1 The Horticulture and Food Research Institute of New Zealand, Private Bag 11
030, Palmerston North, New Zealand
2 Department of Plant Sciences, Oxford University, South Parks Road, Oxford, OX1
3RB, UK
3 Institute of Molecular BioSciences, Massey University, Private Bag 11 222,
Palmerston North, New Zealand
4 Plant Gene Expression Center, 800 Buchanan Street, Albany, CA 94710, USA
Author for correspondence (e-mail:
tfoster{at}hortresearch.co.nz)
Accepted 11 May 2004
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SUMMARY |
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Key words: Maize, liguleless1, Wavy auricle in blade1, Leaf development, Axial patterning, Mosaic analysis, Cell autonomy
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Introduction |
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Clonal analysis of leaf development indicates that the number of leaf
founder cells ranges from about 30 in Arabidopsis to approximately
250 in tobacco and maize (Poethig,
1984; Furner and Pumfrey,
1992
; Irish and Sussex,
1992
; Poethig and Szymkowiak,
1995
). In most dicots, the leaf founder cells occupy only a
portion of the radial dimension of the SAM, whereas in maize, a complete ring
of leaf founder cells surrounds the SAM
(Steffensen, 1968
). Most dicot
leaves first appear as peg-like outgrowths that subsequently grow in the
lateral dimension to form a flattened blade. Substantial evidence suggests
that the juxtaposition of adaxial and abaxial cell types stimulates lamina
outgrowth in dicot leaves (Waites and
Hudson, 1995
; McConnell and
Barton, 1998
; Bowman,
2000
; Kerstetter et al.,
2001
). In contrast, the maize leaf has a lamina from inception,
and furthermore, a number of mutations affect or even delete specific lateral
domains without affecting abaxial-adaxial asymmetry
(Scanlon et al., 1996
;
Fowler and Freeling, 1996
;
Foster et al., 1999
). These
findings suggest that fundamentally different sequences of pattern formation
occur in monocot and dicot leaves.
As the emerging leaf primordium grows away from the SAM, a new
proximodistal axis of growth is established, and cells differentiate according
to positional cues within the developing organ
(McConnell et al., 2001;
Matsumoto and Okada, 2003
). In
maize leaves, four distinct tissues develop along the proximodistal axis. The
proximal sheath and distal blade are separated by a fringe of ligule tissue
and two wedges of auricle tissue (Fig.
1E). The recessive liguleless1 (lg1) and
lg2 mutations remove ligule and auricle, but do not affect the
specification of blade and sheath (Emerson,
1912
; Brink, 1933
).
lg1 is expressed in leaf primordia in the zone of the developing
ligule and encodes a SQUAMOSA PROMOTER-BINDING protein
(Moreno et al., 1997
). Mosaic
analysis has shown that lg1 functions cell autonomously to specify
ligule and auricle (Becraft et al.,
1990
). lg1 has also been implicated in the propagation of
a signal to initiate ligule and auricle
(Becraft and Freeling, 1991
).
lg2, which encodes a bZIP transcription factor, is expressed
ubiquitously throughout the leaf primordia and functions non-cell autonomously
as shown by mosaic analysis (Harper and
Freeling, 1996
; Walsh et al.,
1998
). Based on double mutant analysis, it has been suggested that
lg1 and lg2 function in the same pathway
(Harper and Freeling,
1996
).
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Materials and methods |
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Seeds were allowed to imbibe for 48 hours at 25°C then irradiated with approximately 1,500 rads. The radiation was from a 6 MV photon (X-ray) beam generated by a linear accelerator at the Palmerston North Hospital Radiotherapy Unit, Palmerston North, New Zealand. Irradiated seeds were hand planted into soil at the Institute of Developmental Phenomenology, Raumai, New Zealand.
Sector analysis
Plants were grown to maturity and screened for albino
(w3/), and yellow (v4/) sectors throughout
development. Out of 1681 irradiated seeds, 93 w3 wab1+/
sectored leaves were identified in 42 Wab1/wab1+ plants and 51
sectored leaves were identified in 32 wab1+/wab1+ control plants. In
the second experiment, 4,608 seeds were irradiated; 115 w3
wab1+/ sectors and 65 v4 wab1+/ sectors were
identified in 81 lg1-R/lg1-R; Wab1/wab1+
plants. In 46 lg1-R/lg1-R; wab1+/wab1+ control plants, 90
w3 wab1+/ and 50 v4 wab1+/ sectors were
analysed. All sectored leaves were harvested at maturity and photographed
and/or photocopied. Leaf number, sector width and the lateral position of the
sector within the blade and sheath were recorded. See supplemental material
(http://dev.biologists.org/supplemental/)
for details of data analysis.
Transverse hand sections of freshly harvested sectored leaves were examined by epifluorescence microscopy using a Leica (MZFLIII) stereomicroscope equipped with a 395-440 nm excitation filter and a 470 nm observation filter. All sections were photographed using a DC200 digital camera (Wetzlar, Germany). Under these conditions, normal chloroplasts fluoresce bright red and cell walls appear blue-green. No chlorophyll autofluorescence is detected in w3/ cells. The presence or absence of chlorophyll in epidermal layers was scored by inspecting guard cells, the only chloroplast-containing cell-type in the epidermis. Sectors of v4/ appear yellow because of a delay in the accumulation of chlorophyll, but eventually become green. Boundaries of v4 sectors were marked with a pen.
Scanning electron and light microscopy
Mature leaf tissue was fixed in 3% glutaraldehyde and 2% paraformaldehyde
in 0.1 M phosphate buffer. Prior to fixation, a small notch was made at the
sector boundary (SEM samples only). Samples for SEM were dehydrated in
acetone, critical-point dried in liquid CO2 and sputter coated with
25 nm gold using a Polaron E 5400 sputter coater (SCD-050; Bal-Tec, Balzers,
Liechtenstein). Specimens were examined on a Cambridge 250 Mark III scanning
electron microscope (Cambridge Instruments, Cambridge, UK) operated at 20 kV,
and images were captured on 35 mm film. Samples for light microscopy were
infiltrated and embedded in Procure 812 (ProSciTech, Kelso, Australia).
Sections (1 µm) were cut, heat mounted, stained with 0.05 (w/v) Toluidine
Blue and photographed with an Axioplan microscope equipped with an Axiophot
camera (Zeiss, Jena, Germany).
lg1 and lg2 gene expression
Leaf primordia (P9-10) were removed from the shoot, the ligule region
dissected and immediately placed in liquid nitrogen. Leaf primordia (P6-8)
were removed, dissected 5 mm above their base for a pre-ligule tissue sample
and a further 5 mm above this for a blade tissue sample and immediately placed
in liquid nitrogen. The remaining five plastochrons and SAM were used as a SAM
sample. Each RNA sample consisted of a pool of ten seedlings. Tissue
dissection, RNA isolation and cDNA synthesis were each performed twice
independently, in each case giving identical results. Gene-specific PCR
primers were as described for lg1
(Moreno et al., 1997) and
lg2 (Walsh et al.,
1998
). 20 PCR cycles were performed and amplified products were
detected by Southern hybridization with gene-specific probes.
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Results |
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We constructed double mutants between Wab1 and lg1-R and
lg2-R to analyse the effect that loss of auricle tissue would have on
the Wab1 phenotype. The recessive lg1 and lg2
mutations remove ligule and auricle, giving the mutant leaves a more upright
appearance (Fig. 1D)
(Harper and Freeling, 1996).
Despite the lack of ligule and auricle, lg1-R and lg2-R
leaves have a distinct boundary between blade and sheath
(Fig. 1H). lg1-R
affects all but the uppermost leaves, whereas lg2-R only affects
juvenile leaves (Harper and Freeling,
1996
). lg1-R;Wab1 double mutants exhibit a striking,
narrow leaf phenotype (Fig.
1C,G). Both the normal and ectopic auricle tissue is absent in the
double mutant, most of the proximal blade deleted and sheath-like tissue
extends along the margins of the residual blade. lg2-R;Wab1 and
lg1-R;lg2-R;Wab1 mutants are similarly affected (data not shown).
The ectopic tissue in lg1-R;Wab1 leaf blades has histological and epidermal features of sheath. The adaxial surface is hairless and cells are long with smooth cell wall junctions (Fig. 2M), but the abaxial surface is covered with hairs specific to abaxial sheath tissue (not shown). lg1-R;Wab1 sheath-like tissue is very thin in the transverse dimension (Fig. 2K) and the intervascular spacing and prominent transverse veins resemble those found in marginal sheath tissue (Fig. 2G). In distal positions and near the midrib, lg1-R;Wab1 leaves have normal blade tissue (not shown). Sheath tissue identity is not affected by the lg1, lg2 or Wab1 mutations.
lg1-R leaf shape
Although the lg1-R ligule defect has been well described by
others, the altered shape of lg1-R leaves has not been reported. We
found that lg1-R leaves are significantly narrower at the
blade-sheath boundary than those of non-mutant (Lg1+/lg1-R)
siblings (Table S1,
http://dev.biologists.org/supplemental/).
The mean width of the ninth leaf counting down from the tassel was 76 mm for
lg1-R plants, whereas, the mean width was 102 mm for non-mutant
siblings. A similar trend was seen for the tenth and eleventh leaves down from
the tassel. We also noted that while the overall lengths of lg1-R and
Lg1+/lg1-R leaves are the same, lg1-R blades are
shorter and lg1-R sheaths are longer than those of non-mutant
siblings (Table S1). This finding indicates that the blade-sheath boundary is
established in a more distal position in the lg1-R mutant.
We compared the width of w3-marked clonal sectors in wild-type (Lg1+/Lg1+) and lg1-R plants. Sectors were measured at the base of the blade. Only sectors in adult leaves were included in this analysis to minimise variation in leaf size (see Supplemental data, http://dev.biologists.org/supplemental/). Sectors near the midrib had similar median widths in wild-type and lg1-R blades. However, sectors in lateral and marginal regions were significantly narrower in lg1-R mutants than in wild-type leaves (Table S2, http://dev.biologists.org/supplemental/). These data indicate that the lg1-R lateral growth defect is localised to lateral and marginal domains of the blade.
lg1 is misexpressed early in development of Wab1 leaves
The dramatic effect of lg mutations on the Wab1 phenotype
suggests that the presence of lg1 and lg2 partially
compensates for the defects in leaf width and tissue identity in Wab1
mutants. We carried out RT-PCR to see if lg1 or lg2 were
expressed differently in Wab1 mutants. Previous efforts to detect
lg1 or lg2 by in situ hybridisation have not been successful
(Moreno et al., 1997) (Walsh
and Freeling, personal communication). lg1 transcript is absent from
wild-type tissue samples containing the SAM and P1-5 primordia, but expression
is detected in equivalent Wab1 tissue at 20 PCR cycles
(Fig. 3). This early expression
in Wab1 was confirmed using a dilution of cDNA in the PCR reaction.
Transcript was never detected in equivalent wild-type tissue at 40 PCR cycles
(data not shown). lg1 expression was detected in both wild-type and
Wab1 leaf primordia in the preligule band region of P6-8 and the
ligule ridge region of P9-10 leaves (Fig.
3). Transcript was absent from the blade region of wild-type P6-8
leaves at 20 PCR cycles. Expression of lg1 was reproducibly detected
in the blade region of Wab1 P6-8 primordia at 20 PCR cycles and
confirmed using a dilution of cDNA in the PCR reaction. This result indicates
that the expression domain of lg1 extends distally in Wab1
leaf primordia, consistent with the distal extension of auricle tissue in
mature Wab1 leaves.
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Mosaic analysis of Wab1
Sectors of tissue lacking the dominant Wab1 allele
(wab1+/) were created in both Wab1 and
lg1-R;Wab1 mutants to determine if Wab1 disrupts leaf
patterning in a cell-autonomous manner (Fig. S1,
http://dev.biologists.org/supplemental/).
Stocks carrying Wab1 in repulsion to white seedling3
(w3) were X-irradiated to induce random chromosome breaks.
Radiation-induced breaks proximal to W3 resulted in albino,
non-Wab1 (w3 wab1+) sectors in otherwise green,
Wab1 or lg1-R;Wab1 plants. In lg1-R;Wab1 plants,
chromosome breaks proximal to Virescent4 (V4) created
yellow, lg1-R (v4 wab1+;lg1-R) sectors. The loss of
W3 in normal plants, and either W3 or V4 in
lg1-R plants, provided control sectors that were hemizygous for
chromosome 2L.
To ensure that the chromosome arm carrying Wab1 was lost early in leaf development, only sectors that extended through both the sheath and blade were analysed. Given the variability of the Wab1 phenotype, only sectors adjacent to tissue displaying a mutant phenotype could be scored. Thus, of 273 total sectors, only 77 were scorable for tissue identity. Sectors adjacent to ectopic auricle and sheath tissue were analysed for phenotypic expression (mutant or wild type) and cell layer composition (green or albino) (Table 1). Because v4 sectors eventually accumulate normal amounts of chlorophyll, it was difficult to determine the internal layer composition of yellow, v4 sectors in mature leaves. Thus, only w3 sectors were scored for albino versus green mesophyll and epidermal layers. We predicted that white or yellow sectors would have normal blade tissue if Wab1 functions cell autonomously, while the white or yellow sectors would have the same mutant phenotype as the adjacent green tissue if Wab1 acts in a non-autonomous manner.
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Of the seven sectors that displayed auricle characteristics through all or part of the sector, six had one or more inner layers of green, Wab1 cells (Table 1). These results indicate that Wab1 generally acts cell autonomously in the lateral dimension, but may act non-cell autonomously between cell layers.
An interesting pattern was observed in Wab1 plants with mild auricle extension phenotypes. In most cases, sectors in these plants had an auricle extension to the midrib side of the sector, but recovered normal tissue identity both within the sector and on the marginal side of the sector (e.g. Fig. 4A,B). In plants exhibiting more severe phenotypes such as ectopic auricle and sheath, sectors with normal tissue identity were flanked by mutant tissue on both sides. These results suggest that normal (wab1+) cells may have a directional effect on adjacent Wab1 cells. There was no obvious relationship between recovery of tissue identity and sector size.
Ectopic sheath in Wab1 and lg1-R;Wab1 mutants
In Wab1 mutants, 75% (15/20) of the sectors adjacent to ectopic
sheath exhibited normal blade characteristics. These results also indicate
that Wab1 generally disrupts tissue patterning in a cell-autonomous
manner (Table 1).
Fig. 4J shows an albino sector
adjacent to a region of ectopic marginal sheath tissue, and
Fig. 4I is a transverse section
through this sector boundary. The green, Wab1/wab1+ mutant tissue has
characteristics of marginal sheath tissue; it is thin, has widely spaced
veins, the adaxial surface is hairless, and the abaxial surface has long hairs
without multicellular bases (Fig.
4I). In contrast, the adjacent albino wab1+/
tissue exhibits histological organisation and epidermal features specific to
normal blade tissue (Fig.
2D).
In lg1-R;Wab1 double mutants, all (26/26) scorable wab1+/ sectors exhibited normal blade characteristics, indicating that Wab1 acts completely autonomously in the absence of Lg1+ (Table 1). The widest sectors were located at the margin, and restored the leaf half to a more normal shape and width (Fig. 5A,B). Fig. 5A shows a yellow wab1+ v4/ sector that occurred at the margin. The yellow blade tissue has almost doubled the width of the leaf base. The sector shown in Fig. 5C was sectioned and examined by SEM (Fig. 5E,D). In transverse section, there is a sharp boundary between albino wab1+/ blade tissue and green Wab1/wab1+ tissue with veins appressed against the abaxial surface, typical of sheath (Fig. 5E). The SEM shows crenulated blade cells to the left of the sector boundary (arrowhead), and smooth-walled, elongated sheath-like cells to the right (Fig. 5D). Fig. 5F is a transverse section through another sector boundary, illustrating the abrupt transition between albino blade tissue and green tissue with long abaxial hairs and other characteristics typical of marginal sheath.
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Effect of Wab1 sectors on leaf width
The leaf blades of Wab1 and especially lg1-R;Wab1 mutants
are significantly narrower than those of non-mutant siblings. To investigate
the effect of wab1+/ sectors on Wab1 and
lg1-R;Wab1 leaf width, the width of sectored and non-sectored halves
of each leaf were measured and compared (see Supplemental data,
http://dev.biologists.org/supplemental/).
In both Wab1 and lg1-R;Wab1 plants, there is a small but
significant increase in the median width of the sectored half of the blade
relative to the non-sectored half (Table
2, Table S3). Measurements made at the sheath midpoint show no
significant difference in width between leaf-halves, indicating that the
Wab1 mutation specifically disrupts lateral growth of blade tissue
(Table S3). No difference between the widths of sectored and non-sectored
leaf-halves is found in wild-type and lg1 control plants.
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Many of the widest sectors in lg1-R;Wab1 plants were yellow, v4 sectors. To test if there was a difference in behaviour between v4 and w3 sectors, the median difference in leaf-half widths was evaluated separately for yellow and white sectors in lg1-R;Wab1 and lg1-R plants. Sectors near the midrib were not included in this analysis as we had previously determined that they have no significant effect on leaf width. Surprisingly, yellow sectors had a significantly greater effect on leaf width than the white sectors (Table 2B). No difference was detected between yellow and white sectors in lg1-R controls, indicating that this effect is not inherent to v4 sectors, but only occurs in a Wab1 background.
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Discussion |
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Lg1+ influences cell autonomy of the Wab1 phenotype
In the majority of Wab1 and in all lg1-R;Wab1 leaves,
scorable wab1+/ sectors exhibited characteristics of normal
blade tissue, whereas adjacent tissue differentiated inappropriately as sheath
or auricle. The sharp boundaries between tissue types were coincident with
sector boundaries, indicating that Wab1 generally acts cell
autonomously in the lateral dimension to disrupt normal proximodistal
patterning.
Twelve of the 51 scorable sectors showed some aspect of the Wab1 mutant phenotype and thus are exceptions to the general rule of cell autonomy. Of these 12, two were completely albino and therefore had no layer with Wab1. Of the 10 remaining sectors, half carried Wab1 only in the epidermis, and half carried Wab1 in the epidermis and/or one mesophyll layer. Thus, Wab1 may act non-autonomously in the lateral dimension and/or between cell layers to influence cell identity in wab1+/ tissue.
In contrast, all sectors in lg1-R;Wab1 plants had normal cell types. Wab1 in either the epidermis or a single mesophyll layer did not condition the mutant phenotype (12 of 26 sectors). These results suggest that normal lg1 function is required for Wab1 to act non-autonomously.
We also observed a few cases of non autonomy in which the normal blade phenotype (wab1+) was seen on the margin side of the sector as well as within the sector (e.g. Fig. 4A,B). The extension of the normal phenotype from the sector into genetically Wab1 cells was only seen in mildly affected plants. This pattern could reflect the fact that the Wab1 phenotype is most severe in the lateral domain. Alternatively, it may be that once correct proximodistal patterning is established within wab1+/ tissue, this information can be propagated towards the margins into Wab1/wab1+ tissue, but only if Wab1 activity is low. Interestingly, non-autonomy was never documented in lg1-R;Wab1 plants. Cells in lg1-R;wab+/ sectors always had blade identity and cells outside of these sectors always had sheath identity. Thus, lg1 may affect the autonomy of Wab1 in both lateral and transverse dimensions.
Mosaic analyses of lg1-R have indicated that lg1 is
involved in signal propagation, while also acting cell autonomously to induce
ligule and auricle (Becraft et al.,
1990; Becraft and Freeling,
1991
). One of the key findings of this work was the observation
that ligule and auricle reinitiated immediately within Lg1+/lg1-R
tissue on the margin side of lg1-R/ sectors, but was displaced
proximally. The authors interpreted this as evidence that lg1 is
involved in the propagation of a `make ligule and auricle' signal, and that
this signal moves from the midrib towards the margins. Our observations
support this hypothesis.
Our data suggest that Wab1 alters positional information in an autonomous manner, resulting in inappropriate cell differentiation. We speculate that lg1 is responsible for the non-autonomous effects of Wab1 that were observed in our mosaic analysis. According to this model, lg1 may occasionally transmit the signal to initiate ectopic auricle from Wab1 tissue into wab1+/ sectors (Fig. 6A). Similarly, lg1 may relay correct positioning of the auricle and ligule from wab1+/ sectors into adjacent Wab1 tissue. In the absence of lg1, there is no lateral signalling from Wab1 tissue into wab1+/ sectors, or from sectors into Wab1 tissue (Fig. 6B).
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In both lg1-R;Wab1 and Wab1 leaves, sectors positioned
near the midrib had no significant effect on leaf-half width, whereas sectors
in the outer two thirds of the leaf-half were associated with significant
differences between sectored and non-sectored leaf-half widths. This result
could reflect the fact that sectors near the midrib tend to be very narrow,
and hence have a minimal effect on lateral growth. Alternatively, it may
reflect the fact that the Wab1 phenotype primarily affects regions
outside the midrib domain (Hay and Hake,
2004).
The role of lg1 in leaf morphogenesis
Our study provides evidence of previously unreported functions of
lg1 in leaf morphogenesis. We found that lg1-R leaves have
longer sheaths and shorter blades than non-mutant
(Lg1+/lg1-R) siblings, thus the blade-sheath boundary is
shifted distally (this is shown schematically in
Fig. 7A,B). This suggests that
lg1 is required for correct positioning of the blade-sheath
boundary.
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We suggest that the misexpression of lg1 is responsible for the
ectopic auricle and much of the lateral growth at the base of Wab1
blades. This is reflected in the shape of Wab1 leaves, which are
relatively wide at the base of the blade, but narrow in more distal areas
(Fig. 7C). We speculate that
the lateral signalling function of lg1 permits some recovery of
proximodistal patterning at the margins of Wab1 leaves
(Fig. 7C). In the absence of
lg1, Wab1 leaves never establish blade in this region, and are
extremely narrow (Fig. 7D). A
cell lineage analysis in lg1-R, Wab1 and double mutant backgrounds,
similar to that carried out for narrow sheath
(Scanlon and Freeling, 1997),
would help elucidate cell division patterns in these mutants.
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ACKNOWLEDGMENTS |
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Footnotes |
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* These authors contributed equally to the work
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