by as1, and
regulators of auxin distribution.
There is no morphological evidence that outgrowths are associated with a structured meristem. In addition, the KNOX genes BP (also known as KNAT1 - TAIR) and KNAT2 are not required for as1 pgy1 outgrowths (M.E.B., unpublished), although the role of KNOX genes in the piggyback phenotype may be masked by redundancy. Interestingly, all bifacial outgrowths in as1 pgy1 mutants were oriented with the adaxial side towards the distal tip of the leaf and the abaxial side towards the proximal base of the leaf. This invariant polarity, in the absence of a meristem, suggests sensitivity to additional patterning cues.
PGY1 is a component of the HD-ZIPIII-KANADI pathway
Genetic interactions indicate that AS1 interacts to a minor extent
with the HD-ZIPIII-KANADI gene pathway. The as1 leaf phenotype was
only moderately affected by loss of REV, KAN1 and KAN2
genes. Potentially other members of these gene families are downstream of
AS1 and more dramatic polarity effects are masked by misexpression of
the YABBY gene FILAMENTOUS FLOWER (FIL) in as1
(Garcia et al., 2006;
Li et al., 2005).
In comparison, PGY1 has reciprocal interactions with both
HD-ZIPIII and KANADI family genes. PGY1 may have common downstream
targets with REV, or may regulate other HD-ZIPIII genes. Aspects of
as1 pgy1 leaf phenotypes resemble rev phv and rev phv
phb/+ mutant leaves. These combinatorial mutants exhibit a rippled leaf
surface and develop ectopic leaf lamina on the adaxial side of the leaf (this
study) (Prigge et al., 2005).
Likewise, the similarity of the pgy1 rev inflorescence phenotype to
the enhanced rev phenotype from loss of phv or
phb/+ opens the possibility that downstream targets of PGY1
are HD-ZIPIII genes.
Loss of KANADI function suppresses the leaf phenotype of as1 pgy1, and this suppression is specific to pgy1. Interactions with KANADI genes are also evident in the flower, and pgy1 can rescue the carpel patterning defects of kan1 kan2/+ mutants. However, neither as1 pgy1 nor pgy1 can rescue the kan1 kan2 phenotype. Therefore, PGY1 is not strictly necessary for kan1 kan2 phenotype, and pgy1 loss-of-function is not sufficient to compensate the loss of both KAN1 and KAN2. Together these interactions suggest an antagonistic relationship between PGY1 and KANADI genes, possibly through opposing interactions with a common downstream target. Potential common downstream targets are HD-ZIPIII genes, which are negatively regulated by KANADI genes and, as noted above, may be positively regulated by PGY1.
Potential role of translation in development
Most ribosomal proteins in animals are encoded by a single copy gene, and
mutations in these genes have gross effects on development. For example,
mutations in ribosomal protein genes in Drosophila result in a
semi-dominant Minute phenotype characterised by slow growth and
reduced size of heterozygotes, and homozygous lethality
(Lambertsson, 1998;
Marygold et al., 2007).
However, Drosophila Minute mutants also display various developmental
defects, as does the mouse Minute mutant belly spot and tail
(Bst; also known as Rpl24 - Mouse Genome Informatics), and
ribosomal protein mutants in zebrafish
(Amsterdam et al., 2004;
Oliver et al., 2004;
Uechi et al., 2006).
By contrast to animals, all ribosomal protein genes in Arabidopsis
are represented by small gene families
(Barakat et al., 2001).
Mutations in an S5 ribosomal protein gene, arabidopsis minute-like1
(aml1), are semi-dominant. As with Drosophila Minute
mutants, aml1 heterozygotes are smaller in size than wild type, and
homozygotes are embryo lethal (Weijers et
al., 2001). Unlike aml1, mutations in several ribosomal
protein genes are recessive and result in subtle developmental defects.
Mutations in POINTED FIRST LEAF (PFL) and POINTED FIRST
LEAF2 (PFL2), which encode an S18 ribosomal protein and an S13
ribosomal protein, respectively, have some reduced growth and changes to the
shape of early formed leaves (Ito et al.,
2000; Van Lijsebettens et al.,
1994). Mutations in SHORT VALVE1 (STV1), which
encodes an L24 ribosomal protein, are reduced in stature but, in addition,
display carpel-tissue-patterning defects
(Nishimura et al., 2005). This
phenotype mimics the floral phenotype of AUXIN RESPONSE FACTOR gene mutants,
ettin (ett) and monopteros (mp), and it has been
proposed that STV1 modulates ETT and MP expression
via translation of short upstream open-reading-frames (uORFs) encoded in the
5' UTR of ETT and MP transcripts
(Nishimura et al., 2005).
Mutations in PGY1, PGY2 and PGY3 and combined mutations
in these genes have relatively subtle effects on development, suggesting that
select targets are more sensitive to loss of these ribosomal proteins rather
than a global effect on protein synthesis. The nature of these three ribosomal
proteins does not immediately suggest a mechanism for the specificity of the
phenotype. One possibility is that PGY proteins have a function independent
from the ribosome, as reported for some other ribosomal proteins
(Wool, 1996). However,
PGY genes and related family members are expressed throughout
actively dividing tissues, as would be anticipated for ribosomal proteins
involved in global protein synthesis (this study)
(Schmid et al., 2005). An
alternate possibility is that not all ribosomes are equivalent. The presence
of different isoforms and post-translational modifications of ribosomal
proteins result in ribosome heterogeneity, and this may generate functionally
distinct ribosomes with target-transcript specificity
(Carroll et al., 2007;
Giavalisco et al., 2005;
Komili et al., 2007). This
appears to be the case in Saccharomyces cerevisiae, where mutations
in ribosomal protein paralogues have different phenotypic consequences
(Komili et al., 2007).
PGY target specificity may be conferred by interaction with other
proteins or protein complexes. An interacting complex may be the small RNA
silencing complex, RISC, which interacts with large subunit ribosomal proteins
(Chendrimada et al., 2007;
Ishizuka et al., 2002). Or
specificity may be inherent in target transcripts, either in non-coding UTR
sequences, as with STV1 targets or, for example, may be mediated
through the binding of small RNAs such as mircoRNAs or trans-acting siRNAs
(ta-siRNAs). In this respect, it is noteworthy that several leaf dorsoventral
polarity gene families are targeted by small RNAs. The adaxial HD-ZIPIII genes
are targets of microRNAs mir165 and mir166, whereas the
AUXIN RESPONSE FACTOR genes ETT and ARF4, which are required
for abaxial fate, are targets of TAS3-derived ta-siRNAs
(Allen et al., 2005;
Rhoades et al., 2002;
Tang et al., 2003). These
proposed models for PGY function are not necessarily mutually
exclusive, and it seems likely that global effects on translation are, to some
extent, masked by redundancy between family members in Arabidopsis.
Although the mechanism is still to be defined, PGY mutants provide
new insights into regulatory networks controlling leaf patterning and begin to
address the role of the ribosome as a regulator of development.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/135/7/1315/DC1
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ACKNOWLEDGMENTS |
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|
Footnotes |
|---|
Present address: University of Manchester, Manchester M13 9PT, UK
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REFERENCES |
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TOP
SUMMARY
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
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