1 Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla,
CA 92037, USA
2 Division of Biological Sciences, University of California San Diego, La Jolla,
CA 92093, USA
3 Department of Plant Sciences, The University of Arizona, Tucson, AZ
85721-0036, USA
4 Department of Plant and Microbial Biology, University of California, Berkeley,
CA 94720, USA
5 Department of Molecular Biology, Max Planck Institute for Developmental
Biology, D-72076 Tübingen, Germany
* Author for correspondence (e-mail: weigel{at}weigelworld.org)
Accepted 28 October 2003
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SUMMARY |
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Key words: Arabidopsis thaliana, Leaf development, Bract development, Flower development, JAGGED, APETALA1
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Introduction |
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While our understanding of the specification of organ identity is advanced,
a mechanistic understanding of the processes that sculpt lateral organs is
only now emerging. In Antirrhinum, two members of the TCP family of
transcription factors, encoded by CINCINNATA (CIN) and
CYCLOIDEA (CYC), have been implicated in the regulation of
lateral organ development (Cubas et al.,
1999). CIN controls growth of the leaf blade and is
required to generate flat leaves with zero Gaussian curvature
(Nath et al., 2003
).
cin mutants develop excessive growth at the periphery of the leaf
blade, resulting in wavy leaves. Interestingly, CIN appears to
prevent excessive growth by sensitizing peripheral cells to a cell-cycle
arrest front that moves from the tip of the leaf to the base. CYC,
which also appears to regulate growth via effects on the cell cycle,
suppresses growth of dorsal floral structures, producing the asymmetric
flowers typical of Antirrhinum
(Gaudin et al., 2000
;
Luo et al., 1996
). It is
interesting to note that both genes appear to affect organ shape by promoting
differentiation.
We have characterized JAGGED (JAG) (formerly BRACTS), a gene involved in the formation of lateral organs. JAG encodes a putative transcription factor with a single C2H2 zinc-finger domain and is expressed in the growing regions of lateral organs. Mutations in JAG most severely affect the distal regions of organs, resulting in a jagged edge. In petals, the entire distal half of the organ can be eliminated. In jag mutants, cell-cycle activity declines earlier that in wild type, suggesting that JAG promotes distal petal development by suppressing premature cell-cycle arrest. Misexpression studies with an activation-tagged allele reveal that JAG can promote the growth of many different tissues including the cryptic bract. We discuss a possible role for JAG in maintaining growth of lateral organs and in the diversification of plant form.
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Materials and methods |
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Plant growth and material
Plants were grown under a 3:1 ratio of Cool White and Gro-Lux (wide
spectrum) fluorescent lights at 23°C in long day conditions (16 hour
light, 8 hour dark).
Wild type was either Columbia [Col-0, Col glabrous (Col
(gl)] or Wassilewskija (Ws). jag-1 and jag-4 were
identified by screening the University of Wisconsin Knockout collection
(Krysan et al., 1999) using
JAG-specific primers N-1365 and N-1366 (see Supplementary Table 1 for
oligonucleotide sequences; Table S1,
http://dev.biologists.org/supplemental).
The jag-1 allele is disrupted by a T-DNA derived from pSKI015;
jag-4 by a T-DNA derived from pD991, which contains an
AP3::GUS fusion. As has been observed in other lines derived from
this collection
(http://www.biotech.wisc.edu/Arabidopsis/),
jag-4 has defects in the development of petals and stamens that
appear to be due to co-suppression by AP3 sequences in the T-DNA (see
Fig. S1,
http://dev.biologists.org/supplemental).
The jag-5D mutation was obtained from a population of
Col(gl) pop1-/- plants
(Preuss et al., 1993
)
transformed with pSKI015 (Weigel et al.,
2000
). jag-5D is linked to the pop1 mutation.
The effect of jag-5D on lateral organ development was the same in
Col-0 and Col(gl). ap1-15 is in Col-0
(Ng and Yanofsky, 2001
).
Transgenic Col-0 plants were generated by floral-dip method
(Clough and Bent, 1998
).
Genotyping of jag-1 used primers oJD126 and oJD127, to amplify a
0.7 kb fragment from the wild-type locus. To detect the jag-1 allele,
a T-DNA-specific oligonucleotide, JL202, and N-0681 were used to amplify a 1.1
kb fragment. Genotyping of jag-5D was done using N-1509, N-1510 and
SKC12 in a single PCR reaction. PCR products were digested with EcoRV
producing a band of 0.5 kb representing the wild-type allele and a band of 0.4
kb representing jag-5D. jag-5D homozygotes can also be distinguished
by phenotypes associated with the pop1 mutation
(Preuss et al., 1993).
Genotyping of ap1-15 was as described previously
(Ng and Yanofsky, 2001
).
Biometric analysis
The third and fourth rosette leaves from Ws and jag-1 plants were
scanned. Area and perimeter of leaf blade region were measured using the NIH
Image program (developed at the US National Institutes of Health and available
at
http://rsb.info.nih.gov/nih-image/).
Cloning of JAG genomic locus and cDNA
Plasmid rescue of jag-5D genomic DNA was performed as described
previously (Weigel et al.,
2000). pJDP2, which was used for jag-5D recapitulation,
was plasmid rescued from PstI digested jag-5D genomic DNA.
An initial JAG cDNA clone was obtained by RT-PCR (see below) using
primers targeting exonic sequences predicted by Genscan
(Burge and Karlin, 1997
).
5' and 3' RACE (rapid amplification of cDNA ends) was performed
using the First Choice RLM-RACE kit (Ambion, Inc.) according to the
manufacturer's instructions. A full-length cDNA was obtained using N-0335 and
N-0336. An initial JAGGED-LIKE (JGL) cDNA was amplified
based on the At1g13400 gene model. A full-length JGL clone was
obtained using oJD119 and oJD120 (pPY1).
Construction of transgenic lines
The JAG recapitulation construct pJD71 was made by isolating a
HindIII/ClaI fragment containing the genomic region and
35S enhancer elements from pJDP2 and subcloning it into pBJ36 (pJD63)
(Gleave, 1992). The cassette
was then shuttled into pART27 (pJD71). For AP1::JAG, the JAG
cDNA was PCR amplified from first-strand cDNA with Pfu Turbo
polymerase (Stratagene), using primers N-0680 and N-0681, to introduce
HindIII and BamHI restriction sites. The product was cloned
into pBluescript-SK+ and sequenced (pJD37). The JAG
fragment was subcloned into pJD33 (Wu et
al., 2003
), replacing the AP1 cDNA (pJD41). For
AP1::JAG:GFP, the JAG cDNA was PCR amplified from pJD37 with
N-0680 and N-1413, adding a HindIII site to the 5' UTR and
replacing the stop codon with a PstI site (pJD62). GFP
coding sequence was amplified from pCAMBIA1302
(Hajdukiewicz et al., 1994
),
replacing the start codon with a PstI site and adding an
XbaI site to the 3' UTR (pJD60). JAG was then
translationally fused to GFP and shuttled into pJD51
(Wu et al., 2003
), replacing
AP1:GFP with JAG:GFP (pJD105).
Scanning electron microscopy
Samples for scanning electron microscopy were fixed for 4.5 hours in FAA
(50% ethanol, 5% acetic acid, 3.7% formaldehyde) at room temperature,
dehydrated through an ethanol series and critical point dried. Samples were
sputter-coated using gold and palladium and viewed using a Quanta 600
microscope.
In situ hybridization
In situ hybridization was carried out as described previously
(Long et al., 1996;
http://www.its.caltech.edu/~plantlab/protocols/insitu.htm)
with the following modifications. Tissue samples were fixed in FAA for 2.5
hours at room temperature. RNase treatment of slides was left out. Substrate
solution for alkaline phosphatase color reaction was prepared using 2% of a
NBT/BCIP stock solution (Roche Diagnostic, Germany) in 100 mM Tris pH 9.5, 100
mM NaCl, 50 mM MgCl2.
The JAG probe was transcribed using T3 RNA polymerase (Promega) from pJD37 linearized with HindIII. A HISTONE 4 (H4) cDNA clone was obtained by RT-PCR amplification of ATHH4GA (GenBank accession number M17132) from inflorescence tissue using oJD133 and oJD134 and cloned into pBluescript-SK+ (pH4-T7). H4 probe was transcribed using T7 RNA polymerase (Promega) from pH4-T7 linearized with HindIII. FIL probe was transcribed using T7 RNA polymerase from pY1-Y (provided by J. Bowman) linearized with EcoRI.
RT-PCR
RNA isolation and reverse transcription were performed as described
previously (Kardailsky et al.,
1999). PCR amplification was performed on 2 µl of reverse
transcription reaction. A fragment of the JAG gene that spans the
entire coding sequence was amplified using N-0680 and N-0681. A JGL
fragment was amplified using oJD119 and oJD120. A TUBULIN fragment
was amplified as a control using N-1136 and N-1137. The number of PCR cycles
performed is indicated in Fig.
5. Annealing temperature was 58°C for all reactions.
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Results |
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Inactivation of JAG affects the shape of most lateral organs including leaves and floral organs (Fig. 1). Rosette leaves in the parental Ws strains are paddle shaped and have a smooth edge (Fig. 1A). jag-1 leaves, however, develop with a serrated edge (Fig. 1B). To quantify these shape changes, the area and perimeter of rosette leaf blades were measured. While leaf blade area is not significantly different, jag-1 leaves have a larger perimeter/area ratio (P=0.0016), reflecting the irregular blade margins of these leaves (see Table S2, http://dev.biologists.org/supplemental). All four whorls of floral organs are also affected in jag-1, with the defects being most apparent in sepals, petals and stamens (Fig. 1C,D). These defects are more severe in flowers produced late in development.
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Wild-type stamens consist of two components: the anther and the filament
(Bowman, 1993). jag-1
filaments appear normal (Fig.
1C,D), but anthers are reduced with an altered shape and typically
produce less pollen than wild-type ones
(Fig. 1I,J). Late flowers are
often male-sterile. Carpel development is relatively normal, but under some
growth conditions, surface irregularities develop along the valve walls (data
not shown). Thus, JAG is required for the proper formation of all
lateral organs, with a particularly important role in the development of the
distal regions of sepals, petals and stamens.
Premature differentiation of petals in recessive jag mutants
Because inactivation of JAG has such severe effects on petal
shape, we further explored the role JAG plays in petal development.
To test whether the loss of distal petal tissue could reflect reduced cell
division, we analyzed the expression of the HISTONE 4 (H4)
gene, which has previously been used to assay cell-cycle activity in
developing tissues (Gaudin et al.,
2000; Krizek,
1999
; Nath et al.,
2003
). H4 expression correlates with the expression of
other cell-cycle markers such as Cyclin D3b in Antirrhinum
(Fobert et al., 1994
). As in
Antirrhinum, at any given time only a fraction of cells show strong
H4 expression (Fig.
2B,C). In wild-type petals, the number of cells expressing
H4 increases during floral stages 7 and 8
(Fig. 2A,B)
(Smyth et al., 1990
). The
number of H4-positive cells plateaus during stages 9, 10 and 11, and
it begins to fall at stage 12. This peak in the number of H4-positive
cells correlates with the rapid growth of petals during stages 9-11
(Smyth et al., 1990
).
H4-expressing cells are also much more frequent in the distal region
of petals, especially during stages 8-10.
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Activation of ectopic growth in the dominant jag-5D mutant
We also characterized a JAG gain-of-function allele,
jag-5D, which was obtained using enhancer activation-tagging, in
which a T-DNA with a multimerized, constitutively active enhancer is randomly
inserted in the genome (Walden et al.,
1994; Weigel et al.,
2000
). jag-5D mutants have a striking phenotype, with
bract-like organs forming ectopically on the inflorescence, subtending most
flowers (Fig. 3A-C). These
leaf-like organs have stipules, lack a petiole, are pointed at their tip, and
exhibit delayed senescence, confirming their identity as bracts
(Fig. 3D,E, and data not
shown). Using scanning electron microscopy, we found that the bracts emerge
from the inflorescence meristem, with floral meristems subsequently developing
in their axils (Fig. 3K,L,
Fig. 6I). Thus, the bract in
jag-5D is a product of the shoot and not the floral meristem. The
degree of bract development varies from flower to flower, with alternating
waves of nodes with and without bracts
(Fig. 3B). The size and shape
of bracts also vary, such that the bracts can be large and laminar or small
and filamentous (Fig. 3D).
Bracts tend to be slightly jagged (Fig.
3D), and carpelloidy is sometimes seen in late developing bracts,
which are tipped with stigmatic papillae (data not shown). The jag-5D
mutant is different from other mutants with ectopic bracts like leafy
(lfy), unusual floral organs (ufo) or
filamentous flower (fil) in that jag-5D flowers are
fairly normal, although organ number is occasionally increased in the first
three whorls of flowers subtended by bracts
(Fig. 3A-C, and data not shown)
(Levin and Meyerowitz, 1995
;
Sawa et al., 1999
;
Schultz and Haughn, 1991
;
Weigel et al., 1992
;
Wilkinson and Haughn,
1995
).
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We also found ectopic blade tissue on the stems of coflorescences that arise in the axils of rosette leaves (Fig. 3J). This blade tissue appears to be continuous with that of the first leaves of the coflorescence. The development of blade tissue on rosette leaves and stems shows that jag-5D can activate ectopic growth of tissue and suggests that this activity of JAG may be the cause of ectopic bract development, as well.
Structure of the JAG gene
The JAG gene was initially identified starting with the
jag-5D mutant, which contains a single activation-tagging T-DNA
inserted downstream of the annotated gene, At1g68480. JAG encodes a
putative single zinc-finger of the C2H2 type, with high
sequence similarity (35% identity at amino acid level) to its closest
characterized Arabidopsis homolog, SUP
(Sakai et al., 1995). To
confirm the identity of the JAG gene, a genomic fragment including
the At1g68480 coding sequence and 35S enhancer sequences from the
activation-tagging T-DNA was transformed into wild-type plants
(Fig. 4A). 53 of 150 primary
transformants showed the jag-5D phenotype to various degrees,
including plants that had a stronger phenotype than the original
jag-5D mutant (Fig. 4B
and data not shown). We were also able to complement jag-1 mutants
with a similar genomic fragment that lacked the 35S enhancer sequences (data
not shown).
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Expression pattern of JAG
By RT-PCR, JAG RNA is detected during vegetative and reproductive
development in the shoot apex and open flowers, but not in roots, leaves or
inflorescence stems (Fig. 5A).
As expected, JAG mRNA levels are increased in jag-5D mutants
(Fig. 5B). JGL mRNA is
found in the same tissues where JAG RNA accumulates
(Fig. 5A). The overlap in RNA
accumulation along with the high degree of sequence similarity between
JAG and JGL suggests that the two genes are partially
redundant.
A more detailed picture of JAG gene activity was obtained by in situ localization of JAG mRNA. During the vegetative phase, JAG mRNA is detected in emerging leaf primordia, but is absent from the shoot apical meristem (Fig. 6A). JAG mRNA is localized in the distal region of leaves (Fig. 6A). Serial sections through leaf primordia revealed that JAG is predominantly expressed in the blade regions (Fig. 6B,C). No JAG expression was detected in the petioles (Fig. 6B). During the reproductive phase, JAG mRNA is excluded from the inflorescence and floral meristem, up to early stage 2 of floral development (Fig. 6E).
The accumulation of JAG mRNA in leaf primordia, but its absence
from flowers until mid-stage 2, contrasts with expression of FIL,
another lateral organ marker that is detected not only in emerging leaves, but
also in cells on the abaxial side of stage-2 floral primordia
(Fig. 4D) (Siegfried et al., 1999).
These cells, from which JAG mRNA is notably absent, constitute the
cryptic bract (Long and Barton,
2000
).
Like FIL, JAG mRNA is expressed in initiating sepal, petal, stamen and carpel primordia (Fig. 6E,F). Accumulation of JAG mRNA in sepals and stamens declines soon after stage 6, while expression in the distal region of the petal is maintained through stage 11 (Fig. 6H). This expression domain overlaps with the region of the petal that has the highest proportion of H4-positive cells (Fig. 2B). In the carpel, JAG mRNA initially accumulates throughout the valves during stages 7 and 8 (Fig. 6G). By stage 9, JAG mRNA accumulates primarily near the valve margins and gradually disappears by stage 12 (Fig. 6G). The JAG signal seems somewhat patchy in most tissues, with some cells apparently accumulating more JAG transcript than others.
That JAG is expressed in leaf primordia, but excluded from cryptic
bracts suggests that ectopic expression of JAG in the cryptic bract
of jag-5D mutants leads to ectopic bract development. Consistent with
this hypothesis, JAG RNA accumulates in the initiating bracts of
jag-5D heterozygotes (Fig.
6I), where it is maintained long after emergence of the bracts.
JAG RNA is also detected in the mutant in other tissues in which it
is normally not expressed, such as the inflorescence meristem and ovules
(Fig. 6I,J). Finally,
JAG mRNA also accumulates in the ectopic bracts that replace
first-whorl sepals in apetala1 (ap1) mutants
(Fig. 6K)
(Bowman et al., 1993;
Irish and Sussex, 1990
).
Requirement of JAG for bract development in ap1-15 mutants
The appearance of bracts in jag-5D mutants is of special interest,
since Arabidopsis normally does not produce such organs, although, as
mentioned above, ectopic bracts are produced in flowers of strong ap1
mutants. To determine whether JAG is not only sufficient, but also
necessary for bract formation, we introduced the jag-1
loss-of-function allele into the ap1-15 background. Most jag-1
ap1-15 flowers do not develop any organs in the first whorl
(Fig. 7A-D,
Table 2). Bracts are sometimes
replaced by rudimentary organs that are similar to those found in late-arising
ap1-15 flowers (data not shown). Scanning electron microscopy showed
that early bract development is similar in ap1-15 and jag-1
ap1-15 flowers (Fig.
7E,F). In ap1-15 flowers, medial bracts continue to grow,
while lateral bract primordia typically abort. In jag-1 ap1-15
flowers, both medial and lateral bracts abort soon after initiation.
Importantly, other aspects of the ap1-15 mutant phenotype are
unaffected by jag-1 (Fig.
7C,D, Table 2).
Thus, JAG is required for the outgrowth of bracts in ap1
mutants, but dispensable for their initiation. This is consistent with the
finding that cryptic bracts in wild-type plants also initiate independently of
JAG.
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To determine the identity of the structures that develop in the place of
flowers in strong AP1::JAG lines, we examined the expression of
FIL, which, in stage 3 flower primordia, marks discrete populations
of cells that develop into sepals
(Siegfried et al., 1999). In
strong AP1::JAG lines, FIL expression extends down the
length of the snake-like outgrowths, suggesting that these structures have at
least partial lateral organ identity (Fig.
8I,J).
In aggregate, the phenotypes caused by the AP1::JAG transgene suggest that JAG can override the arrest or delay in the growth of several tissues. In weak and intermediate lines, growth is activated between organs leading to fusion of sepals, petals and stamens. In intermediate lines, precocious growth of sepals leads to an elongated sepal tube. In the strongest lines, growth may be initiated before floral organs are properly established leading to the outgrowth of stumps that lack any discrete organ development.
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Discussion |
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The role of JAG in lateral organ development
The plant shoot apex is a dynamic structure in which a meristem maintains a
population of undifferentiated stem cells that later undergoes a process of
differentiation to form lateral organs. This process involves several steps,
beginning with the loss of meristem identity and the acquisition of lateral
organ identity, followed by organ outgrowth and morphogenesis, then cell-cycle
arrest and finally histogenesis. Progress through differentiation, however,
must be regulated so that organs can be properly shaped. If tissues exit the
cell cycle prematurely, morphogenesis is incomplete, whereas if cell-cycle
arrest does not occur, lateral organs would continue to grow ad infinitum.
In jag loss-of-function mutants, lateral organs do not develop
completely, with the strongest defects in the distal regions of organs. In
petals, we have shown that this is probably due to a reduction in cell-cycle
activity. In eudicots, lateral organs typically differentiate in a basipetal
fashion with cells at the tip exiting the cell cycle before those at the base
(Donnelly et al., 1999;
Nath et al., 2003
;
Poethig and Sussex, 1985
). We
propose that JAG slows the cessation of cell division in the distal
region of organs until proper morphogenesis has occurred, which is
particularly apparent in floral organs, since these form different structures
along the proximal-distal axis. JAG is also expressed in the blade
region of leaves, and jag loss-of-function mutants develop serrated
leaves. While we did not detect a change in total leaf area, the serrated
leaves may be caused by a reduction in growth in the inter-hydathode regions
of the blade. In this regard it is interesting to note that plants that
overexpress ICK1 or KRP2, negative regulators of the cell
cycle, also have jagged leaf blades (De
Veylder et al., 2001
; Wang et
al., 2000
). This interpretation is also consistent with
jag-5D gain-of-function phenotypes in which rosette leaves develop
ectopic blade tissue along the petiole. It is an intriguing concept that the
shape of organs and the architecture of shoots in plants may be, in part, the
result of controlled differentiation of tissues. Thus, the plant may be
sculpted by the opposing inputs from genes like CIN that promote
cell-cycle arrest, and genes like JAG that suppress cell-cycle
arrest.
One of the most dramatic consequences of JAG over-expression in AP1::JAG plants is the inhibition of floral organ boundaries and the precocious growth of sepals creating tube- and snake-like structures. These phenotypes suggest that increased JAG levels can override factors that inhibit the growth of specific organ regions. That JAG over-expression has such dramatic consequences even though JAG is normally expressed in young organs indicates that expression levels need to be finely tuned for proper function of JAG.
Bract development in Arabidopsis
One of the characteristic features of members of the Brassicaceae family is
that most flowers lack bracts, which is in stark contrast to the presence of
these organs in most eudicots. However, bracts are not completely absent in
Brassicaceae as basal flowers in many species are subtended by bracts
(Arber, 1931). Although bracts
are normally absent in Arabidopsis, they can develop in certain
backgrounds, such as lfy, ufo or fil mutants. Less
pronounced activation of cryptic bracts is seen when flowers are ablated
through expression of a toxin (Nilsson et
al., 1998
). Even in wild-type plants, molecular markers indicate
the presence of a cryptic bract whose outgrowth is normally suppressed
(Long and Barton, 2000
). Thus,
while the bract appears to be dispensable for the final architecture of the
Arabidopsis inflorescence, the bract is still patterned.
In Arabidopsis, several genes, FIL, AINTEGUMENTA, ASYMMETRIC
LEAVES1 and STYLISH1, are expressed in incipient lateral organs
(Byrne et al., 2000;
Kuusk et al., 2002
;
Siegfried et al., 1999
). At
least some of these genes are required for the development of lateral organs,
but none is sufficient to activate bract development, even though they are
expressed in the cryptic bract. Thus, their activity is either specifically
suppressed in the cryptic bract, or bract outgrowth requires another factor.
The latter scenario is supported by the finding that JAG is absent
from the cryptic bract, but can activate its outgrowth when ectopically
expressed in jag-5D mutants. That this function does not merely
represent a neomorphic activity is demonstrated by our observation that
JAG is required for outgrowth of ectopic bracts that form in
ap1-15. It is particularly interesting that loss of JAG
function in an ap1-15 background primarily affects bracts, even
though it is also expressed in other organs. This may indicate that
JAG is more important for the growth of bracts, and that redundancy
with a gene such as JGL may mask essential functions in other organs.
Alternatively, ap1 bracts may be particularly sensitive to defects in
organogenesis. This could be the case if ap1 bracts are under similar
suppressive influences as bracts of the main inflorescences. In this case,
loss of JAG would sensitize the bract to suppression of outgrowth.
This interpretation is further supported by the observation that
loss-of-function in another gene important for lateral organ development,
AINTEGUMENTA, also has a negative effect on bract development in
ap1 mutants (B. Krizek, personal communication).
Since our data suggest that JAG is both necessary and sufficient
for bract formation, and since JAG expression is normally excluded
from the cryptic bract, one can speculate that bract-specific suppression of
JAG expression is the cause of bractless flowers in the Brassicaceae.
As there are also other examples of bract suppression in plants outside of
Brassicaceae, such as in the maize inflorescence
(Ritter et al., 2002), it will
be interesting to determine the possible role that JAG plays in the
evolution of this intriguing plant characteristic in other species, as
well.
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ACKNOWLEDGMENTS |
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Footnotes |
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