Plant Signaling & Behavior

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Shedding light on flower development

Phytochrome B regulates gynoecium formation in association with the
transcription factor SPATULA

Julia Foreman, James White, Ian Graham, Karen Halliday & Eve-Marie Josse

To cite this article: Julia Foreman, James White, Ian Graham, Karen Halliday & Eve-Marie Josse
(2011) Shedding light on flower development, Plant Signaling & Behavior, 6:4, 471-476, DOI:
10.4161/psb.6.4.14496

To link to this article: https://doi.org/10.4161/psb.6.4.14496

Published online: 01 Apr 2011.

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 short communication
Plant Signaling & Behavior 6:4, 471-476; April 2011; ©2011 Landes Bioscience

Shedding light on flower development

Phytochrome B regulates gynoecium formation
in association with the transcription factor SPATULA
Julia Foreman,1 James N. White,1 Ian A. Graham,2 Karen J. Halliday1 and Eve-Marie Josse1,*
Institute of Molecular Plant Sciences; School of Biological Sciences; University of Edinburgh; Edinburgh, Scotland, UK; 2Centre for Novel Agricultural Products;
1

Department of Biology; University of York; York, UK

Key words: flower development, gynoecium, SPATULA, phytochrome, auxin

Abbreviations: bHLH, basic helix-loop-helix; PIF, phytochrome interacting factor; NPA, N-1-naphthylphthalamic acid; GA,
gibberellic acid; wt, wild-type

Accurate development of the gynoecium, the female reproductive organ, is necessary to achieve efficient fertilization. In
Arabidopsis, the correct patterning of the apical-basal axis of the gynoecium requires the establishment of a morphogenic
gradient of auxin. This allows the production of specialized tissues, whose roles consist of attracting pollen, allowing
pollen tube growth and protecting the ovules within the ovaries. Mutations in the bHLH transcription factor SPATULA
(SPT) are known to impair the development of the apical tissues of the gynoecium. Here, we show that the spt phenotype
is rescued by the removal of phytochrome B, and discuss how light signaling may control flower development.

Introduction Mutations in the SPATULA (SPT ) gene impair the develop-

In Arabidopsis, the gynoecium, the female reproductive organ, is
a highly specialized organ resulting from the congenital fusion of
two carpels, forming a hollow cylinder. A fully developed gynoe-
cium consists of a short basal gynophore on which sits the large
ovary, within which the ovules develop. The ovary is divided into
two compartments by a septum, and is extended apically by a
short style and a stigma. The stigmatic tissue is designed to trap
the pollen and during fertilization, the pollen tubes germinate on
the stigma and grow through the transmitting tract that devel-
ops within the style and the septum, before swerving laterally to
eventually reach the mature ovules.1
Several regulatory mechanisms are involved in the forma-
tion of the gynoecium and its apical-basal specification. The
current dogma implies the formation of a morphogenic gra-
dient of auxin, where an auxin maximum on the apical side
of the gynoecium is needed to promote the formation of the
style and stigma. Progressively diminishing levels of auxin
towards the basal side of the gynoecium specify the ovaries
area and eventually the gynophore at the basal side, where
auxin concentration reaches a minimum.2,3 A large number of
transcription factors have been described to take part in gynoe-
cium patterning via the mediation of auxin-related processes,
including ETTIN (ETT), STYLISH (STY), SPATULA
(SPT), HECATE (HEC) and SEUSS (SEU) (reviewed in refs.
1, 3 and 4).
ment of the apical tissues of the gynoecium, as the carpels fail to
fuse properly, disrupting the formation of the transmitting tract,
the style and the stigma.5-7 This results in a reduced frequency of
fertilization and low seed production.8 Several lines of evidence
have linked SPT and the establishment of the morphogenic auxin
gradient throughout the basal-apical axis of the gynoecium:
indeed, spt apical phenotype can be rescued by the application
of N-1-naphthylphthalamic acid (NPA), a polar auxin transport
inhibitor, suggesting that SPT activity may result in disrupting
auxin transport. Furthermore, the auxin-response factor ETTIN
(ETT) is crucial for both the setup and the interpretation of the
auxin gradient, and has been shown to mainly act by restrict-
ing SPT expression.2 In addition to its role in gynoecium pat-
terning, SPT has also been shown to be involved in defining the
fate of the apical meristem during the very early stages of flower
development.6
SPT is a basic helix-loop-helix transcription factor, belong-
ing to the Phytochrome Interacting Factors/PIF-Like (PIF/PIL)
family, where almost all members have been shown to regulate
different aspects of light development.7,9 Phytochromes are red/
far-red light photoreceptors which, upon red light activation,
change into an active conformation and rapidly migrate into the
nucleus, where they bind members of the PIF family, leading to
the de-repression of PIFs-controlled transcription. While PIF1,
PIF3, PIF4, PIF5, PIF6 and PIF7 bind to the phytochromes
directly,10-14 PIL factors lack the ability to bind phytochromes

*Correspondence to: Eve-Marie Josse; Email: eve-marie.josse@ed.ac.uk

Submitted: 12/13/10; Accepted: 12/13/10
DOI: 10.4161/psb.6.4.14496

www.landesbioscience.com Plant Signaling & Behavior 471

 Figure 1. Effect of hormone treatment on gynoecium development. Light microscopy images of the apical extremity of Col (A–D) and spt-11 (E–H) gy-
noecia dissected from stage 12 flowers. The early buds were treated as indicated and the flowers were left to develop for 7 days. Bar = 200 μm (inset:
whole gynoecium, bar = 500 μm).

directly.11 They however can form heterodimers with true PIFs,
and modulate their function.15,16 SPT belongs to this later PIL
category.11
SPT has been shown, together with PIF1, to control seed
germination in response to both cold and light treatment.17,18
One mechanism through which SPT and PIF1 act is by regu-
lating gibberellic acid (GA) biosynthetic genes in the develop-
ing seed.14,17-19 GA is a phytohormone triggering cell expansion,
and is required for seed germination, as well as growth at many
stages throughout the plant life. Of particular interest, GA is
necessary for the development of the fruit post-fertilization. In
this instance, it was recently shown that auxin promotes GA
metabolism in fertilized ovules, and that constitutive GA signal-
ing is sufficient to trigger parthenocarpy, independently of the
fertilization event.20
SPT is also involved in seedling development: while spt
mutants present large cotyledons, an overexpression of SPT
leads to the development of a long hypocotyl and very small
cotyledons when grown in red light, resembling a phytochrome
B (phyB)-null mutant.17 Additionally, SPT also controls leaf size
in a similar manner, especially under colder conditions.21,22
The possibility of a role for SPT in phytochrome signaling,
as well as its dramatic action in gynoecium development, led
us to investigate whether phyB could influence SPT-dependent
gynoecium development.
Results
In spt monogenic mutants, the gynoecium develops abnormally,
with unfused carpels at the upper-most side and reduced stig-
matic papillae. However, when polar auxin transport is inhibited
by NPA treatment, the spt gynoecium presents a morphology
similar to an untreated wt gynoecium 2,6 (Fig. 1). We have previ-
ously shown that SPT regulates GA biosynthesis in the seed,17
and it has been demonstrated that, post-fertilization, an auxin
signal is able to trigger GA production in the developing fruit.20
We therefore set out to determine whether the spt gynoecium phe-
notype could be affected or rescued by GA treatment. Figure 1
shows that GA treatment of a wt gynoecium does not affect its
formation (Fig. 1C), but is unable to rescue spt-11 gynoecium
development (Fig. 1G). However, GA treatment does not pre-
vent spt-11 phenotypic rescue by NPA treatment (Fig. 1H). This
suggests that, when controlling gynoecium development, SPT is
not targeting GA biosynthesis.
Since SPT belongs to the same clade as the light regulated PIF
proteins, we next decided to test whether SPT function during
gynoecium formation was phytochrome-dependent. Null phyB

472 Plant Signaling & Behavior Volume 6 Issue 4

 Figure 2. phyB mutation complements the spt gynoecium, silique and seed phenotypes. (A) Light microscopy images of the apical extremity of
Ler, spt-2, phyB-1, spt-2phyB-1, Col, spt-11, phyB-9 and spt-11phyB-9 gynoecia dissected from stage 11 flowers. Bar = 100 μm. (inset: whole gynoecium,
bar = 200 μm). (B) Length of dry siliques produced by the same plants grown in long days at 22°C (n = 20). (C) Seed area measured from seeds har-
vested from the siliques measured in (B). Error bars represent standard error (n = 200).

mutant fruits develop normally, both pre- and post-fertilization
(Fig. 2A–C), the final silique’s size being only slightly longer
in a phyB-1 mutant (Ler ecotype), but not in a phyB-9 mutant
(Col ecotype) (Fig. 2B). Both the Ler spt-2 and the Col null allele
spt-11 present the previously described gynoecium development
defect6,21 (Fig. 2A). However, in a phyB null background, this phe-
notype is fully rescued (Fig. 2A). Additionally, the phyB mutation
rescues the spt short silique phenotype (Fig. 2B) as well as spt larger
seed size (Fig. 2C). This clearly demonstrates that, for gynoecium
and fruit development, the function of SPT is phyB-dependent.
SPT function has been shown to be involved at different
stages of the gynoecium development: indeed, on one hand, SPT
promotes carpel development early during flower formation,6 and
on the other hand SPT is required for normal tract formation and
apical fusion during gynoecium development.5-7 We therefore set
out to observe the phyB-dependence of the spt gynoecium pheno-
type through a number of developmental stages (Fig. 3). While
both Col gynoecium and phyB-9 gynoecium apices are fused
throughout development, spt-11 gynoecium presents a lack of car-
pel fusion at the apical pole as early as we could observe (stage 8).
Interestingly, the spt-11 phyB-9 double mutant is very similar to
a spt-11 mutant at these early developmental stages. Fusion of
the carpels and rescue of the spt phenotype only occurred by
stage 11 of gynoecium development. This suggests that the phyB

www.landesbioscience.com Plant Signaling & Behavior 473

mutation is only able to rescue SPT function at a later devel-
opmental stage, when the basal-apical axis of the gynoecium is
being defined.
Discussion
Phytochrome’s paramount role in controlling numerous aspects
of the plant life, from germination and early development to
plant architecture and flowering, have been studied at length in
the past years.23-25 However, this is the first report of a role for
phyB in flower development.
A large body of evidence has shown that, under the regulation
of the transcription factor STYLISH (STY), auxin forms a mor-
phogenetic gradient within the gynoecium, which is believed to
be interpreted by ETT, SPT and HECATE (HEC), leading to
the formation of a series of different structures along the apical-
basal axis of the gynoecium, in an auxin concentration-depen-
dent manner.2,26-29 Meanwhile, numerous recent studies have
investigated the relationship between phyB and phytohormones,
with a large focus on auxin pathways. Indeed, phytochrome sig-
naling has been shown to influence auxin pathways at different
levels: auxin production, auxin distribution and sensitivity to
auxin signals (reviewed in ref. 30).
Phytochromes have recently been shown to directly control
auxin production. Active phyB reduces auxin production via the
concurrent activation of (SUPERROOT 2) SUR2, a suppres-
sor of auxin biosynthesis and the inhibition of TRYPTOPHAN
AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1),
an enhancer of auxin biosynthesis.30-33 Conversely, it has been
shown that reduced levels of phyB, triggered by shade condi-
tions, set off the opposite response, with an elevation of IAA
production.30,33 Strikingly, mutations in TAA1, together with its
homolog TRYPTOPHAN AMINOTRANSFERASE RELATED
2 (TAR2) lead to the production of a gynoecium presenting an
apicalized phenotype, with reduced or nonexistent valve area
and an over-abundance of stigmatic tissue,34 showing that the
integrity of the TAA1-dependent branch of auxin biosynthesis is
essential for a correct patterning of the gynoecium. Interestingly,
the expression pattern of both TAA1 and TAR2 in the gynoe-
cium coincides with SPT expression, suggesting a causal link
between SPT and auxin production, with SPT either directly
responding to or being involved in auxin production.35 Here, we
show that in a phyB-null mutant, the spt gynoecium phenotype
is rescued. This suggest that, in a spt mutant, where the auxin
gradient fails to either be set-up or interpreted, reducing phyB
levels could result in a modification of auxin production, par-
ticipating to local changes in auxin concentration throughout
the gynoecium, and resulting in a rescue of the spt phenotype.
Additionally, polar auxin transport and light signaling have
been functionally linked in numerous studies, mainly looking at
seedling development, shoot-root communication and the con-
trol of branching. Indeed, phytochrome mutants have reduced
sensitivity to NPA-induced hypocotyl growth inhibition, sug-
gesting that polar auxin transport requires functional phyto-
chrome action.36 Similarly, phytochrome mutants show reduced
shoot-root auxin transport,37 as well as reduced auxin-dependent
474 Plant Signaling & Behavior
branching.25 At the molecular level, phytochromes were shown
to influence both the expression and the localization of a hand-
ful of auxin transporter involved in polar auxin transport.37-40
This means that the absence of phyB in a spt background could
impair auxin transport through the gynoecium in a NPA-
mimicking way, resulting in the establishment of the auxin
gradient needed for the correct specification of the gynoecium
apex, and a rescue of the spt phenotype.
Eventually, both light and auxin pathways share common
targets and are highly integrated, especially during the shade
avoidance response, where neighboring vegetation produce a
far-red light rich environment, which depletes the active phyB
pool (reviewed in refs. 30 and 41). There, phyB depletion leads
to the accumulation of PIF family members, resulting in the
induction of the expression of a number of transcription factors.
These include the SPT homologs LONG HYPOCOTYL IN
FAR-RED (HFR1), PIL1 and PIL2,42-44 as well as the more dis-
tant relatives PHYTOCHROME RAPIDLY REGULATED1
(PAR1) and PAR2.45,46 Interestingly, both HFR1 and PAR1/2
have been shown to suppress the transcription of a number of
auxin signaling targets including members of the SAUR and
the Aux/IAA family, suggesting that shade conditions lead to
a de-repression of auxin signaling.43,45,46 Moreover, PIF4 was
also shown to regulate auxin-mediated signaling pathways in
response to high temperature.47 Additionally, members of the
PIF/PIL family are known to regulate each other’s expression44
and have highly redundant functions.12,48 Taken together, these
results offer the possibility that SPT could regulate auxin sig-
naling by targeting shade-induced genes like HFR1 and PIL1.
In this case, SPT function could therefore be supplemented in
a phyB-null mutant by the action of members of the PIF family
like PIF4 and PIF5 that are stabilized.
In this context, it is also interesting to notice that SPT is
able to heterodimerize with a wide range of bHLH transcrip-
tion factors, showing interaction in yeast-2-hybrid experiments
with HEC1/2/3, 28 as well as with PIF1 and PIF4 (Bou-Torrent
and Martinez-Garcia, personal communication). This there-
fore offers the possibility that in the gynoecium, SPT and PIF4
could dimerize, leading to an increase in PIF4 stability, and an
induction of shade related genes.
Alternatively, as the spt phenotype could result from a
decrease in auxin sensitivity, 2 the de-repression of auxin signal-
ing when phyB levels are depleted could increase the general
sensitivity for auxin, rescuing the gynoecium development in
a spt mutant.
In conclusion, we show here that the spt phenotype is rescued
equally by NPA addition and by a phyB mutation: this is correl-
ative evidence that phyB could be acting on auxin production,
distribution or sensitivity within the gynoecium to promote the
establishment of the basal-apical axis of the developing flower.
This work demonstrates a role for phyB in the control of flower
development, and shows a cooperative function for the PIF3-
homologue SPT and phyB in this developmental process. Future
work, however, will be necessary to identify the exact point(s)
of interaction between phyB and SPT signaling leading to the
establishment of the auxin gradient within the gynoecium.
Volume 6 Issue 4
 Figure 3. phyB mutation does not complement the spt early phenotype. Time series of gynoecium development: Col, spt-11, phyB-9 and spt-11phyB-9
flowers from stage 8 to 16 were dissected and their gynoecium was observed by light microscopy. Bar = 100 μm.

Materials and Methods
Lines and growth conditions. Both Landsberg erecta (Ler) and
Columbia-0 (Col) accessions of Arabidopsis thaliana were used.
The spt-2 and phyB-1 mutants (Ler alleles) as well as the spt-
11 and phyB-9 mutants (Col alleles) were described previously
in references 6, 21 and 49. spt-2 phyB-1 and spt-11 phyB-9 were
obtained by cross-pollination of their respective parents and
were selected via PCR and sequencing methods.
Plants were grown in a (2:1) soil-sand mixture under long
days conditions (16:8) at 22°C under 100 μmol.m-2.s-1 of white
light.
Hormone treatments. All siliques, flowers and large buds
were removed, and the inflorescences were dipped 2 days in a
row in the indicated solution of hormone (NPA or GA 3) or water
(mock) prepared in 0.01% silwet L-77 (Lehle seeds, VIS-02).
Flowers were then observed 7 days later.
Light microscopy and size measurements. Unstained plant
material was dissected and viewed with a Leica MZ 16 F micro-
scope. Silique length (n = 20) and seed area (n = 200) were mea-
sured using the ImageJ software (http://rsbweb.nih.gov/ij/).
Gynoecium development stages were defined as published in
references 1 and 50.
Acknowledgments
This work was supported by the UK Biotechnology and Biological
Sciences Research Council (B.B.S.R.C.) grants BBE0003631 to
K.J.H. and BBE0005411 to I.A.G.

www.landesbioscience.com Plant Signaling & Behavior 475


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