Department of Plant and Microbial Biology, 111 Koshland Hall, University of California, Berkeley, CA 94720-3102, USA
E-mail: jpfluger{at}nature.berkeley.edu; zambrysk{at}nature.berkeley.edu
Accepted 14 June 2004
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SUMMARY |
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Key words: Seuss, Auxin, Ettin, Flower, Pinoid
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Introduction |
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The Arabidopsis flower is particularly well suited to study the
effects of auxin on plant development because the flower arises in a very
stereotypical pattern, resulting in four types of organs that are
morphologically distinguishable from one another. Each organ type develops in
a concentric whorl: four evenly spaced sepals envelop and protect the
developing internal organs; four petals arise just inside the sepal margins;
six stamens are patterned as two lateral and two pairs of medial organs; and
two fused carpels collectively comprise the central gynoecium. The conceptual
framework for flower development has been the elegantly simple ABC model, in
which three classes of genes are expressed in concentric overlapping domains
that combinatorially specify organ identity in each of the four floral whorls
(Bowman et al., 1991). Although
identification of genes involved in meristem function and organ identity has
increased exponentially (Carles and
Fletcher, 2003
; Franks and
Liu, 2001
), relatively little is known about how organs are
patterned both within and between whorls. Transcription factors such as
SUPERMAN and CUP-SHAPED COTYLEDON2 function in whorl and/or organ partitioning
(Aida et al., 1997
;
Sakai et al., 1995
), while
UNUSUAL FLORAL ORGANS and PERIANTHIA affect initiation and spacing of floral
organs (Levin and Meyerowitz,
1995
; Running and Meyerowitz,
1996
). Yet how floral organs are initiated in such specific
positions and in such a reproducible pattern is still not well understood.
The ettin (ett) mutant has pleiotropic effects on flower
development, including increases in perianth organ number and aberrations in
regional differentiation of reproductive organs. In ett, development
of the gynoecium has been the best characterized. The gynoecium in the
Brassicaceae, including Arabidopsis, develops from two
congenitally fused carpels that arise from the center of the floral meristem.
The two outer ovary walls, or valves, are separated from each other by a
longitudinal furrow, or replum. In ett, the organization of apical
style and stigma, central ovary and basal internode (termed stipe), is
disrupted. Strong alleles of ett are characterized by a shift in
boundaries between these tissues, including a reduction in valve length, an
increase in basal stipe, and an overproliferation of apical stigma and style
(Sessions and Zambryski,
1995). There is also a concomitant eversion or abaxialization of
internal tissues, the severity of which increases towards the gynoecium apex.
The reduction in the proportion of ovary in ett is reminiscent of the
phenotypes of the auxin regulatory mutants pinoid (pid) and
monopteros (mp), and therefore similarly may be due to a
disruption in auxin signaling (Bennett et
al., 1995
; Przemeck et al.,
1996
). In fact, transient application of naphthylphthalamic acid
(NPA), a polar auxin transport inhibitor, to the inflorescence apex of
wild-type plants results in a reduction of ovary relative to apical style and
basal stipe, effectively phenocopying ett and weak alleles of
pid. Because NPA presumably causes auxin to pool at its sites of
synthesis instead of being transported in a normal polar fashion, it has been
hypothesized that ETT responds to a gradient of auxin to establish ovary
boundaries within the gynoecium (Nemhauser
et al., 2000
).
ETT is a member of the auxin response factor (ARF) family of transcription
factors (Sessions et al.,
1997). This family is central to auxin response, as almost
immediately after auxin entry into a cell, ARFs activate transcription of
early auxin response genes (Ulmasov et
al., 1999a
). The ARF family is difficult to study genetically,
owing to a high level of sequence homology and probable functional redundancy.
Only three out of 22 ARFs from Arabidopsis have demonstrated
loss-of-function phenotypes (Guilfoyle and
Hagen, 2001
). ETT is unique among ARFs because it lacks two
C-terminal domains responsible for heterodimerization with Aux/IAAs, a family
of transcriptional repressor proteins. Instead, ETT has a unique C-terminal
half, containing a region rich in serine residues. Thus, the prevailing model
for auxin action in which Aux/IAA repressors are rapidly targeted for
degradation when auxin is present, liberating ARFs to activate transcription
of target genes cannot hold for ETT. Yet ETT is clearly involved in
auxin response in the gynoecium, as NPA treatment of wild type gynoecia
phenocopies ett. In addition, auxin may have an as yet undescribed
role in outer whorl development, because the auxin response mutant
ett, the auxin signaling mutant pid, and the auxin transport
mutant pin-formed1 (pin1) all alter floral organ numbers
(Bennett et al., 1995
;
Sessions, 1997
).
To understand more about how ETT responds to auxin to influence initiation
and patterning of floral organs, modifiers of the ett phenotype were
identified. One such modifier was found to carry a mutation in the
SEUSS (SEU) gene, which encodes a putative transcriptional
co-regulator of the floral homeotic gene AGAMOUS (AG)
(Franks et al., 2002). We
describe the effects of seu on ett and extend genetic and
morphological studies using the novel seu-3 allele. We demonstrate
that seu confers auxin resistance to the root and disrupts flower
development in combination with the auxin response mutants ett and
pid. We propose a model in which SEU acts in concert with ETT to
promote floral organ development by transcriptionally regulating
auxin-responsive genes.
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Materials and methods |
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Plant growth conditions
Plants grown on plates were in a growth chamber with 24 hours light at
22°C. Culture media consisted of half-strength MS salts, 1% sucrose and
0.8% bacto-agar at pH 5.8. For naphthaleneacetic acid (NAA) experiments, NAA
was dissolved in 70% ethanol and added to the medium before autoclaving, or in
1 M NaOH and added after autoclaving. Plants grown in soil were sown on
Metromix in 7.6 cm2 pots and grown at a 1-4 per pot density under
long-day greenhouse conditions.
Root assays
seu and wild-type seeds were grown on vertical plates. At 1-2 days
after planting (dap), seedlings were examined for presence of an emerged
radicle, and these seedlings were transplanted at 3 dap to treatment plates
(100 mm2). seu and wild-type seedlings were grown on the
same treatment plate. For lateral root counts, roots were counted at 10 dap.
For measurements of primary root length, digital photos were taken at 8 dap
and roots measured in ImageJ (public domain software available from NIH at
http://rsb.info.nih.gov/ij/).
The segmented line tool was used to trace roots, and the measure function was
used to determine root length. For root reorientation assays, plates were
rotated 90° with respect to gravity and photos were taken 24 hours later.
Root angles were calculated in Adobe Photoshop using the measure tool.
Histochemistry
ß-Glucuronidase staining was performed using 2 mM X-gluc substrate
from Rose Scientific, 2 mM potassium ferrocyanide, and 2 mM potassium
ferricyanide, at room temperature from 3 hours to overnight
(Weigel and Glazebrook,
2002).
Yeast two hybrid assays
Yeast two hybrid protocols are from Clontech. SEU prey is in pGAD424, ETT
bait is in pBD, ARF1 bait is in pGBT9 and UFO bait is in pAS1. pBD and pGAD424
were used as empty vector controls. All assays were performed in yeast strain
YD116.
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Results |
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seu plants have decreased apical dominance and appear shorter
overall (Franks et al., 2002).
Compared with wild-type flowers, seu-3 flowers are reduced in size
because of smaller petals and stamens (Fig.
1A,B). The most noticeable aspect of seu-3 flower
morphology is the apical cleft in the gynoecium. The stigma and style are
split so that two balls of stigmatic tissue are usually seen. Often, the
distal valve tips splay out where the style divides in two, resembling small
horns. Occasionally these horns have stigmatic papillae at their tips
(Fig. 1C). The lack of fusion
rarely extends far into the ovary. seu-3 flowers are semi-fertile and
produce few and irregular numbers of seeds when selfed. This is probably due
to both male and female fertility defects, as reciprocal outcrosses produce
low numbers of seeds (data not shown).
|
|
Flowers of the ett-7 seu-3 double mutant are markedly different from flowers of either single mutant. Mature flowers are half the size of single mutant flowers (Fig. 1E,I,J). The gynoecium is most often reduced to a stalk-like, ovary-less gynophore topped with stigmatic tissue, although some gynoecia retain a seu-like irregular tip (Fig. 1I). There is no eversion of internal transmitting tract or ectopic stigma, as in ett single mutants. ett-7 seu-3 intermittently develops a large ovary (Fig. 1J), which is often split open to reveal malformed ovules. In those few double mutants that develop ovaries, valve length is greater than half the length of the gynoecium 99% of the time, whereas in ett-7 single mutants, only 16% of the carpels have valves greater than half the length of the gynoecium.
seuss ettin displays severe outer whorl defects
ett affects outer whorl organs such that sepal and petal numbers
are increased from four in wild type to an average of five in ett-7
(Fig. 1D, Table 1). The outer whorls are
also affected in ett-7 seu-3 compared with each single mutant, and
this phenotype becomes more severe acropetally. Remaining petals are variably
narrowed with most being reduced to mere filaments
(Fig. 1E,I). Some sepals are
also filamentous, and others are wrinkled and reduced in size (arrowhead in
Fig. 1I). Stamens are generally
stunted and/or withered. In addition, 15% of flowers have a stamen fused
to the length of the gynoecium (Fig.
1J). Organ numbers are more variable in whorls one and two, and
reduced in whorl 3 (Table 1) compared with organ numbers in ett-7 or seu-3 single
mutants. Phyllotaxy in the outer two whorls is disrupted and organ spacing
becomes increasingly disorganized in later arising flowers, so that it becomes
difficult to distinguish whorl 1 from whorl 2. A few sepals and petals are
recognizable, but most organs have aberrant morphologies. These organs
sometimes appear to develop from the same (merged) outer organ whorl.
Disparities in ett-7 seu-3 floral organ position, shape and size can be seen at primordia inception (Fig. 2). In wild type, sepals originate from the floral meristem as four distinct bulges, which overlie the meristem by stage 6 (Fig. 2A). seu-3 sepals develop similarly, with initiation of four discrete sepal primordia occurring at stage 3 (Fig. 2B). The sepals in the lateral plane arise slightly later than the sepals in the medial plane and are therefore smaller (arrows versus arrowheads in Fig. 2A,B). Beginning at stage 4, a modest difference can be seen between seu-3 and wild-type flower development. seu-3 sepals appear smaller and often do not completely enclose the bud, leaving some of the developing meristem exposed (compare asterisks in Fig. 2A with 2B). In ett-7, although there are five sepal primordia, they are clearly distinct from each other as with wild-type sepals (Fig. 2C).
|
Effect of agamous on ettin seuss
seu causes ectopic and precocious AG expression in whorls
one and two, leading to partial homeotic transformations of sepals into mosaic
carpelloid, stamenoid or petalloid organs
(Franks et al., 2002). AG is a
MADS-box transcription factor responsible for stamen and carpel identity, as
well as for determinacy of the floral meristem
(Bowman et al., 1989
;
Yanofsky et al., 1990
). This
latter growth suppression role is supported not only by the indeterminate
flower in the ag mutant, but also by evidence that ectopic expression
of AG in whorl 2 under the AP3 promoter inhibits growth of
whorl 2 petals (Jack et al.,
1997
). If AG expression suppresses petal growth and
affects floral organ identity, the ectopic AG present in seu
could be responsible for the filamentous organ phenotype in the ett
seu double mutant.
The null ag-1 allele produces flowers with petals and sepals in
place of stamens and carpels (Fig.
3A). In addition, the indeterminate floral meristem produces an
indefinite number of additional organ whorls as (sepal, petal,
petal)n. The seu-1 mutant in Ler occasionally has
a mosaic sepal, owing to the ectopic expression of AG
(Fig. 3B). When ag-1
is crossed with seu-1, AG protein activity is removed and sepals no
longer exhibit homeotic transformations
(Franks et al., 2002). An
ag-1 seu-1 double mutant retains the organ identity and indeterminacy
of ag-1 single mutant flowers, causing reiterating whorls of sepals,
petals, petals (Fig. 3C). An
ag-1 ett double mutant also resembles ag-1 in its floral
organ identity and floral meristem indeterminacy
(Sessions et al., 1997
). Like
the double mutants, an ag-1 ett-11 seu-1 triple mutant produces a
repeating pattern of sepals, petals, petals
(Fig. 3D). However, both sepals
and petals are variably narrowed, reminiscent of the ett seu double
mutant phenotype. Each flower contains recognizable sepals and petals in its
initial whorls, but as the floral meristem develops acropetally, the organs
become increasingly filamentous. Floral meristems occasionally continue to
elongate without producing lateral organs
(Fig. 3D, arrowhead).
Determination of organ numbers in these ag ett seu mutants is
difficult because organs are not evenly spaced around the floral meristem and
individual whorls cannot be distinguished from each other. Nevertheless, it is
clear that removing ectopic and precocious AG from ett seu by
generating ag ett seu does not rescue the filamentous, mispositioned
organ phenotype present in the ett seu double mutant.
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Expression of the DR5 auxin response reporter is reduced in seuss
To further test the hypothesis that seu displays diminished auxin
response, we examined expression of the synthetic auxin response reporter
DR5::GUS (Ulmasov et al.,
1997). seu-3 shows a clear decrease in DR5 expression in
both the root and the shoot. In wild type, DR5 expression in the root meristem
extends into the root cap and stele, whereas seu-3 roots have
decreased DR5 expression in the root cap and no expression in the developing
vascular tissue (Fig. 5A,B).
The attenuation of DR5 expression in seu-3 is even more apparent in
the shoot. DR5 expression in 5-day-old wild-type seedlings is most intense at
the distal leaf tip, where auxin is produced, and also is present throughout
the leaf in incipient secondary and tertiary veins
(Fig. 5C). DR5 expression in
seu-3 seedlings, however, occurs only occasionally at the leaf tip
and in hydathodes (Fig. 5D). In
7-day-old wild-type seedlings, DR5 expression occurs in the basal half of the
leaf, paralleling the basipetal differentiation of vascular tissue
(Fig. 5E). seu-3
seedlings never show DR5 expression in these procambial sites of future vein
formation (Fig. 5F). That sites
of maximum auxin response in both the root and the leaves are diminished in
seu-3 supports a role for SEU in auxin signaling.
|
|
The pid-1 seu-3 double mutant gynoecium displays characteristics of both pid-1 and seu-3 mutants. Like pid-1, the central whorl of pid-1 seu-3 most often develops as a long gynophore topped with stigmatic tissue (Fig. 6E). The gynoecium is frequently missing major tissues, such as valves, and often is split into multiple stalks, as if carpel fusion did not occur normally (Fig. 6F).
Evaluation of organ numbers confirms the strong interaction between pid-1 and seu-3 (Fig. 7). Wild-type Ler flowers typically produce four sepals, four petals, six stamens and two carpels. When seu-3 is in the Ler background, petal and stamen numbers are decreased slightly, with a mean of 3.1 petals and 5.0 stamens. Sepal and carpel numbers in seu-3 are similar to wild type. In pid-1, variability in organ number increases, with a median of three sepals, six petals, three stamens and no valves. The double mutant produces a mean of 0.5 sepals, 0.5 petals, 0.5 stamens and 0.1 valves, with median numbers of zero for each organ type. Those few flowers that generate organs tend to be the first few in an inflorescence, with the lack of organ development increasing in later-formed flowers. This drastic reduction in organ numbers in pid-1 seu-3 suggests a synergistic interaction between these two mutants, especially in whorl two, where the increased number of petals in pid-1 is reduced to almost none in pid-1 seu-3.
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Discussion |
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SEUSS functions with ETTIN to promote floral organ development
seu-3 was originally identified as a modifier of the ett
floral mutant. ETT affects multiple patterning events during flower
development, including number and spacing of perianth organs and regional
differentiation of reproductive organs
(Sessions et al., 1997).
ETT function has been best characterized in the gynoecium because
ett ovaries are severely reduced in size, with the missing ovary
tissue replaced by abaxialized style and transmitting tract tissues. In the
ett seu double mutant, the few ovaries that are produced are longer,
making ett appear suppressed in the central whorl. SEU
promotes development of marginal tissue between the valves that gives rise to
style, transmitting tract and ovules (R. G. Franks, personal communication).
The partial suppression of ett may be explained by the lack of
development of these tissues in ett-7 seu-3, which normally
overproliferate in ett.
In the outer whorl organs, the interaction of seu and ett
appears synergistic. In seu, sepals and petals are narrower and
stamens produce little pollen. In ett, there is a slight increase in
number of sepals and petals, affecting the spacing between organs. The ett
seu double mutant exhibits a more severe phenotype, with substantial
decrease in stamen number and filamentous mispositioned perianth organs. The
spacing between organs is disrupted not only within whorls but between whorls,
so that stamens are occasionally fused with the gynoecium. This suggests that
SEU and ETT participate in convergent pathways in the floral
meristem for positioning and growth of floral organs. It is not known whether
SEU and ETT expression patterns overlap. By northern
analysis, SEU is expressed at low levels in all tissues analyzed
(Franks et al., 2002).
ETT is expressed in incipient floral meristems, but later expression
is restricted to vascular bundles of petals and stamens and the abaxial side
of the gynoecium where valves and replum differentiate
(Sessions et al., 1997
).
The SEUSS ETTIN pathway is distinct from the SEUSS AGAMOUS pathway
Double mutant analysis of ett with homeotic mutants involved in
the ABC model of floral organ development established that ETT does
not play a role in floral organ identity
(Sessions et al., 1997). By
contrast, SEU causes ectopic and precocious expression of the MADS
box transcription factor AGAMOUS, responsible for stamen and carpel
identity (Franks et al.,
2002
). Removing this misexpressed AG from the outer floral whorls
by generation of an ag-1 ett-11 seu-1 triple mutant does not affect
the filamentous, mispositioned organ phenotype caused by ett and
seu. Thus, the effects of SEU on ETT are
independent of the repression of AG by SEU. These
experiments suggest that SEU and ETT act in a distinct
pathway affecting floral organ positioning and development.
SEUSS is a novel factor affecting auxin response
Several facets of the seu phenotype resemble hallmark defects of
auxin response. Auxin is required in the root for organization of the
meristem, gravitropic response, primary root elongation and initiation of
lateral roots (Sabatini et al.,
1999; Moore, 2002
;
Casimiro et al., 2003
). The
meristem in seu-3 roots appears to function normally, but after
reorientation of vertically grown seedlings, the angle of root growth in
seu-3 is more variable than in wild type. seu-3 produces
half as many lateral roots as wild type, suggesting that either not enough
auxin is present in the root zone where lateral roots initiate, or that the
auxin present is not perceived as efficiently as in wild type.
To distinguish between these hypotheses and to confirm that seu affects auxin response, seu-3 seedlings were grown in the presence of exogenous NAA, a biologically active auxin. seu-3 roots are longer relative to wild-type roots when grown on NAA, indicating that seu-3 root growth is less inhibited by exogenous auxin than wild-type roots. That seu-3 is less responsive to NAA treatment than wild type indicates seu is defective in auxin perception or response.
Further insight into the role of SEU in auxin response was gained by examining expression of the auxin response reporter DR5. If seu is unable to transport auxin normally, auxin would pool at sites of synthesis and be depleted in other tissues. This perturbed auxin flux would be reflected in an increase in DR5 expression at the distal leaf tip and a decrease in expression in outlying areas of vascular development. However, in seu, DR5 expression is reduced but not displaced in both developing leaves and the root tip, supporting the hypothesis that seu is defective in perception of/response to auxin within a cell and not in transport of auxin between cells.
seuss flowers are sensitized to disruptions in auxin flux
The striking abolishment of outer whorl organs in the pid-1 seu-3
double mutant demonstrates a strong synergism between seu-3 and
pid-1. Because pid is thought to destabilize auxin levels in
the inflorescence meristem, the seu-3 pid-1 interaction further
implicates SEU in floral auxin response. Based on ectopic expression
data, the PID kinase has been postulated to both positively regulate auxin
transport and negatively regulate auxin signaling
(Benjamins et al., 2001;
Christensen et al., 2000
). PID
probably affects regional auxin distribution in the inflorescence meristem,
because the auxin efflux carrier PIN1 is reduced and mislocalized in
developing pid meristems
(Reinhardt et al., 2003
). This
disruption in auxin flux, together with the decreased auxin response of
seu, may account for the lack of organ primordia development in
pid-1 seu-3 double mutant flowers. Those few outer whorl organs that
develop in pid-1 seu-3 are stunted and/or filamentous, similar to
organs in ett-7 seu-3. The parallel organ phenotypes in these double
mutants supports the hypothesis that SEU functions in auxin response,
with pid-1 compromising seu floral meristems even more
severely than ett, owing to reduced auxin levels as well as reduced
auxin response. Transient application of the polar auxin transport inhibitor
NPA to wild-type inflorescences also reduces the number of outer whorl floral
organs that develop in affected flowers
(Nemhauser et al., 2000
). By
contrast, micro-application of the natural auxin indole-3-acetic acid (IAA)
promotes lateral outgrowth of both leaves and flowers
(Reinhardt et al., 2000
). The
rings of meristem tissue that develop in both ett-7 seu-3 and
pid-1 seu-3 bear similarity to the rings of flowers and floral organs
that develop in the auxin transport mutant pin1 after treatment with
IAA at the top of the pin1 inflorescence meristem
(Reinhardt et al., 2000
).
Taken together, the above findings suggest that lack of organ development in
pid-1 seu-3 is due to insufficient levels of auxin and deficient
response to auxin within organ primordia.
The severity of the pid-1 seu-3 phenotype suggests several
possible roles for the PID kinase in the ETT-SEU pathway. Because
PID has an AuxRE in its promoter and is auxin-inducible
(Benjamins et al., 2001), SEU
and ETT may function together to directly affect PID transcription. A
second possibility is that PID indirectly affects the SEU
pathway by its effect on auxin transport and regional auxin levels
(Benjamins et al., 2001
;
Reinhardt et al., 2003
).
A model for SEUSS action
The collective auxin response phenotypes of seu may reflect a
novel and fundamental role for SEU in auxin-mediated signal
transduction. Based on the genetic and physical interactions of SEU
with ETT (Figs 1,
2,
8), we propose that SEU
functions with ETT to regulate transcription of auxin response genes involved
in floral meristem patterning (Fig.
9).
|
SEU is homologous in its central region with mouse Ldb1, which
homodimerizes and binds LIM-homeodomain transcription factors to form a
tetrameric complex (Jurata et al.,
1998). SEU may similarly act as a bridging factor between ETT and
other regulatory molecules (Fig.
9). These regulatory molecules could include ARFs and/or Aux/IAAs,
which would allow regulation of the ETT transcriptional complex by the Aux/IAA
family. However, SEU interacts with ETT/ARF3 but not with ARF1, another
putative ARF repressor, in a yeast two-hybrid assay
(Fig. 8). These results suggest
a testable hypothesis that SEU interacts specifically with ETT among ARFs. In
this case, ETT and SEU may function together in regions outside the flower, as
seu mutants have global auxin response defects, and both SEU
and ETT are expressed in a variety of plant tissues
(Franks et al., 2002
;
Sessions et al., 1997
;
Ulmasov et al., 1999b
). The
present research demonstrates a role for SEU in auxin-mediated floral
organ development. Future studies will clarify the role of SEU in
transcriptional regulation of auxin response genes, and will undoubtedly
reveal additional novel players in this complex developmental program.
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ACKNOWLEDGMENTS |
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