A DELLAcate balance: the role of gibberellin in plant

morphogenesis
Christine M Fleet1 and Tai-ping Sun2
The importance of gibberellin (GA) in vegetative and
reproductive development has been known for some time.
Recent studies have uncovered new roles of GA in leaf
differentiation, photomorphogenesis and pollen-tube
growth. Significant contributions to our understanding of
GA-regulated morphogenesis include the identification of
upstream regulators of GA biosynthesis, the elucidation of the
function of GA signaling components, and the isolation of
downstream targets. In addition, the mechanisms of
interactions between GA and other hormone pathways are
beginning to be revealed at the molecular level.
Addresses
1
UWP Box 90025, Duke University, Durham, North Carolina 27708, USA
e-mail: cmf7@duke.edu
2
Biology Department, Box 91000, Duke University, Durham,
North Carolina 27708, USA
Corresponding author: Sun, Tai-ping (tps@duke.edu)

Current Opinion in Plant Biology 2005, 8:7785

This review comes from a themed issue on
Growth and development
Edited by Liam Dolan and Michael Freeling
Available online 26th November 2004
1369-5266/$ see front matter
# 2005 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2004.11.015
Abbreviations
ABA
abscisic acid
AGL15
AGAMOUS-LIKE15
AP
APETALA
BEL
BELL
DDF1
DWARF AND DELAYED FLOWERING1
FUS3
FUSCA3
GA
gibberellin
GA20ox GA 20-oxidase
GAI
GA-INSENSITIVE
GFP
green fluorescent protein
GID2
GA-INSENSITIVE DWARF2
KNOX
KNOTTED1-like homeobox
LEC
LEAFY COTYLEDON
LFY
LEAFY
LUE1
LUCIFERASE SUPER-EXPRESSOR1
PKL
PICKLE
POTH1
POTATO HOMEOBOX1
RGA
Repressor of ga1-3
RGL1
RGA-like1
RSG
REPRESSION OF SHOOT GROWTH
SLN1
SLENDER1
SLR1
SLENDER RICE1
SLY1
SLEEPY1
SNE
SNEEZY
www.sciencedirect.com

SOC1
SPY

SUPPRESSOR OF CONSTANS1
SPINDLY

Introduction
The plant hormone gibberellin (GA) has long been
known to modulate development throughout the plant
life cycle. Mutants that are impaired in GA biosynthesis
or response tend to have small and dark green leaves and
reduced stem length. Some of them are also defective in
seed germination and floral development, and are delayed
in flowering time (see [1,2,3] for reviews). Conversely,
plants with increased GA levels or GA signaling have a tall
and spindly phenotype (reviewed in [4]).
Insight into mechanisms of GA-regulated plant growth
and development has been gained from research into both
GA biosynthesis and signaling pathways. The genes
encoding GA biosynthetic enzymes (Figure 1) have been
identified in numerous species. Among these enzymes,
GA 20-oxidase (GA20ox) and GA 3-oxidase (GA3ox),
corresponding to the last portion of GA biosynthesis,
are particularly important for control of bioactive GA
levels. In addition to biosynthesis, GA levels are also
modulated by catabolism via GA2ox enzymes (Figure 1)
and by feedback regulation through activity in the
GA-response pathway. Transcript levels of some of the
GA20ox and GA3ox genes are downregulated, whereas
GA2ox genes are upregulated by elevated GA signaling
or GA treatment (reviewed in [3,5,6]).
GA biosynthetic genes are expressed in specific cell- and
tissue-types during development, and their transcript
levels are often elevated in rapidly growing regions, such
as the rib meristem of shoot apex, elongating internodes,
developing anthers and embryo axes [3]. In rice, GA20ox
and GA3ox are expressed in a pattern similar to that of GA
signaling genes [7], further suggesting that GA may be
synthesized at the site of perception. Recent studies also
suggest, however, that GA made in anthers and developing embryos is probably transported to regulate the
growth of other floral organs and fruits. Similarly, GA that
is synthesized in the embryo during seed germination
needs to be transmitted to aleurone cells to induce the
expression of hydrolytic enzymes [7,8].
GA signaling operates as a de-repressible system that
is moderated by DELLA-domain proteins, which are
transcriptional regulators that repress GA responses
(Figure 2). DELLA proteins are highly conserved among
Current Opinion in Plant Biology 2005, 8:7785

78 Growth and development

Figure 1

CPS

KS

KO

KAO

GA20ox

GA3ox

Bioactive
GA

GA2ox

Inactive
GA

GA signaling pathway

GA responses
Current Opinion in Plant Biology

GA biosynthetic and catabolic enzymes, and feedback regulation of GA biosynthesis by the GA-response pathway. Bioactive GAs are
synthesized from geranyl geranyl diphosphate via multiple enzymes that catalyze sequential steps in the pathway. Boxed italic text indicates
metabolites. T-bars indicate the inhibition of gene expression, the block arrow indicates the promotion of gene expression. GA homeostasis is
achieved by a feedback mechanism. An elevated activity in the GA-response pathway downregulates transcript levels of some of the GA20ox
and GA3ox genes, but upregulates transcript levels of GA2ox genes. CPS, copalyl diphosphate synthase; GA2ox, GA 2-oxidase (encoded by
multiple genes); GA3ox, GA 3-oxidase (encoded by multiple genes); GA20ox, GA 20-oxidase (encoded by multiple genes); KAO, ent-kaurenoic
acid oxidase; KO, ent-kaurene oxidase; KS, ent-kaurene synthase.

different species, including Arabidopsis, barley, Brassica,

grape, maize, rice, and wheat (reviewed in [1]). A single
DELLA protein gene is present in rice and barley
(SLENDER RICE1 [SLR1] and SLENDER1 [SLN1],
respectively) and functions to repress all aspects of GA
Figure 2

GA
Receptor

SLY1/SNE
/GID2

SPY

DELLA

PKL

LUE1

SOC1

GAMYB

B & C genes

LFY

Embryonic
cell fate*

Germination

Stem Flowering
elongation

Flower
development

Current Opinion in Plant Biology

Model of the GA signaling pathway. Ovals represent transcription

factors, gray lines indicate hypothesized interactions. Arrows and
T-bars indicate direct or indirect activation and inhibition, respectively.
B genes encode PI and AP3; the C gene in this pathway encodes
AGAMOUS; DELLA includes RGA, GAI, RGLs, SLR1, SLN1, and
other orthologs. *PKL inhibits embryonic cell fate during
post-embryonic development.
Current Opinion in Plant Biology 2005, 8:7785

responses in these species. Surprisingly, five DELLA

protein genes (GA-Insensitive [GAI], Repressor of ga1-3
[RGA], RGA-like1 [RGL1], RGL2 and RGL3) have been
identified in Arabidopsis, with RGA and GAI being the
major GA repressors during vegetative growth and floral
induction [3,4]. During seed germination, RGL2 plays a
major role, whereas RGA, RGL1 and RGL2 together
modulate flower development [9,10,11].
In response to GA, DELLA proteins are rapidly degraded
by the ubiquitin-proteasome pathway [12]. F-box proteins that mediate this degradation (as part of the E3
ubiquitin ligase SCF [Skp1-Cullin-F-box] complex) have
been identified in Arabidopsis (SLEEPY1 [SLY1]) and
rice (GA-INSENSITIVE DWARF2 [GID2]) [13,14].
Other components of GA responses include the positive
regulator PHOTOPERIOD-RESPONSIVE1 (PHOR1)
of potato, which shows similarity to the U-box ubiquitin
E3 ligase and might also be involved in the degradation of
DELLA proteins [15], and the negative regulator,
SPINDLY (SPY), an O-linked N-acetylglucosamine
transferase that has been identified in Arabidopsis, barley
and petunia, and is hypothesized to modify and activate
DELLA proteins (Figure 2; [1,3,4]). In addition, the
chromatin-remodeling factor PICKLE (PKL) is thought
to function as a positive regulator of GA response [1,4].
An important downstream component of GA response
is the GA-inducible transcription factor GAMYB. This
transcription factor was first identified for its role in
promoting a-amylase expression in germinating barley
seeds (reviewed in [16]), but GAMYB homologs have now
been identified in other species. In addition to GAMYB,
GA is known to induce the expression of GLABROUS1, a
transcription factor that is required for trichome production, consistent with the role of GA in regulating trichome
initiation and branching [17].
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Gibberellin in plant morphogenesis Fleet and Sun 79

GA biosynthesis and signaling pathways have been discussed in detail in several recent reviews [1,2,3,4,6,12].
In addition, several reviews discuss general mechanisms
of morphogenesis [18,19]. Although the role of GA in
many stages of development is well established
(Figure 3), many questions remain as to how GA functions
and which components of the GA pathway are required
for what aspects of morphology. This review focuses on
recent studies on the mechanisms of GA action in particular developmental stages.

Vegetative elongation
One of the most well-known functions of GA is to
promote vegetative growth, including the elongation of
stems and roots, and the expansion of leaves. Loss-offunction mutations in GA-biosynthetic genes or in positive regulators of GA signaling (e.g. sly1, gid2 or pkl) confer
a characteristic dwarf phenotype, whereas knocking out
GA signaling repressors (e.g. DELLA proteins or SPY)
results in GA-independent growth (reviewed in [1,3,4]).
Table 1 lists upstream and downstream components
that affect GAs influence on plant development and
morphogenesis.
Stem

Most of the original GA-deficient dwarf mutants had

defects in GA biosynthetic enzymes, but more recent
work has focused on genes that encode GA-catabolizing
enzymes, the GA2-oxidases. Overexpression of these
genes also results in decreased height and internode
length in several species, including Arabidopsis [20], rice
[21], and poplar [22], emphasizing the importance of GA
in regulating height.
The recent identification of transcriptional regulators of
the GA biosynthetic genes is beginning to reveal the
mechanism through which GA levels control plant
growth. The tobacco protein REPRESSION OF
SHOOT GROWTH (RSG), a bZIP transcription factor,
binds to and activates the transcription of the GA biosynthetic gene Kaurene Oxidase (Figure 1; [23]). Overproduction of a dominant negative mutant form of RSG confers a
GA-deficient dwarf phenotype and prevents the upregulation of GA20ox expression in transgenic tobacco, suggesting that RSG also plays a role in feedback regulation
of GA20ox. Interestingly, GA treatment promotes the
translocation of RSG from the nucleus to the cytoplasm,
where RSG interacts with 14-3-3 proteins and thus is
prevented from migrating to the nucleus [24].
Overexpression studies of two other transcription factors
suggest their roles in regulating GA biosynthesis in
Arabidopsis. Overproduction of either the APETALA2
(AP2)-type transcription factor DWARF AND DELAYED FLOWERING1 (DDF1) [25] or the MADSbox protein AGAMOUS-LIKE15 (AGL15) [26] results in
a GA-deficient dwarf phenotype. The decreased GA
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accumulation of DDF1 overexpressors suggests that

DDF1 may directly or indirectly repress the expression
of GA biosynthetic genes, although a preliminary investigation did not show changes in the levels of the biosynthetic genes tested. Chromatin immunoprecipitation
studies show that AGL15 binds to the promoter of
AtGA2ox6, suggesting that AGL15 might also regulate
GA levels [26]. The physiological functions of RSG,
DDF1 and AGL15 require further investigations, however, because the effects of these genes on GA metabolism have mainly been shown by ectopic expression
studies.
Two new positive components of GA response, which
affect stem elongation, have recently been identified in
Arabidopsis. Overexpression of SNEEZY (SNE), a homolog of the Arabidopsis F-box protein SLY1, rescues the
stem elongation of sly1 mutants, presumably by promoting the degradation of DELLA proteins [27]. On the
basis of the high expression level of SNE in flowers,
however, its normal function may be more important in
floral development. The Arabidopsis LUCIFERASE
SUPER-EXPRESSOR1 (LUE1) gene encodes a katanin
p60 ortholog [28]. Loss of LUE1 function results in
altered microtubule orientation and decreased stem
length, as well as in an increased expression of the
biosynthetic gene AtGA20ox1 that may occur because
impaired GA response affects the feedback mechanism
[28,29].
Hypocotyl

GA is important in promoting cell elongation in hypocotyls as well as in the stems of light-grown plants. Recently,
ethylene, auxin and brassinolide were each shown to have
synergistic effects with GA in promoting cell elongation
and hypocotyl length in Arabidopsis (Figure 3; [3032]).
However, the precise means of interaction among these
hormones is not yet known.
Seedling development is altered in response to light. In
photomorphogenic (light-grown) seedlings, hypocotyls
are shorter than those of dark-grown seedlings and the
cotyledons are green and fully expanded. Etiolated (darkgrown) seedlings, however, have unexpanded cotyledons
and elongated hypocotyls with apical hooks (reviewed in
[30]). In dark-grown Arabidopsis and pea, decreased GA
levels result in a partially photomorphogenic phenotype
and increased expression of light-induced genes [33].
Loss-of-function rga and gai mutations rescue the abovementioned GA-deficient phenotype, indicating that the
DELLA proteins RGA and GAI repress GAs inhibition
of photomorphogenesis in etiolated Arabidopsis seedlings
[33,34]. Interestingly, ethylene and auxin response
pathways appear to interact with the GA signaling pathway upstream of the DELLA proteins to promote apicalhook formation [34,35]. LUE1, a putative downstream
component of GA response, is also suggested to promote
Current Opinion in Plant Biology 2005, 8:7785

80 Growth and development

Figure 3

Auxin and ethylene

ABA

GA

Brassinolide

Germination

Ethylene + GA

Hypocotyl

Ethylene +GA
Auxin + GA
Brassinolide +GA

elongation
Apical hook formation

Auxin

or

Light
Ethylene

Dark

Root

GA

elongation

Auxin

Stem
elongation

Leaf shape

Auxin + GA

Auxin + GA
Cytokinin
GA
Trichome
formation

Flower

Fertility

development

GA

GA

GA
Fruit
development

Current Opinion in Plant Biology

Interaction of GA with other hormones. Roles for hormones other than GA are indicated only when they interact with GA functions. Large
arrows indicate changes in developmental stage. Italic text indicates a developmental process that is affected by the indicated hormones.
T-bars denote inhibition of the indicated process, whereas black arrows denote promotion. Gray arrows denote a hypothesized role (on the
basis of data from microarray analysis of transcripts in germinating seeds treated with GA). Two hormones showing synergistic interaction are
denoted by a + between them; this does not imply an ordering of their activities. ABA, abscisic acid.

apical-hook formation in response to ethylene [28].

During de-etiolation, red-light perception induces photomorphogenesis and acts partially through GA; red-light
treatment of seedlings reduces GA sensitivity in several
species and also reduces GA biosynthesis in pea
(reviewed in [30]). Blue light may also influence GA
biosynthesis in a manner that promotes de-etiolation
[30,36].
Current Opinion in Plant Biology 2005, 8:7785

Root

The roots of the Arabidopsis GA-deficient mutant ga1-3

are shorter than those of wildtype plants, and their length
is restored by knockout mutations of the DELLA genes
RGA and GAI [37], suggesting that RGA and GAI inhibit
root elongation and that GA promotes root growth by
inducing the degradation of these DELLA proteins.
Other hormones appear to play a role in regulating the
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Gibberellin in plant morphogenesis Fleet and Sun 81

Table 1
Genes involved in GA modulation of morphogenesis.
Gene

Species

Protein function

Relation to GA pathway Mutant phenotype(a)

Reference(s)

GA biosynthesis regulators
AGL15

Arabidopsis

DDF1
FUS3

Arabidopsis
Arabidopsis

MADS-box transcription
Induces GA2ox6
factor
AP2-like transcription factor Decreases GA levels
B3 transcription factor
Represses GA3ox

KNAT1

Arabidopsis

KNOX

Represses GA20ox

POTH1
RSG
STM1

Potato
Tobacco
Arabidopsis

KNOX
bZip transcription factor
KNOX

Represses GA20ox
Represses KO
Represses GA20ox

DELLA transcription
regulator

Represses GA
response

Reduced height, late flowering (OE)

[26]

Reduced height, late flowering (OE)

Cotyledons replaced by vegetative
leaves (LOF); reduced height (OE)
Increased leaf lobes (OE), repressed
by GA
Reduced height, rounded leaves (OE)
Reduced stem elongation (DN)
Defective or missing shoot apical
meristem (LOF), enhanced by spy

[25]
[61]
[19,41]
[43]
[23,63]
[41]

GA signaling components
DELLA

Multiple(b)

PHOR1
PKL

Potato
Arabidopsis

Ubiquitin E3 ligase
CHD3 chromatin
remodeling factor
SLY1/GID2 Arabidopsis/rice F-box protein
SNE

Arabidopsis

F-box protein

SPY

Arabidopsis,
barley, petunia

O-GlcNac transferase

Reduced height, reduced fertility,

delayed flowering (GOF); tall,
slender phenotype in single-gene
species (LOF)
Promotes GA response Reduced height (AS)
Promotes GA response Embryonic characteristics in
root tissue (LOF)
Promotes degradation Reduced germination and height,
of GA repressors
delayed flowering (LOF)
Promotes degradation Rescues height of sly1 (OE)
of GA repressors
Represses GA
Elongated stem, reduced
response
fertility (LOF)

[1,9,1012,39,57]

[15]
[5860]
[13,14]
[27]
[1,4]

Downstream effectors
GAMYB

Multiple

Transcription factor

Promotes GA-induced
gene expression

GL1
LUE1

Arabidopsis
Arabidopsis

MYB transcription factor

Katanin p60-like

Induced by GA
Promotes GA effects

miR159

Multiple

MicroRNA

SOC1

Arabidopsis

MADS-box
transcription factor

Promotes degradation
of GAMYB
Promotes GA effects

Reduced a-amylase expression,

reduced pollen development
(rice LOF); male sterility (barley OE)
Lacks trichome development (LOF)
Reduced stem elongation, delayed
flowering (LOF)
Delayed flowering, reduced anther
development (Arabidopsis OE)
Early flowering, partially rescues
flowering delay of ga1-3 (OE)

[16,53,54]

[17]
[28,29]
[47]
[48]

(a)

Mutant phenotype caused by: AS, anti-sense; DN, dominant negative; GOF, gain-of-function; LOF, loss-of-function; OE, overexpressors.
Includes RGA, GAI, RGL1, RGL2, RGL3 of Arabidopsis, SLN1 of barley, SLR1 of rice, d8 of maize, RHT of wheat, Vvgai1 of grape,
and DWF2 of Brassica. GL1, GLABROUS1; KNAT1, KNOTTED1-like in ARABIDOPSIS THALIANA; PHOR1, PHOTOPERIOD-RESPONSIVE1.
(b)

action of GA in root growth. Observations of green

fluorescent protein (GFP)RGA fusion protein in
Arabidopsis roots suggest that auxin is required for GAmediated root elongation because it promotes the GAinduced degradation of RGA [37]. Conversely, ethylene
inhibits both GA-induced degradation of GFPRGA and
GA promotion of root elongation [34]. Interestingly, this
is different from the GA and ethylene interaction in the
hypocotyl, where ethylene and GA act together.

Seed germination
GA plays a crucial role in germination, and its function
has been studied extensively in germinating cereals. GA
promotes the degradation of the DELLA proteins SLN1
of barley and SLR1 of rice. This degradation allows the
activation of GAMYB to induce the expression of awww.sciencedirect.com

amylase and other hydrolases and proteases, mobilizing

nutrients that are stored in the endosperm [2,16,38,39].
The 1-hour lag time between DELLA protein degradation and GAMYB induction suggests that GAMYB might
not be a direct target of DELLA proteins. Numerous
studies have also shown a role for DOF-type transcription
factors in either promoting or opposing the action of
GAMYB (reviewed in [12]).
GA antagonizes the dormancy-promoting effects of
the plant growth regulator abscisic acid (ABA) and the
germination-inhibiting effects of DELLA proteins
(reviewed in [2,40]). Microarray data from analyses of
expression profiles in germinating Arabidopsis seed
suggest that GA may decrease the expression of
ABA-response-element-containing genes to promote
Current Opinion in Plant Biology 2005, 8:7785

82 Growth and development

germination [8]. The DELLA protein RGL2 of Arabidopsis plays a major inhibitory role in germination and is
rapidly degraded in response to GA [9,10].
Studies in tomato show that GA promotes radicle penetration through the seed coat and induces the expression
of expansins and cell-wall modifying genes [2], suggesting additional roles for GA in germination. Microarray
analysis of GA-treated germinating Arabidopsis seeds
shows the induction of several cell-elongation-promoting
genes. Such analysis also shows the induction of genes
that are related to the plant growth regulators ethylene
and auxin [8], suggesting that GA may promote radicle
extension through interactions with other hormones.

Leaf initiation and morphogenesis

Maintenance of the shoot apical meristem and initiation
of leaf primordia are in part regulated by KNOTTED1like homeobox (KNOX) transcription factors and GA. In
simple-leaved species, such as Arabidopsis and tobacco,
in situ hybridization and biochemical studies show that
KNOX genes are expressed at the meristem where they
exclude the expression of the GA biosynthetic gene
GA20ox. Instead, GA accumulates in the leaf primordia
of these species to promote determinate growth
(reviewed in [19]). Interaction between KNOX genes
and GA also affects leaf shape. In tomato, which has
dissected leaves, KNOX genes are expressed in meristems
as well as in leaf primordia, where decreased GA levels are
suggested to promote increased leaf dissection [41]. Overexpression of KNOX genes in tobacco, Arabidopsis and
tomato represses GA20ox expression and results in both
the formation of ectopic meristems on leaves and
increased lobe formation [41,42].
In potato, overexpression of the KNOX gene POTATO
HOMEOBOX1 (POTH1) not only represses GA20ox
expression and results in smaller wrinkled leaves but also
promotes tuber formation [43]. This result is consistent
with the inhibitory role of GA in potato tuber formation
[6], and suggests that the regulation of GA biosynthesis by
homeobox genes is not limited to leaves. Recent studies
also indicate the involvement of BELL (BEL) proteins,
another class of homeobox proteins, in KNOX repression
of GA biosynthesis. Transient expression studies using
tobacco protoplasts showed that binding of POTH1 to the
GA20ox promoter requires interaction with a BEL protein, StBEL5 [43,44].
It will be of interest to determine whether GA interacts
with other hormones, such as cytokinin and auxin, to
regulate leaf initiation. The potential roles of these hormones are implicated by the findings that cytokinin levels
are elevated by overexpression of KNOX or BEL [45],
and that proper distribution of auxin in the apex may be
required to downregulate KNOX expression and to control
the phyllotaxy of lateral organs [19].
Current Opinion in Plant Biology 2005, 8:7785

Reproductive development
Floral induction

Many GA-related mutations that affect stem elongation

also alter flowering time. In long-day plants such as
Arabidopsis, mutations that block GA biosynthesis or
responsiveness (e.g. sly1) cause delayed flowering,
whereas mutants with increased GA signaling (e.g. rga,
gai and spy) flower early [3]. In addition, the overexpression of DDF1, which reduces GA levels, and loss-offunction of LUE1 both result in late flowering in
Arabidopsis [25,28,29].
The GA response is one of several pathways that promote
flowering in Arabidopsis functioning upstream of the floral
integrators LEAFY (LFY) and SUPPRESSOR OF CONSTANS1 (SOC1; also known as AGL20) (reviewed in
[46]). LFY expression is activated by GA and is probably
mediated by AtGAMYBs. Interestingly, AtGAMYB transcripts can be degraded by overexpression of the microRNA miR159, resulting in delayed flowering in short days
[47]. SOC1 acts upstream of LFY and functions to
integrate the long-day, vernalization and autonomous
pathways for flowering time [46]. In short days, GA is
essential for floral induction in Arabidopsis, and the recent
finding that GA induces SOC1 expression suggests that
SOC1 also mediates GA-dependent flowering [48].
Flower development

Severely GA-deficient mutants of some species have

impaired flower development, including defective petals
and stamens. These mutants tend to be male sterile
because of defects in pollen development before (in
tomato) or after (in Arabidopsis) meiosis during microsporogenesis [11,49,50]. Examination of mutations in the
DELLA genes of Arabidopsis shows that RGA, RGL1 and
RGL2 act together to repress GA-dependent petal and
pollen development, as well as the elongation of the
anther filament [10,11].
Downstream of the integrator proteins of flowering pathways are the floral meristem identity proteins that regulate flower development. In Arabidopsis, GA has recently
been shown to induce expression of the floral meristem
identity genes AP3, PISTILLATA (PI), and AGAMOUS,
which control B and C function in the formation of petal
and stamen primordia [51]. These results suggest that
maintenance of B and C gene expression by GA is
important for the continued development of petals and
stamens. In Arabidopsis, GA is also required to promote
pollen-tube elongation [52], consistent with the role of
GA in the cell elongation of other tissues.
In addition to its role in germinating seeds and floral
induction, GAMYB also functions to regulate flower
development. OsGAMYB is highly expressed in stamen
primordia and in the tapetum in rice, and loss-of-function
mutations in OsGAMYB cause defects in anthers and
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Gibberellin in plant morphogenesis Fleet and Sun 83

premeiotic pollen development [53]. Interestingly,

overexpression of barley GAMYB results in male sterility
with small anthers and pollen that fails to dehisce [54];
this overexpression phenotype resembles that of plants
that are overdosed with GA [55,56]. Similarly, knockout
of SLR1 in rice or SLN1 in barley results in a sterile
phenotype [39,57]. Taken together, these findings point
to the importance of precise regulation of DELLA proteins and GAMYB levels for the proper development of
anthers.

Foundation (IBN 0235656 and IBN 0348814) and the US Department

of Agriculture (03-35304-13284).

References and recommended reading

Papers of particular interest, published within the annual period of
review, have been highlighted as:
 of special interest
 of outstanding interest
1. Thomas SG, Sun T-p: Update on gibberellin signaling. A tale of

the tall and the short. Plant Physiol 2004, 135:668-676.
A current review on gibberellin signaling that emphasizes the role of
DELLA proteins in Arabidopsis and in crops.
2.

Peng J, Harberd NP: The role of GA-mediated signalling in

the control of seed germination. Curr Opin Plant Biol 2002,
5:376-381.

3.

Olszewski N, Sun T-p, Gubler F: Gibberellin signaling:

biosynthesis, catabolism, and response pathways.
Plant Cell 2002, (Supplement):S61-S80.

4.

Richards DE, King KE, Ait-ali T, Harberd NP: How gibberellin

regulates plant growth and development: a molecular genetic
analysis of gibberellin signaling. Annu Rev Plant Physiol Plant
Mol Biol 2001, 52:67-88.

5.

Yamaguchi S, Kamiya Y: Gibberellin biosynthesis: its regulation

by endogenous and environmental signals. Plant Cell Physiol
2000, 41:251-257.

6.

Hedden P, Phillips AL: Gibberellin metabolism: new insights

revealed by the genes. Trends Plant Sci 2000, 5:523-530.

Embryo development

The developmental program for embryogenesis not only

needs to be activated following fertilization but also
should be turned off in vegetative tissues; GA may play
roles in both of these processes. The chromatin-remodeling factor PKL, a putative positive regulator of GA
response, inhibits the expression of the LEAFY COTYLEDON (LEC) genes, LEC1, LEC2, and FUSCA3 (FUS3);
it also represses embryonic cell fate in post-embryonic
development in Arabidopsis [5860]. Although the
mechanism of PKL interaction with the GA pathway is
not clear, the pkl phenotype suggests a role for GA in
preventing inappropriate embryonic fate by suppressing
LEC genes. Recently, FUS3 was shown to repress transcript levels of the GA biosynthetic gene AtGA3ox1, but to
upregulate ABA levels during early embryogenesis [61].
These studies raise an interesting possibility that FUS3
regulates embryo development by modulating GA- and
ABA-mediated pathways. Although the results described
above suggest that GA could inhibit embryo development, some GA is necessary for embryogenesis, as suggested by the kaurene oxidase mutation in pea that results
in seed abortion [62]. GA appears to feed-back regulate
FUS3 by inducing its degradation [61], suggesting that
the interactions between GA and LEC genes are complex.

Conclusions
Recent progress has been made in understanding the
molecular mechanisms of GA action at particular developmental stages, but many gaps remain to be filled if we
are to understand how GA modulates plant growth and
morphogenesis. One striking characteristic of the recent
findings is the importance of other hormones in regulating
GA responses (Figure 3). It is intriguing that ethylene and
auxin appear to alter GA responses by directly or indirectly affecting the degradation of GA signaling repressors,
DELLA proteins. Further investigation of the molecular
mechanisms that are involved in hormone cross-talk will
allow us to understand how GA and other hormone
pathways interact to control plant morphogenesis in
response to developmental and environmental cues.

Acknowledgements
We regret that length limitations prevent us from mentioning
additional excellent papers that relate GA and plant morphogenesis.
This work was supported by grants from the National Science
www.sciencedirect.com

7.


Kaneko M, Itoh H, Inukai Y, Sakamoto T, Ueguchi-Tanaka M,

Ashikari M, Matsuoka M: Where do gibberellin biosynthesis and
signaling occur in rice plants? Plant J 2003, 34:1-12.
The authors use b-glucuronidase (GUS) reporter constructs to compare
the localizations of GA biosynthesis and signaling proteins in rice.
Observations of OsGA20ox1, OsGA20ox2, OsGA3ox1, OsGA3ox2, D1,
and SLR1 show that the biosynthesis and signaling genes have overlapping expression in germinating seeds, elongating stem, inflorescence
and floral meristem, suggesting that GA is synthesized at the site of
perception. In the seed epithelium and anther tapetum, only biosynthetic
genes are observed; and in the aleurone, only signaling genes are
observed.

8.


Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y,

Yamaguchi S: Gibberellin biosynthesis and response during
Arabidopsis seed germination. Plant Cell 2003, 15:1591-1604.
The authors of this paper present microarray data to show the effects of
GA on gene expression in germinating seeds. The data identify GAresponsive genes that are involved in cell elongation. GA also affects
other hormone pathways; for example, it is involved in the downregulation
of ABA-responsive genes and the upregulation of genes that are involved
in auxin transport or ethylene synthesis and response.
9.

Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J,

Harberd NP, Peng J: Gibberellin regulates Arabidopsis seed
germination via RGL2, a GAI/RGA-like gene whose expression
is up-regulated following imbibition. Genes Dev 2002,
16:646-658.

10. Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun T-p:

DELLA proteins and gibberellin-regulated seed germination
and floral development in Arabidopsis. Plant Physiol 2004,
135:1008-1019.
Together with [11], this paper points to particular roles for the Arabidopsis DELLA proteins RGA, RGL1 and RGL2 in development. Roles in
germination are shown for RGL2 [10], and in flower development and
fertility for all three DELLA proteins [10,11]. This is consistent with the
high expression levels of RGL1 and RGL2 observed in flowers, siliques
and germinating seeds [10].
11. Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D,

Harberd NP, Peng J: Gibberellin regulates Arabidopsis floral
development via suppression of DELLA protein function.
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See annotation for [10].
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signaling in plants. Annu Rev Plant Biol 2004, 55:197-223.
A comprehensive review on gibberellin signaling.
Current Opinion in Plant Biology 2005, 8:7785

84 Growth and development

13. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM,
 Sun T-p, Steber CM: The Arabidopsis SLEEPY1 gene encodes
a putative F-box subunit of an SCF E3 ubiquitin ligase.
Plant Cell 2003, 15:1120-1130.
The authors identify SLY1 by map-based cloning. SLY1 is similar to
members of the F-box family, which are involved in proteasomemediated degradation. Loss-of-function sly mutants, which were shown
previously to have increased dormancy, reduced height, delayed flowering and decreased fertility, are partially rescued by a rga loss-of-function
mutation. Additionally, wildtype RGA protein accumulates to high levels in
sly mutants, supporting a role for SLY in mediating GA-induced RGA
degradation.
14. Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K,
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Accumulation of phosphorylated repressor for gibberellin
signaling in an F-box mutant. Science 2003, 299:1896-1898.
Rice GID2, whose loss-of-function results in a severe dwarf phenotype,
encodes a putative F-box protein. GID2 interacts with a rice SKP homolog
in the yeast two-hybrid assay, indicating that the SCF (Skp1, Cullin,
F-box) ubiquitin ligase complex might mediate the degradation of components of the GA signaling pathway. The rice gid2 mutants accumulate
high levels of the DELLA protein SLR1, suggesting that GID2 may be
required for GA-induced degradation of SLR1 via the proteasome
pathway.
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24. Ishida S, Fukazawa J, Yuasa T, Takahashi Y: Involvement of

14-3-3 signaling protein binding in the functional regulation
of the transcriptional activator REPRESSION OF SHOOT
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Observation of a RSG::GFP fusion protein shows that GA treatment
reduces the nuclear localization of RSG, presumably preventing its
transcription factor activity. Additionally, this work shows that RSG must
be phosphorylated to allow its binding to 14-3-3, and suggests that
dominant negative RSG may interfere with GA feedback regulation of
the biosynthetic gene NtGA20ox.
25. Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K: dwarf and

delayed-flowering 1, a novel Arabidopsis mutant deficient in
gibberellin biosynthesis because of overexpression of a
putative AP2 transcription factor. Plant J 2004, 37:720-729.
The authors identify an activation-tagged Arabidopsis mutant, ddf1,
which shows the phenotype of a GA-deficient dwarf. Levels of bioactive
GA are decreased in ddf1, and its phenotype is fully rescued by the
Current Opinion in Plant Biology 2005, 8:7785

addition of GA. The mutation is suggested to be caused by overexpression of an AP2-type transcription factor that is related to the DREB1/CBF
family, which is known to function in stress response.
26. Wang H, Caruso LV, Downie AB, Perry SE: The embryo MADS

domain protein AGAMOUS-like 15 directly regulates
expression of a gene encoding an enzyme involved in
gibberellin metabolism. Plant Cell 2004, 16:1206-1219.
Promoter binding assays were used to show that AGL15 is a direct
regulator of the GA-catabolizing gene AtGA2ox6, identifying one of only
a few known transcription factors that regulate GA metabolic genes.
Overexpression of either AtGA2ox6 or AGL15 results in decreased levels
of bioactive GA and a GA-responsive GA-deficient dwarf phenotype. The
role of AtGA2ox6 is suggested by promoter-reporter assays that show
AtGA2ox6 expression in developing embryos, germinating seeds and
seedlings, and by the increased seed dormancy observed in
35S::AtGA2ox6 overexpressors.
27. Strader LC, Ritchie S, Soule JD, McGinnis KM, Steber CM:

Recessive-interfering mutations in the gibberellin signaling
gene SLEEPY1 are rescued by overexpression of its
homologue, SNEEZY. Proc Natl Acad Sci USA 2004,
101:12771-12776.
The authors show that stem elongation is rescued in the GA-signaling
mutant sly1-10 by overexpression of SNE, a SLY1 homolog. SNE expression is shown to be highest in flower tissue, with significant accumulation
also occurring in the stem.
28. Bouquin T, Ole M, Henrik N, Randy F, Mundy J: The Arabidopsis

lue1 mutant defines a katanin p60 ortholog involved in
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growth. J Cell Sci 2003, 116:791-801.
The authors use map-based cloning to identify a mutation in the AtKSS
(which encodes Arabidopsis thaliana katanin-like microtubule-severing
protein) that causes the lue1 phenotype. This phenotype includes
reduced height and altered GA response. The mutant shows altered
cortical microtubule arrangement, supporting the idea that GA might
promote growth partly through effects on microtubule orientation.
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32. Tanaka K, Nakamura Y, Asami T, Yoshida S, Matsuo T,
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growth of Arabidopsis: brassinosteroids have a synergistic
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repress photomorphogenesis in darkness. Plant Physiol 2004,
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With the authors of [34,35], the authors of this paper show the importance of GA in apical hook formation in Arabidopsis, and they further
extend this work to pea. RNA-blot analysis demonstrates that the lightregulated genes CAB and RbcS remain upregulated in GA-deficient darkgrown seedlings relative to wildtype, and that this upregulation is partially
rescued by brassinolide (BR) in Arabidopsis. Interestingly, in etiolated
pea, BR treatment cannot replace the role of GA in repressing photomorphogenesis.
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regulates Arabidopsis development via the modulation of
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Using a GFP fusion protein and immunoblot analysis, the authors show
that ethylene delays GA-responsive degradation of RGA in Arabidopsis
roots, suggesting that ethylene antagonizes the promotion of root growth
by GA. Conversely, the phenotypes of dark-grown seedlings in which
GA and/or ethylene levels or response is altered suggest that the two
hormones work coordinately in promoting apical hook formation
[34,35].
35. Vriezen WH, Achard P, Harberd NP, Van Der Straeten D:

Ethylene-mediated enhancement of apical hook formation in
www.sciencedirect.com

Gibberellin in plant morphogenesis Fleet and Sun 85

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36. Folta KM, Pontin MA, Karlin NG, Bottini R, Spalding EP: Genomic
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 modulating gibberellin response. Nature 2003, 421:740-743.
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defective anther development, indicating an important role for miRNA
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48. Moon J, Sung-Suk S, Lee H, Choi K-r, Hong CB, Paek N-C,

Kim S-g, Lee I: The SOC1 MADS-box gene integrates
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shows reduced sensitivity to GA.

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51. Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM: Floral


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Current Opinion in Plant Biology 2005, 8:7785