1 Division of Biological Sciences, University of California San Diego, La Jolla,
CA 92093, USA
2 Plant Biology Laboratory, The Salk Institute for Biological Studies, La Jolla,
CA 92037, USA
3 Department of Molecular Biology, Max Planck Institute for Developmental
Biology, 72076 Tübingen, Germany
* Author for correspondence (e-mail: marty{at}biomail.ucsd.edu)
Accepted 25 August 2005
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SUMMARY |
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Key words: Arabidopsis thaliana, Development, Fruit, Patterning, Polarity, Dehiscence
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Introduction |
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The development of the fruit in the model plant, Arabidopsis,
provides an excellent system for dissecting the mechanisms that pattern an
organ in plants because of the presence of distinctive morphological landmarks
and the availability of reporter lines that mark specialized tissues
(Dinneny and Yanofsky, 2005).
The region of the fruit that encloses the seeds (ovary) is divided into three
tissue zones: valve, replum and valve margin
(Fig. 1A-D). The valves, or
seed pod walls, protect the seeds during their development and detach after
maturation to promote seed dispersal in a process known as dehiscence. The two
valves are separated by a central ridge of replum tissue. At the valve/replum
junction, a specialized stripe of tissue, termed the valve margin, forms that
facilitates the detachment of the valves from the replum through the action of
two different cell types. On the replum side of the valve margin, the
separation layer forms, which permits the detachment of the valve from the
replum through cell-cell separation (Fig.
1E) (Jenkins, 1999; Peterson, 1996). On the valve side of the
margin, a layer of rigid lignified cells forms
(Fig. 1E,F). The lignified
layer of the valve margin is continuous with an adjacent layer of lignified
cells present in the valves, termed the endocarp layer b
(enb) (Fig. 1E-G).
Together, these tissues are thought to provide spring-like tension that
mechanically drives valve detachment (Spence, 1996).
Recent work has identified several genetic components that are important
for specifying valve margin development and defining its borders
(Fig. 7). The redundant
MADS-box genes, SHATTERPROOF 1/2 (SHP), are at the top of a
cascade of transcription factor genes that specify valve margin identity
(Liljegren et al., 2000). When
SHP activity is eliminated, fruits are indehiscent and lack lignified
layer and separation layer development. Acting both downstream and in parallel
to SHP, the INDEHISCENT (IND) and ALCATRAZ
(ALC) basic helix-loop-helix-type transcription factor genes also
specify valve margin identity with IND playing important roles in
lignified and separation layer development, and ALC regulating
separation layer development (Liljegren et
al., 2004
; Rajani and
Sundaresan, 2001
).
The expression of the valve margin identity genes is limited to the valve
margin through negative regulation by FRUITFULL (FUL) in the
valves and REPLUMLESS (RPL) in the replum. FUL
encodes a MADS-domain transcription factor that is expressed in the valves
(Gu et al., 1998). When
FUL is mutated, the valve margin identity genes become ectopically
expressed in the valves, imparting valve margin-like development, including
the ectopic formation of lignified and separation layer-like cell types
(Ferrándiz et al.,
2000b
). Similar to the role that FUL plays, RPL
negatively regulates the expression of the valve margin identity genes in the
replum (Roeder et al., 2003
).
RPL encodes a BELL-family homeodomain transcription factor and is
expressed in the replum. When RPL is mutated, ectopic SHP
expression in the replum causes the valve margins to coalesce into a single
stripe of tissue in place of the replum, rendering rpl fruit
partially indehiscent. SHP expression is positively regulated by
AGAMOUS (AG), a MADS-domain transcription factor gene that
controls carpel identity (Savidge et al.,
1995
). However, AG probably acts redundantly with other
factors, since SHP activity is still present in ag apetala2
mutants (Lee et al., 2005
;
Pinyopich et al., 2003
).
|
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Materials and methods |
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Genotyping
Genotyping of jag-1 has been previously described
(Dinneny et al., 2004). To
genotype fil-8 we used primers oJD174 and oJD175 to detect the
wild-type FIL allele and oJD175 and oJD176 to detect the
fil-8 allele. To genotype yab3-2, we used primers oJD172 and
oJD173 to detect the wild-type YAB3 allele and oJD173 and oJD177 to
detect the yab3-2 allele. Genotyping of ful-1
(Gu et al., 1998
) and
rpl-3 (Roeder et al.,
2003
) has already been described. The
jag-5D+/ shp1,2 triple mutant was
identified phenotypically.
The sequences of the oligonucleotide primers used were as follows:
In situ hybridization, microscopy and histology
In situ hybridization was performed as previously described
(Dinneny et al., 2004). Tissue
was prepared for scanning electron microscopy (SEM) as previously described
(Dinneny et al., 2004
). Late
stage 17 fruit were fixed, sectioned (8 µm) and stained using
Phloroglucinol (Liljegren et al.,
2000
) or Saffranin O and Alcian Blue
(Roeder et al., 2003
) as
previously described.
GUS staining
To monitor FUL expression, the ful-1 enhancer trap line
was crossed to fil-8 yab3-2 or jag-1 fil-8
yab3-2+/ mutants. F2 segregants were
genotyped for jag-1, fil-8, yab3-2 and ful-1 alleles and
stained for GUS activity if plants were heterozygous for ful-1. The
yab3-2 allele is also a GUS enhancer trap line, however, no
overlapping GUS staining was detected with that of ful-1 in fil
yab3 and jag fil yab3 mutant backgrounds during the stages of
development described (data not shown). To monitor SHP2 expression,
the SHP2::GUS reporter line was crossed to fil-8 yab3-2, jag-1
fil-8 yab3-2 and jag-5D mutant backgrounds. F2
segregants were genotyped for jag-1, fil-8, yab3-2 alleles and
stained for GUS activity. Plants heterozygous for jag-5D were
identified phenotypically. To monitor AG expression, the KB9
reporter line was crossed to fil-8 yab3-2 mutants
(Busch et al., 1999). GUS
staining was performed as previously described
(Blázquez et al.,
1997
).
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Results |
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The loss of valve margin development in fil yab3 fruit suggests that FIL and YAB3 have important roles in controlling the expression of the valve margin identity genes. To determine this relationship, we examined the activity of a SHP2::GUS reporter. Consistent with the loss of valve margin development in the apical region, reporter activity was absent from the valve margins of fil yab3 mutants but was unaffected in regions where FIL and YAB3 are not expressed (Fig. 3A-D). Thus, FIL and YAB3 play important roles in promoting valve margin development, in part by promoting SHP expression at the valve margin.
The basal region of fil yab3 fruit develops ectopic valve margin tissue
Paradoxically, fil yab3 mutants develop ectopic valve
margin-associated cell types in the basal region of the fruit. By SEM, ectopic
valve margin can be seen as patches, or stripes, of small cells
(Fig. 2B,F). In cross section
these patches stain similarly to cells of the separation and lignified layers
(Fig. 2G,H and Fig. S1E in
supplementary material). Ectopic valve margin in fil yab3 mutants can
develop both as an expansion of the valve margin normally present on either
side of replum and in stripes in the middle of the valves
(Fig. 2F,G,H and Fig. S1E in
supplementary material).
The development of the ectopic valve margin suggests that SHP expression might have expanded into the valves at the base of fil yab3 fruit. We examined SHP2::GUS activity in fil yab3 mutants and found that, in contrast to the apical region, reporter activity in the basal region was increased in the valves (Fig. 3A-E). The stark contrast in reporter activity between the apical and basal regions of fil yab3 fruit is most dramatic in whole mounts (Fig. 3A,B).
|
FIL and YAB3 are required for the maintenance of SHP expression at the valve margin and the activation of FUL expression in the valves
We examined the expression of SHP2 and FUL during early
stages of gynoecium development when FIL and YAB3 are most
strongly expressed. In wild type, the SHP2::GUS reporter is initially
expressed in a broad domain during early gynoecium development in cells that
will develop into the replum, septum and valve margins (Fig. S3 in
supplementary material). Expression in the replum eventually fades, leaving
SHP2 expression at the valve margins and septum. In fil yab3
mutants, SHP2::GUS expression initiates as in wild type, however,
expression is quickly lost in the replum and presumptive valve margins (Fig.
S2 supplementary material).
FUL expression, in wild-type gynoecia, initiates in the adaxial cell layers of the valves, and then expands into all cell layers by stage 10. In fil yab3 mutants, however, expression is never detected in the valves. These data show that FIL and YAB3 are required for expression of SHP2 and FUL during early gynoecium development in addition to later stages in the fruit. The observation that SHP2 and FUL expression is affected in tissues where FIL and YAB3 are not expressed (i.e. replum for SHP2 and adaxial epidermis for FUL) suggests that they can act cell non-autonomously.
The loss of enb lignification suggests that FIL and YAB3 also regulate other valve margin identity genes
In fil yab3 mutants, enb lignification is reduced in the
apical region of the fruit (Fig.
1F,G and Fig.
2D,E). The development of the enb layer is redundantly
specified by both FUL and the valve margin identity genes
(Liljegren et al., 2004).
Expression of at least one of these factors is sufficient for enb
lignification: consistent with this scenario, a 35S::FUL transgene
restored enb lignification in the apical region of fil yab3
mutants (Fig. 2D,E and
Fig. 3J,L). Since a complete
loss of enb lignification is otherwise only observed in the ful
shp1 shp2 ind alc quintuple mutant, we conclude that besides FUL
and SHP, the activity of IND and ALC is also
compromised in fil yab3 mutants. To test this possibility further, we
examined the effect that loss of FIL and YAB3 function had
on the ectopic valve margin development seen in ful mutants
(Fig. 3M). The apical phenotype
of ful fil yab3 fruit is very similar to fil yab3 double
mutants, with a clear absence of valve margin development and enb
layer lignification, indicating that the fil yab3 mutations are
epistatic to ful (Fig.
2E and Fig. 3M,N)
and necessary for the activity of the genes that confer ectopic valve margin
identity to ful valves. Importantly, the base of ful fil
yab3 fruit still develop ectopic valve margin, however, the ectopic
tissue appears to be composed only of cells with separation layer-like
characteristics (not shown).
JAG acts redundantly with FIL and YAB3 to regulate valve margin development
Our data show that FIL and YAB3 promote the expression of
both SHP and FUL. However, while FIL and
YAB3 are essential for FUL expression in the valves,
SHP expression is only partially affected. One possible reason for
this incomplete effect may be genetic redundancy of FIL and
YAB3 with another factor that also promotes SHP expression.
We have tested whether FIL and YAB3 act redundantly with
other non-YABBY family members and in other work have found that
FIL and YAB3 function redundantly with an unrelated
C2H2 zinc-finger transcription factor gene,
JAG, to promote leaf blade growth (Fig. S3A,B in the supplementary
material). To determine if this redundancy extends into the fruit we examined
the effect of various combinations of fil, yab3 and jag
mutations.
|
The combination of jag with fil results in the apparent expansion of the basal gynophore and apical style tissues into the ovary region (Fig. 4C). Furthermore, jag fil mutants develop a stripe of ectopic tissue that runs through the center of the valves (Fig. 4D). The cells in this region are narrow and can occasionally be seen separating from each other. Examination of cross sections of this stripe shows that it is composed of cells with separation and lignified layer characteristics, indicating that jag fil mutants develop an ectopic stripe of valve margin in the middle of the valves (Fig. 4E). Interestingly, this stripe of valve margin always develops overlying the main vascular bundle of the valves. The ectopic development of valve margin tissues also correlated with the expansion of SHP2::GUS activity into the valves of jag fil double mutants (Fig. 5F,J). Some ectopic reporter activity can be seen in the valves of jag and fil single mutants as well (Fig. 5F,G,H).
|
The effect of the yab3 mutation was next examined in the context of the jag and fil mutations. Loss of a single copy of YAB3 resulted in a strong increase in the expansion of gynophore and style regions into the ovary of jag fil yab3+/ fruit (Fig. 4F). The increase in the size of the style was particularly apparent when the fruits were not mutant for ERECTA (Fig. 4G). The fruit of jag fil yab3+/ also developed a dramatic expansion of valve margin tissues, with large patches forming in and around the valves (Fig. 4I). The replum of jag fil yab3+/ fruit was also greatly expanded and twisted along the length of the fruit (Fig. 4H). These phenotypes are reminiscent of those observed in ful mutant fruit, which develop enlarged and twisted repla (Fig. 4J) along with ectopic valve margin tissue in the valves (Fig. 4K), although to a greater extent than jag fil yab3+/. Consistent with these phenotypes, the expression of the SHP2::GUS reporter further expands into the valve regions in jag fil yab3+/ fruit (Fig. 5K,L), with FUL expression diminishing to small islands (Fig. 5A,B). Together, these data indicate that JAG acts redundantly with FIL and YAB3 to promote FUL expression in the valves. Importantly, fil yab3+/ mutants, which can develop stripes of ectopic valve margin in the valves, do not develop ectopic valve margin or ectopic SHP2::GUS activity to the extent of jag fil yab3+/ mutant fruit (Fig. 5I and data not shown).
Surprisingly, the loss of the second copy of YAB3 in jag fil yab3 triple mutants reverses the expansion of valve margin development seen in jag fil and jag fil yab+/ mutants. Fruits of jag fil yab3 mutants do not develop valve margin-like cell types in either the apical or basal portions (Fig. 4M-P and data not shown). In the valve regions, the epidermis is composed of elongated cells with interspersed stomata, similar to wild-type valve cells (Fig. 4N). Some valve cells have an irregular shape. The expression of FUL is completely absent from the valve regions of jag fil yab3 mutant gynoecia (Fig. 5C,D), similar to fil yab3 mutants. Contrary to what was observed in jag fil yab3+/ fruit, however, SHP2::GUS activity is strongly reduced in both the valves and valve margins (Fig. 5M,N). A low level of SHP2 expression occurs only in the vicinity of the vascular bundles (Fig. 5M,N). These data indicate that JAG not only acts redundantly with FIL and YAB3 to promote FUL expression, but also to promote SHP expression. Furthermore, the strong reduction of SHP expression in jag fil yab3 mutants demonstrates that genetic redundancy with JAG is a cause of the remaining SHP expression seen in fil yab3 mutants. The other floral organs of jag fil yab3 mutants are also severely affected and develop little, if any floral characteristics, suggesting that JAG, FIL and YAB3 promote the patterning of other floral organs as well (Fig. 4L).
|
The ectopic development of valve margin tissues in jag-5D mutants suggested that the presence of JAG activity in the replum might be able to promote the expansion of SHP expression into this region. We therefore examined SHP2::GUS activity in jag-5D mutants, and found that reporter activity had expanded into the replum (Fig. 3C and Fig. 6C). To test whether expanded SHP expression was the cause of the ectopic valve margin development, we removed SHP activity by constructing a jag-5D shp1 shp2 triple mutant and found that replum development was rescued (Fig. 6A,B,D,E). Thus, JAG is sufficient to drive the ectopic expression of SHP in the replum, converting this region into valve margin.
RPL promotes the formation of two stripes of valve margin by repressing JAG/FIL activity in the replum
The conversion of the replum into valve margin in jag-5D is very
similar to the effect that the rpl mutation has on replum development
(Fig. 6F)
(Roeder et al., 2003). As in
jag-5D, rpl mutants develop ectopic separation and lignified layer
tissues in the replum, which is caused by the expansion of SHP
expression into the replum. Likewise, loss of SHP function in a
rpl mutant background rescues replum development. These similarities
suggest the basis of the rpl mutant phenotype may be ectopic
JAG expression in the replum. To test this, we examined JAG
expression in rpl mutants by in situ hybridization, however, we could
not detect JAG transcript in the replum
(Fig. 6G). Nevertheless, we
examined the effect of removing JAG activity from a rpl
mutant background by constructing jag rpl double mutants and found
that replum development was partially rescued
(Fig. 6F,H,I). The rescue of
replum development is somewhat variable, however (data not shown). Thus, while
expression of JAG can not be detected in the replum of rpl
mutants, genetic evidence suggests some JAG activity may be
present.
|
We also examined the expression of FIL in jag-5D mutants to see if the replumless phenotype could be caused by ectopic FIL expression in the replum. No effect on FIL expression was apparent in jag-5D gynoecia, however, indicating that JAG is not sufficient to activate FIL expression in these tissues (Fig. S5B in supplementary material). Together, our data suggest that the effect of RPL on SHP is indirect, and mediated by repression of FIL and JAG, two activators of SHP expression. This hypothesis is consistent with in situ hybridization experiments that show RPL expression in the replum during the same stages that FIL expression expands into the replum region of rpl mutants. Our data, however, do not exclude the possibility that RPL may repress SHP expression through a parallel pathway as well.
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Discussion |
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The relationship between organ polarity and fruit patterning
Plant organogenesis is regulated by a genetic system that divides organs
into abaxial and adaxial halves. Members of a miRNA-regulated clade of HD-ZIP
family transcription factors, including PHABULOSA, PHAVOLUTA and
REVOLUTA, control the identity of the adaxial domain, the half of the
organ that is proximal to the shoot meristem
(Emery et al., 2003;
McConnell and Barton, 1998
;
McConnell et al., 2001
). On
the other side, the GARP-type transcription factor genes, KANADI 1
and 2 control the identity of the abaxial domain
(Eshed et al., 1999
;
Eshed et al., 2001
;
Eshed et al., 2004
;
Kerstetter et al., 2001
). Not
only do these factors impose adaxial or abaxial development on their
respective sides, but they also restrict the spread of the opposing identity.
FIL and YAB3 also function with KAN genes to
control abaxial identity, however, they do not appear to be involved in the
initial establishment of organ polarity. Instead it has been proposed that
FIL and YAB3 function downstream of KAN to
facilitate abaxial identity and to promote the growth of the leaf blade
(Eshed et al., 2004
). Thus,
FIL and YAB3 may function downstream of polarity
establishment to begin carrying out an abaxial-specific developmental
program.
Although it is known that the establishment of organ polarity controls the distribution of cell types in an organ, it is not yet known what the functional relationship is between the specification of adaxial/abaxial identity and the development of specialized cell types that constitute these regions. By showing that FIL and YAB3 promote the expression of the FUL and SHP genes, our work provides the first functional link between the establishment of organ polarity and the regulation of genes that control tissue identity. Because the FIL and YAB3 genes are expressed in all lateral organs, it is likely that they control tissue identity in the fruit by interacting with other factors, such as those encoded by the floral homeotic genes. Thus, FIL and YAB3 would provide positional information that is common to all organs, with the floral homeotic genes contributing identity information specific to individual organs. Importantly, we have found that the expression of the floral homeotic gene, AG, which regulates the identity of the carpels, is unaffected in fil yab3 mutants (Fig. S6 in supplementary material). This indicates that FIL/YAB and AG represent independent pathways regulating FUL and SHP expression.
The fil yab3 double mutants and jag fil yab3 triple
mutants also have defects in patterning all other floral organs
(Siegfried et al., 1999). The
defects seen in these other organs do not resemble the patterning defects of
mutants, such as phb-1D or kan1 kan2, that have been
classified as having ectopic adaxial development
(Eshed et al., 2001
;
McConnell and Barton, 1998
).
It will be interesting to examine these floral organs more carefully to
determine the exact nature of the patterning defects and to see if specific
floral organ cell types are missing, as they are in the fruit.
Activation of FUL in the valves and SHP in the valve margin
While FIL, YAB3 and JAG are expressed in both the valves
and presumptive valve margin, FUL and SHP are expressed in
mutually exclusive domains in these tissues. How is it then that FIL,
YAB3 and JAG pattern the expression of both sets of genes? Our
loss-of-function genetic results show that FUL expression is most
severely affected by reductions in FIL/YAB3/JAG activity whereas
SHP expression is more robust. For example, FUL expression
is strongly affected in fil yab3 mutants, whereas SHP
expression is lost in only part of the fruit. These data suggest that the
activation of FUL and SHP expression may require different
levels of FIL, YAB3 and JAG activity. In this light, it is
intriguing that SHP is expressed at the periphery of the
FIL/YAB3/JAG expression domain where FIL/YAB3/JAG activity
may be weakest; possibly pointing to their proteins having properties of a
morphogen that controls different downstream targets in a
concentration-dependent manner. It will be necessary to develop tools to
quantitatively detect FIL, YAB3 and JAG proteins, in order to enable a close
comparison of their distribution with FUL and SHP expression
during fruit development.
Mechanistic insight into the role of RPL in fruit development
We have gained further insight into how fruit patterning is established by
showing that JAG/FIL activity is negatively regulated by RPL
in the replum. In rpl mutants, the two valve margins coalesce into a
single stripe of tissue with valve margin characteristics. This expanded valve
margin development correlates with the presence of ectopic FIL
expression in these medial tissues. Removal of either JAG or
FIL activity from a rpl mutant rescues replum development,
demonstrating that ectopic JAG/FIL activity in the replum is the
cause of the rpl phenotype. Thus, RPL effectively divides
JAG/FIL activity into two domains, creating two separate valve
margins that enable each valve to separate independently from the fruit.
The spatial regulation of JAG/FIL activity in the fruit identifies
an interesting parallel to lateral organ and meristem patterning at the shoot
apex. In the shoot, antagonism between the meristem and lateral organ
primordia ensures that the meristem is not consumed during the process of
organogenesis and prevents organ primordia from fusing together. In the fruit,
RPL [a.k.a. BELLRINGER
(Byrne et al., 2003),
PENNYWISE (Smith and Hake,
2003
) and VAAMANA
(Bhatt et al., 2004
)]
determines the limits of valve margin development by inhibiting
JAG/FIL activity. BELLRINGER also plays important roles in
meristem development and acts redundantly with SHOOTMERISTEMLESS to
prevent the fusion of the cotyledons (seed leaves) at their base
(Byrne et al., 2003
). Thus, the
mechanism that prevents the margins of the valves from fusing may be derived
from the process by which organ fusion is suppressed in the seedling shoot. It
will therefore be interesting to determine whether ectopic FIL or
JAG activity is responsible for any of the shoot defects seen in
rpl mutants.
Fruits as modified leaves
In 1790, Goethe proposed that floral organs represented modified vegetative
leaves. It would take nearly 200 years for plant biologists to develop the
technologies to test this intriguing hypothesis. The formation of the ABC
model of floral organ development led to an understanding of the molecular
basis of floral organ identity (Coen and
Meyerowitz, 1991). These discoveries demonstrated that the
expression of a handful of genes was responsible for transforming simple
leaves arising on flowers into sepals, petals, stamens and carpels. These
principles came full circle when it was shown that the constitutive expression
of floral homeotic genes and their co-factors could convert vegetative leaves
outside of flowers into individual floral organs
(Honma and Goto, 2001
;
Pelaz et al., 2001
). The
observation that these ectopic floral organs formed all of the appropriate
tissue types in the correct spatial arrangement, despite the constitutive
expression of the homeotic genes, suggests that these genes do not directly
control the arrangement of tissues. Furthermore, since leaves can be converted
into floral organs, and vice versa, the positional information that controls
the arrangement of tissues must be the same for every organ. Our work showing
that FIL, YAB3 and JAG, which are expressed in all organs,
are important for the development of fruit-specific tissues and for the
development of all floral organs, suggests that they are important for this
positional information. Thus, not only do floral organs share a common
ancestry with leaves, but the mechanisms that pattern the arrangement of
tissues are also common. It will be interesting to determine how the
FIL/YAB3 and JAG pathways were co-opted to pattern the wide
array of organ types found in plants.
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ACKNOWLEDGMENTS |
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![]() |
Footnotes |
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Supplementary material for this article is available at http://dev.biologists.org/cgi/content/full/132/21/4687/DC1
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REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bhatt, A. M., Etchells, J. P., Canales, C., Lagodienko, A. and Dickinson, H. (2004). VAAMANA a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene 328,103 -111.[CrossRef][Medline]
Blázquez, M. A., Soowal, L. N., Lee, I. and Weigel,
D. (1997). LEAFY expression and flower initiation in
Arabidopsis. Development
124,3835
-3844.
Busch, M. A., Bomblies, K. and Weigel, D.
(1999). Activation of a floral homeotic gene in Arabidopsis.Science 285,585
-587.
Byrne, M. E., Groover, A. T., Fontana, J. R. and Martienssen, R.
A. (2003). Phyllotactic pattern and stem cell fate are
determined by the Arabidopsis homeobox gene BELLRINGER.Development 130,3941
-3950.
Coen, E. S. and Meyerowitz, E. M. (1991). The war of the whorls: genetic interactions controlling flower development. Nature 353,31 -37.[CrossRef][Medline]
Dinneny, J. R. and Yanofsky, M. F. (2005). Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned. BioEssays 27,42 -49.[CrossRef][Medline]
Dinneny, J. R., Yadegari, R., Fischer, R. L., Yanofsky, M. F.
and Weigel, D. (2004). The role of JAGGED in
shaping lateral organs. Development
131,1101
-1110.
Emery, J. F., Floyd, S. K., Alvarez, J., Eshed, Y., Hawker, N. P., Izhaki, A., Baum, S. F. and Bowman, J. L. (2003). Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13,1768 -1774.[CrossRef][Medline]
Engstrom, E. M., Izhaki, A. and Bowman, J. L.
(2004). Promoter bashing, microRNAs, and Knox genes. New
insights, regulators, and targets-of-regulation in the establishment of
lateral organ polarity in Arabidopsis. Plant Physiol.
135,685
-694.
Eshed, Y., Baum, S. F. and Bowman, J. L. (1999). Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99,199 -209.[CrossRef][Medline]
Eshed, Y., Baum, S. F., Perea, J. V. and Bowman, J. L. (2001). Establishment of polarity in lateral organs of plants. Curr. Biol. 11,1251 -1260.[CrossRef][Medline]
Eshed, Y., Izhaki, A., Baum, S. F., Floyd, S. K. and Bowman, J.
L. (2004). Asymmetric leaf development and blade expansion in
Arabidopsis are mediated by KANADI and YABBY
activities. Development
131,2997
-3006.
Ferrándiz, C., Gu, Q., Martienssen, R. and Yanofsky, M.
F. (2000a). Redundant regulation of meristem identity and
plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER.Development 127,725
-734.
Ferrándiz, C., Liljegren, S. J. and Yanofsky, M. F.
(2000b). Negative regulation of the SHATTERPROOF genes
by FRUITFULL during Arabidopsis fruit development.
Science 289,436
-438.
Gu, Q., Ferrandiz, C., Yanofsky, M. F. and Martienssen, R.
(1998). The FRUITFULL MADS-box gene mediates cell
differentiation during Arabidopsis fruit development.
Development 125,1509
-1517.
Honma, T. and Goto, K. (2001). Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409,525 -529.[CrossRef][Medline]
Jenkins, E. S., Paul, W., Craze, M., Whitelaw, C. A., Weigand, A. and Roberts, J. A. (1999). Dehiscence-related expression of an Arabidopsis thaliana gene encoding a polygalacturonase in transgenic plants of Brassica napus. Plant Cell Env. 22,159 -167.[CrossRef]
Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. and Poethig, R. S. (2001). KANADI regulates organ polarity in Arabidopsis. Nature 411,706 -709.[CrossRef][Medline]
Kumaran, M. K., Bowman, J. L. and Sundaresan, V.
(2002). YABBY polarity genes mediate the repression of
KNOX homeobox genes in Arabidopsis. Plant
Cell 14,2761
-2770.
Lee, J. Y., Baum, S. F., Alvarez, J., Patel, A., Chitwood, D. H.
and Bowman, J. L. (2005). Activation of CRABS
CLAW in the nectaries and carpels of Arabidopsis. Plant
Cell 17,25
-36.
Liljegren, S. J., Ditta, G. S., Eshed, Y., Savidge, B., Bowman, J. L. and Yanofsky, M. F. (2000). SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404,766 -770.[CrossRef][Medline]
Liljegren, S. J., Roeder, A. H., Kempin, S. A., Gremski, K., Ostergaard, L., Guimil, S., Reyes, D. K. and Yanofsky, M. F. (2004). Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116,843 -853.[CrossRef][Medline]
Logan, M. (2003). Finger or toe: the molecular
basis of limb identity. Development
130,6401
-6410.
McConnell, J. R. and Barton, M. K. (1998). Leaf
polarity and meristem formation in Arabidopsis.Development 125,2935
-2942.
McConnell, J. R., Emery, J., Eshed, Y., Bao, N., Bowman, J. and Barton, M. K. (2001). Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411,709 -713.[CrossRef][Medline]
Ohno, C. K., Reddy, G. V., Heisler, M. G. and Meyerowitz, E.
M. (2004). The Arabidopsis JAGGED gene encodes a
zinc finger protein that promotes leaf tissue development.
Development 131,1111
-1122.
Pelaz, S., Tapia-Lopez, R., Alvarez-Buylla, E. R. and Yanofsky, M. F. (2001). Conversion of leaves into petals in Arabidopsis. Curr. Biol. 11,182 -184.[CrossRef][Medline]
Peterson, M., Sander, L., Child, R., Van Onckelen, H., Ulvskov, P. and Borkhardt, B. (1996). Isolation and characterization of a pod dehiscence zone-specific polygalacturonase from Brassica napus. Plant Mol. Biol. 31,517 -527.[CrossRef][Medline]
Pinyopich, A., Ditta, G. S., Savidge, B., Liljegren, S. J., Baumann, E., Wisman, E. and Yanofsky, M. F. (2003). Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424,85 -88.[CrossRef][Medline]
Rajani, S. and Sundaresan, V. (2001). The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr. Biol. 11,1914 -1922.[CrossRef][Medline]
Roeder, A. H., Ferrándiz, C. and Yanofsky, M. F. (2003). The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr. Biol. 13,1630 -1635.[CrossRef][Medline]
Savidge, B., Rounsley, S. D. and Yanofsky, M. F.
(1995). Temporal relationship between the transcription of two
Arabidopsis MADS box genes and the floral organ identity genes.
Plant Cell 7,721
-733.
Sawa, S., Watanabe, K., Goto, K., Liu, Y. G., Shibata, D.,
Kanaya, E., Morita, E. H. and Okada, K. (1999).
FILAMENTOUS FLOWER, a meristem and organ identity gene of
Arabidopsis, encodes a protein with a zinc finger and HMG-related
domains. Genes Dev. 13,1079
-1088.
Siegfried, K. R., Eshed, Y., Baum, S. F., Otsuga, D., Drews, G.
N. and Bowman, J. L. (1999). Members of the
YABBY gene family specify abaxial cell fate in Arabidopsis.Development 126,4117
-4128.
Smith, H. M. S. and Hake, S. (2003). The
interaction of two homeobox genes, BREVIPEDICELLUS and
PENNYWISE, regulates internode patterning in the Arabidopsis
inflorescence. Plant Cell
15,1717
-1727.
Spence, J., Vercher, Y., Gates, P. and Harris, N. (1996). `Pod shatter' in Arabidopsis thaliana, Brassica napus and B. juncea. J. Microsc. 181,195 -203.
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