gibberellin signal pathway

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Gibberellin signalling pathwayKenji Gomi and Makoto Matsuoka

Recent molecular biological and genetical studies have identifiedseveral positive and negative regulators of gibberellin (GA)

signalling pathways in higher plants. The DELLA protein

functions as a negative regulator of GA signalling; its degradation

through the ubiquitin/proteasome pathway is a key event in the

regulation of GA-stimulated processes.

Addresses

BioScience Centre, Nagoya University, Nagoya 464-8601, Japane-mail: [email protected]

Current Opinion in Plant Biology 2003, 6:489493

This review comes from a themed issue on

Cell signalling and gene regulationEdited by Kazuo Shinozaki and Elizabeth Dennis

1369-5266/$ see front matter

2003 Elsevier Ltd. All rights reserved.

DOI 10.1016/S1369-5266(03)00079-7

Abbreviations

d1 dwarf1

GA gibberellin

gai gibberellic-acid insensitive

GAMYB GA-regulated MYB transcription factorGFP green fluorescent protein

gid1 GA-insensitive dwarf1

KGM KINASE ASSOCIATED WITH GAMYBPHOR1 PHOTOPERIOD-RESPONSIVE1

rga repressor of ga13Rht Reduced height

RSG REPRESSION OF SHOOT GROWTHSCF Skp1cullinF-box

Skp1 Suppressor of kinetochore protein1

sln1 slender1

slr1 slender rice1

SLY1 SLEEPY1

spy spindly

IntroductionGibberellins (GAs) are a large family of tetracyclic diter-

penoid plant growth regulators. To date, 126 GAs havebeen identified in higher plants, fungi and bacteria [1].They are associated with several plant growth and devel-

opment processes, such as seed germination, stem elon-

gation, flowering, fruit development and the regulation

of gene expression in the cereal aleurone layer [24].

Many GA-related mutants have been isolated from var-

ious plant species [3,4,5], and these mutants have

helped to determine the physiological role of GA and

to elucidate its biosynthetic pathways. Genes that

encode GA-catalytic enzymes have been identified using

GA-deficient mutants, enabling researchers to build

an almost complete cascade of the GA biosyntheticprocess [1]. In contrast to the GA-biosynthesis cascade,

the mechanisms of GA signal transductionare still poorly

understood. Recent studies have revealed that a negative

regulator functions as a molecularswitch in GA signalling

[610,11]. In this review, we summarise recent findings

on theGA signalling pathway, focusing on studies carried

out in the past two years.

Positive regulation of GA signallingGAMYB is a GA-regulated MYB transcription factor that

was first identified as an activator ofa-amylase expression

in barley aleurone cells [1214]. A recent study demon-strated that the role of GAMYB is not restricted to

aleurone cells but is also involved in anther development

in barley [15]. Furthermore, GAMYB interacts with

KGM (KINASE-ASSOCIATED WITH GAMYB), which

was isolated by yeast two-hybrid screening using GAMYB

as bait. KGM is a member of an emerging subgroup of

protein kinases and it represses GAMYB function in

barley aleurone [16]. Although the phosphorylation of

GAMYB by KGM has not been demonstrated and the

detailed function of KGM is not yet clear, the character-

isation of KGM function will provide new insights into

GA signalling pathways.

The rice dwarf1 (d1) mutant has a GA-insensitive dwarf

phenotype. The D1 gene encodes an a-subunit of hetero-trimeric G proteins [17,18]. Phenotypic analysis revealed

that increased expression of the GA 20-oxidase gene led to

the accumulation of high concentrations of bioactive GA in

the stunted internodes of d1 mutants. Furthermore, ana-

lysis of a d1 and slender rice1 (slr1) double mutant revealed

that SLR1 is epistatic to D1 [19]. These results indicate

that D1 functions as a positive regulator of GA signalling.

Some recent studies have demonstrated, however, that the

D1 protein also functions in auxin signalling and disease

resistance [20,21]. More precise analysis will be necessary

to identify the overall function of the D1 protein.

REPRESSION OF SHOOT GROWTH (RSG) isthought to be a positive regulator of the GA-biosynthetic

pathway in tobacco. Transgenic tobacco plants expressing

a dominant-negative form of RSG had a dwarf phenotype

and a reduced concentration of the active GA, GA1. RSG,

which contains a basic leucine-zipper (bZIP) domain,

transactivated the expression of the ent-kaurene oxidase

gene through interaction with its promoter sequence [22].

Recently, it has been demonstrated that 14-3-3 proteins

bind RSG and control its subcellular localisation, thus

regulating its efficiency as a transcriptional effector of

GA-synthesis genes in the nucleus [23].

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PHOTOPERIOD-RESPONSIVE1 (PHOR1) encodes the

armadillo-repeat (arm-repeat) protein, which is upreg-

ulated in potato leaves under conditions that induce

tuberisation. PHOR1-antisense plants have a semi-dwarf

phenotype similar to that of GA-deficient mutants and

exhibit reduced GA responsiveness. A PHOR1::greenfluorescent protein (GFP) construct was transported from

the cytosol into the nucleus in response to GA treatment

[24], suggesting that PHOR1 acts as a positive regulator in

GA signalling.

The GA-insensitive dwarf1 (gid1) rice mutant has a GA-

insensitive dwarf phenotype [25]. The GID1 gene

encodes a member of the serine hydrolase family, which

includes esterases, lipases, and proteases [25,26]. Al-

though the enzymatic function of GID1 has not yet beenidentified, analysis of a gid1 and slr1 double mutant has

revealed that SLR1 is epistatic to GID1. Consistent with

the idea that GID1 acts upstream of SLR1, SLR1 was not

degraded in the gid1 mutant when treated with GA,

whereas GA treatment causes rapid degradation of SLR1

in wildtype plants [26]. Recent studies have indicated

that the GID1 protein may be directly involved in the

degradation of the SLR1 protein (M Ueguchi-Tanaka,

M Matsuoka, unpublished data).

Negative regulation of GA signallingGA-insensitive mutants that are defective in the DELLAgenes have been identified in screens of various plant

species, such as Arabidopsis (repressor of ga13 [rga] and

gibberellic-acid insensitive [gai]), barley (slender1 [sln1]),

maize (Dwarf8 [D8]), wheat (Reduced height [Rht]), and

rice (slr1) [610,11,27]. These mutants fall into twoclasses: those caused by semi-dominant gain-of-function

mutations in Arabidopsis, maize, barley, and wheat, which

lead to GA-insensitive dwarfism; and those caused by

recessive loss-of-function mutations in barley and rice,

which lead to increased growth. The wheat Rhtallele was

used to produce the wheat varieties that enabled the

green revolution [8].

The DELLA proteins are members of the GRAS family,

which also includes SCARECROW and SHORT ROOT

[28]. In addition to the GRAS family consensus motifs,

GA-signal-related DELLA proteins also contain unique

motifs in their amino-terminal region called DELLAdomains. These domains are absent from other GRAS

proteins. The sequence of the Arabidopsis gai allele

demonstrated that in-frame deletion mutations in the

DELLA domain induced the GA-insensitive dwarf phe-

notype ofgaimutants [6]. Similarly, wheat Rht-B1/Rht-D1

and maize D8alleles also have an in-frame deletion in the

DELLA or TVHYNP domain, respectively [8]. Further-

more, transgenic rice plants that overproduced an SLR1

protein that had a truncated DELLA domain showed a

dominant GA-insensitive dwarf phenotype [10,11]. On

the other hand, null alleles for these proteins, such as

those of rice slr1 and barley sln1 mutants, induced a

constitutive GA-responding phenotype [10,11]. These

results demonstrate that DELLA proteins function as

negative regulators of GA signalling, and that the

DELLA and TVHYNP domains are essential for this

function. Further domain analysis using transgenic riceplants that overproduced different kinds of truncated

SLR1 proteins revealed that the SLR1 protein can be

divided into four parts: a GA signal perception domain at

the amino terminus (DELLA and TVHYNP), a regula-

tory domain that controls the proteins repression activity

(S/T-rich domain), a dimer-formation domain (leucine

zipper), and a repression domain at the carboxyl terminus

[11]. DELLA proteins are localised in the nuclei where

they suppress the downstream GA action and are rapidly

degraded in response to GA signals [2931]. It has beensuggested recently that GA-dependent degradation of

DELLA proteins is a key event for GA-signalling.

Arabidopsis spindly (spy) was first identified as a mutant

that is resistant to the GA-biosynthesis inhibitor paclobu-

trazol (PAC); spy germinates in the presence of PAC,

which blocks the germination of wildtype Arabidopsis[32]. The SPYgene encodes a protein that is homologous

to O-GlcNAc transferase. Recent studies on the over-

expression ofSPYhave indicated that SPY functions not

only as a negative regulator of GA signalling but also in

other signalling pathways. Filardo and Swain [33] dis-cussed the possibilities of the negative regulation of

PHOR1 function by SPY and of crosstalk between the

GA response and the circadian clock.

Involvement of the ubiquitin/proteasomepathway in GA signallingVery recently, we isolated a new GA-insensitive dwarf rice

mutant, gid2, which has a severe dwarf phenotype without

any GA-responses [34]. The GID2 gene encodes a puta-

tive F-box protein, which interacted with a rice Skp1

(Suppressor of kinetochore protein1) homologue in a yeast

two-hybrid assay. GID2 is therefore expected to form aSkp1cullinF-box (SCF) complex and to function as an

E3 ubiquitin ligase. In gid2mutants, SLR1 accumulates in

a phosphorylated form even though these mutants also

accumulate high levels of active GA. In contrast, SLR1 is

rapidly degraded by GA through ubiquitination in the

wildtype [34

]. The Arabidopsis SLEEPY 1 (SLY1) genehas been isolated by positional cloning and found to

encode a putative F-box protein with structural similarity

to rice GID2. In the sly1 mutant, the DELLA protein

RGA accumulates to high concentrations even after GA

treatment [35]. Furthermore, a recent phenotypical anal-

ysis of barley sln1 revealed that the degradation of SLN1

protein is inhibited by proteasome and kinase inhibitors

[36]. These findings indicate that GA induces the degra-

dation of DELLA-repressor proteins through the ubiqui-

tin/proteasome pathway, mediated by the SCF complex.

The degradation mechanisms are probably not uniform

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for all DELLA proteins, however, because ArabidopsisGAI is not degraded as a result of GA3 treatment [37].

Further biochemical studies are needed to solve the

overall function of the DELLA proteins in the GA

signalling pathway.

PHOR1, which contains an U-box domain at its amino

terminus, may also be involved in the degradation of

DELLA proteins. The U-box motif was first identified

in yeast UFD2, an E4 multiubiquitin chain assembly

factor, and was later recognised as a conserved domain

that is shared with proteins in various kinds of organisms

[38]. In Arabidopsis, 37 predicted U-box proteins have

been identified in database searches [39], although their

biological function has not yet been characterised. The

predicted three-dimensional structure of the U-boxdomain is similar to that of RING fingers [40], some of

which have E3 ubiquitin ligase activity in triggering the

degradation of target proteins [41]. Recent studies have

demonstrated that U-box proteins in mammals possess

ubiquitin ligase activity [42,43]. In this context, PHOR1

may act as an E3 ubiquitin ligase that degrades DELLA

proteins in the GA signalling pathway.

ConclusionsThe processing of the GA signal in the nucleus depends

directly on the presence or absence of DELLA proteins,

which are therefore presently considered to be a mole-

cular switch for GA signalling (Figure 1). An SCF com-

plex is essential for the degradation of DELLA proteins,

which results in the transduction of the GA signal. Rice

GID2 and Arabidopsis SLY1 are F-box proteins, which are

typically components of SCF complexes. Many F-box

proteins contain a proteinprotein interaction domain,such as a leucine-rich repeat (LRR) or a WD-40 repeat

sequence, which allows their interaction with target

Figure 1

GAMYB

GA-response genes

KGM

Nucleus

GA signal

PHOR1

PHOR1

RSG

14-3-3 protein

RSG

GA-mediated action

Cytoplasm

GID2/SLY1

Kinase

SLR1/RGA

GID1

D1

GA

GA

SPY

Current Opinion in Plant Biology

Possible roles of recently identified factors in the GA signalling pathway. In the absence of GA, DELLA protein (SLR1/RGA) directly or indirectly inhibits

the expression of GA-induced genes, including GAMYB. KGM inhibits GAMYB activity by phosphorylation. SPY activates the negative regulator and

inhibits the activity of the positive regulator by O-GlcNAc modification. GA binds to an unidentified GA receptor(s) and activates G proteins (D1) that

enhance the GA signal. PHOR1 is translocated into the nucleus, where it acts as a positive regulator by GA signalling. The GA signal also activates

protein kinase and GID1 to trigger GID2/SLY1-mediated degradation of SLR1/RGA. 14-3-3 proteins regulate the subcellular localisation of RSG,

which controls the expression of the ent-kaurene oxidase gene.

Gibberellin signalling Gomi and Matsuoka 491



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proteins [4446]. GID2 and SLY1 do not contain such

interactive sequences, however, suggesting that they may

not interact directly with SLR1 and RGA. Additional

protein(s) may be required as mediators of the interaction

between GID2/SLY1 and their target proteins, SLR1/

RGA, respectively.

Phosphorylation of the DELLA protein (SLR1) triggers

its ubiquitin/proteasome-mediated degradation through

interaction with SCFGID2. In barley, a tyrosine kinase

inhibitor blocked the GA-induced degradation of SLN1

[36], indicating that GA-dependent phosphorylation of

DELLA protein forms part of the GA signalling pathway.

Thus, the next steps in unravelling the GA signalling

pathway are to identify DELLA-protein-specific kinases

and the phosphorylation site of DELLA proteins.Furthermore, as DELLA proteins may not contain

DNA-binding domain, even though they seem to func-

tion as trans-acting factors, other interacting factors that

contain DNA-binding motifs should exist. At present,

there is little information on the relationship between

GAMYB and DELLA proteins. GA-induced expression

of GAMYB was inhibited in the barley dominant Sln1mutant, indicating that SLN1 functions upstream of the

transcription of GAMYB in barley aleurone cells [31,47].

Whether GAMYB and DELLA proteins interact directly

is unclear; other protein(s) may be necessary to transduce

the signal from a DELLA protein to GAMYB. Finally, thenature of the primary GA receptor is still obscure, despite

great efforts to identify it. At present, favoured hypoth-

eses assume that there may be two types of GA receptor in

plant cells; one a plasma-membrane-bound receptor and

the other a cytoplasm-type receptor. The isolation andcharacterisation of the GA receptor is one of the most

important targets in this field.

AcknowledgementsOur research on GA is supported by a Grant-in-Aid forCentres of Excellence,a Grant-in-Aid from the program for the Promotion of Basic ResearchActivities for Innovative Bioscience, and by the Ministry of Agriculture,Fisheries and Food (MAFF) Rice Genome Project.

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