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Please cite this article in press as: Denison FC, et al. 14-3-3 proteins in plant physiology. Semin Cell Dev Biol (2011),

doi:10.1016/j.semcdb.2011.08.006

ARTICLE IN PRESSGModel

YSCDB-1215; No.ofPages8

2 F.C. Denison et al. / Seminars inCell &Developmental Biologyxxx (2011) xxxxxx

levels ofsignaling molecules such as divalent cations or AMP to

which 14-3-3s can bind. Thepost-translational modification ofspe-

cific 14-3-3 isoforms may also be affected.

The number of putative 14-3-3 client proteins identified in

plants has now risen to over 300 [15]. These expanding data sug-

gest that 14-3-3s could potentially be involved in many signaling

pathways and physiological processes in plants. Despite the iden-

tification ofmany potential 14-3-3 clients, in vivo validation ofthe

majority ofthese clients and the mechanisms by which 14-3-3 reg-

ulates them is still lacking. Furthermore, the direct confirmation,

by phenotypic analysis, of14-3-3 roles in plant physiological path-

ways is complicated by redundancy. Plants have a varying number

ofisoforms reflecting their evolutionary histories including whole

genome and chromosomal duplications. For example, Arabidopsis

has 13 known protein isoforms [6,7], cotton has six [8], rice has

eight [9], barley has five [10] and tobacco has 17 potential iso-

forms [11]. There is high sequence conservation both within and

among species. While there is likely to be a high degree ofoverlap

between the functions ofthe different isoforms in plants, there is

also increasing evidence for variation in their affinity for certain

clients suggesting the possibility that different isoforms may play

specific roles in specific processes.

Current data clearly implicate plant 14-3-3s in key physiolog-

ical processes, in particular, abiotic and biotic stress responses,metabolism (especially primary carbon and nitrogen metabolism),

as well as various aspects ofplant growth and development. A sum-

mary ofthe 14-3-3 functions covered in this review is shown in

Fig. 1.

2. Plant stress responses

An increasing body ofwork is beginning to clarify the roles of

14-3-3s in stress response pathways in plants. These studies have

made a number of observations: 14-3-3 transcription is altered

by various stress stimuli; 14-3-3s interact, albeit mainly in vitro,

with clients known to be involved in stress signaling pathways;

transgenic plants/cells withaltered14-3-3expression show alteredstress responses; and finally, there is some evidence for phospho-

rylation of14-3-3s themselves by kinases thatare usually activated

by stress.

2.1. Effects ofstress on 14-3-3s themselves

Environmental and biotic stresses can impact 14-3-3s directly

by altering expression of specific isoforms. Some of the stimuli

shown to cause alterations in 14-3-3 expression are displayed in

Table 1. These stresses often have different effects on different iso-

forms in terms ofthe level of expression and the time course of

altered transcription. Studies ofthe putative promoter regions of

14-3-3 genes in rice have identified cis elements that can be regu-

lated by a number ofthese stimuli [9,12].At the protein level, phosphorylationat various siteshas increas-

ingly been associated with cellular stress in mammals, particularly

stresses that lead to apoptosis [1319]. A possible link between

14-3-3 phosphorylation and stress in plants has also recently been

recognized. SnRK2.8, a kinase that plays a role in drought tolerance

[20], phosphorylates certain Arabidopsis 14-3-3 isoforms in vivo

[21]. Another study reported that 14-3-3 is phosphorylated undersimulated microgravity in Arabidopsis [22]. However, few studies

in plants have looked at the biochemical and functional effects of

these modifications,while in mammals phosphorylation at specific

sites is known to affect the interaction with clients [23,24].

These expression and modification observations suggest 14-3-

3s may play an important role in stress signaling pathways and

recent attention has turned to identifying the precise nature ofthat

role and the precise positions in stress pathways that 14-3-3s are

integrated.

2.2. Response to environmental stress

The most direct evidence that 14-3-3s play a major functional

role in environmental stress responses comes fromthe overexpres-

sion ofArabidopsis 14-3-3 in cotton. These transgenic plants aremore tolerant to drought, as determined by less wilting and visible

damage to the leaves. Transpiration and photosynthesis rates are

higher thanwild-type due to increasedopeningofthe stomata [25].

One mechanism by which 14-3-3s could act in the regulation

of such environmental stress responses is though the regulation

ofion channels. The H+-ATPase, a well characterized 14-3-3 client

[2628], acts by creating the gradients that causepotassiumuptake

into guard cells and therefore stomatal opening. In sugar beet cells

exposed to cold or osmotic stress, 14-3-3 proteins increase at the

plasma membrane and are associated with increased activity the

H+-ATPase [29]. 14-3-3s are also implicated in the regulation ofa

number ofdifferent K+ channels, including an inward rectifier K+

channel, KAT1, which is involved in stomatal opening [3035]. 14-

3-3s affect the activity ofthe KAT1 channels as well as the number

ofchannels present in the membrane [33,36].

14-3-3s may also exert their effects by interacting with compo-nents ofhormone signaling pathways. A major pathway activated

by stresses such as drought, temperature and salt stress is the

abscisic acid (ABA) signaling pathway. One effect of the ABA sig-

naling pathway is to increase the expression of genes necessary

to mitigate or tolerate these stresses [37]. Interestingly, 14-3-3s

interact with some ofthe transcription factors involved in ABA

signal transduction (see Section 5). In addition, plants with down-

regulated 14-3-3 levels exhibit altered expressionofABA-regulated

genes [10]. One downstream effect of ABA signaling is stomatal

closure to prevent water loss, which involves a reduction ofthe

activity ofa 14-3-3 client, the H+-ATPase [38]. This is one exam-

ple of the involvement of14-3-3s at more than one position in a

signaling pathway, from an involvement in the signal transduction

pathwaysthemselves to interactionswith the downstreameffectorprotein that elicit the response.

2.3. Response to biotic stress

14-3-3s have long been thought to play a role in defense

against pathogens [reviewed in 29]. A number of recent stud-

ies have implicated 14-3-3s in R-gene mediated plant disease

resistance. Several 14-3-3 isoforms interact with the tobacco N

protein, which is involved in resistance to tobacco mosaic virus

[11]. Arabidopsis plants with reduced 14-3-3 expression show animpaired resistance to powdery mildew fungus infection, whereas

over-expression of 14-3-3 increases resistance and leads to theplant hypersensitive response (cell death to decrease pathogen

spread). This may be due to 14-3-3 interaction with the RPW8.2protein (product of an R gene) which acts via the salicylic acid

signaling pathway to increase resistance to powdery mildew fun-

gus. This interaction was shown by a yeast two-hybrid (Y2H)

assay and pull-down assays from 14-3-3 overexpressing plant

cell extracts. However, the authors were unable to show co-

immunoprecipitation of endogenous 14-3-3 with overexpressed

RPW8.2 in plant cells. Interestingly, 14-3-3 which shares 92%identical residues with 14-3-3 was shown not to interact withthe RPW8.2 protein [39].

14-3-3s have been implicated in Pto-mediated (product of an

R-gene) programmed cell death (PCD) in tomato in response to

effector virulence proteins from Pseudomonas syringae pv tomato.

Y2H and co-immunoprecipitation from transfected cells demon-

strated that a 14-3-3 (TFT7) could interact with the tomato
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F.C. Denison et al. / Seminars inCell &Developmental Biologyxxx (2011) xxxxxx 3

Fig. 1. Illustration ofplant 14-3-3 functional diversity.Key physiological processesin which 14-3-3s have been implicated are shown.A selection ofclient proteins to which

14-3-3s bind to affect these processes are displayed. The shape ofthe box indicates the mechanism, ifknown, by which 14-3-3 binding modifies the client (see key). For

citations, refer to the main text.

MAPKKK protein kinase [40] and its downstream kinase MAPKK[41]. The MAPK pathway is involved in plant stress and defense

responses and has been shown to positively regulate programmed

cell death in response to P. syringae [42,43]. The 14-3-3 may act

by stabilizing the MAPKKK protein so that it can activate down-stream MAPK cascades leading to PCD [40]. However, in terms of

the downstream kinase, MAPKK, a mutant version that is reduced

in its ability to bind 14-3-3 was still able to efficiently induce PCD.

PCD induction is therefore not dependent on 14-3-3 binding to this

protein, but rather a 14-3-3 mayact by bringingthe MAPKKK andMAPKK proteins together in the cell. The authors were, however,

unable to detect interaction between the two kinases in plant or

yeast cells [41]. In tobacco, TFT7 is involved in PCD induced notonly by Pto, but also by four other R proteins from different species

[40].

Recently, a 14-3-3 has been shown to be involved in another

mechanism ofplant defense: reactive oxygen species (ROS) pro-

duction. Suspension cells expressing antisense 14-3-3 displayed a

lower production of ROS in response to the fungal elicitor cryp-

togein. An interaction with tobacco NtrBohD, a plasma membrane

oxidase involved in the production ofreactive oxygen species, was

identified by Y2H [44]. Another study found a 14-3-3 protein to be

increased in detergent resistant membrane (DRM) microdomains,

the probable equivalent ofmammalian lipid rafts, after treatment

oftobaccowith cryptogein[45]. 14-3-3s and known clients (such as

H+-ATPase) have been found associated with DRMs in other stud-

ies [46,47]. These DRMs have been described as potential signaling

platforms and hence it is perhaps not surprising that 14-3-3s have

been identified at these sites. Interestingly, NtBohD has also been

shown to be increased in DRMs after cryptogein treatment [46]

suggesting a potential localization for this interaction in the plant

defense mechanism.

14-3-3s are also detected in the extracellular environment of

plant cells where they may play a role in disease resistance. 14-3-

3s have been detected in the cell wall of green algae [48,49] and

the roots ofwheat seedlings [50]. They have also been found in the

secretome from pearoot tips where it was suggested that they may

be involved in resistance toNectra haematococca [51]. In this study,

roots were treated with the R18 peptide, which binds to the 14-

3-3 client binding pocket thereby excluding clients. This bindingincreased root tip infection, although the authors admit that this

may be due to other intracellular effects ofR18. Immunofluores-

cence studies in pea and maize using an antibody raised against

Arabidopsis 14-3-3 showed extracellular fluorescence around root

border cells and it was proposed that 14-3-3s may help proteins to

function outside ofthe cell [51]. It has been suggested that 14-3-3s

may be co-transported out of the cell with clients as they do not

have typical export signals.

3. Response to light

Another plant environmental response in which 14-3-3s have

a functional role is the response to light. In particular, 14-3-3s

have been implicated in the transition to flowering in response

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Table1

Stimuli that cause altered expression of14-3-3 RNA and/or protein are displayed for various plant species. The method used to detect the altered expression is indicated.

Stimuli Species Method Isoforms Effect on

expression

Ref.

Phosphate deprivation At RNA blot 14-3-3, ,, ,

Decrease [113]

Long term potassium deficiency At 2D-GE plus MS 14-3-3,

14-3-3Decrease

Increase

[114]

-Aminobutyric acid (GABA) At RT-PCR and

protein blot

Various

isoforms

Decrease [115]

Powdery mildew fungus, salicylic acid At RT-PCR 14-3-3 Increase [39]

Temperature, salinity, oxidation, heavy

metals, hormones

Os RNA blot OsGF14b, c,

d, e, f, g

Variations

between

isoforms and

stresses

[9]

Pathogens, defense compounds,

salinity, drought, wounding, ABA

Os RNA blot OsGF14b, c,

e, f

Variations

between

isoforms and

stresses

[12]

Metal ions, NaCl, ABA St GUS reporter

assay,

RNA/protein

blot

20R Increase [116]

PVY Virus, salycilic acid, sucrose, IAA,

ABA

St GUS reporter

assay, RNA blot

16R Increase [116]

Fusicoccin Le RNA blot TFT4, 8, 9,

10

Increase [117]

Avr9 (Cladosporium fulvumelicitor) Le RNA blot TFT1, 4,6 Increase [117]

Pi, K and Fe Le RNA blot Not stated Increase [118]

Long term salt stress Nt RNA blot 14-3-3 Decrease [119]

Verticillium wilt pathogen Gh RNA blot 14-3-3 Increase [120]

Wounding, chitosan, methyljasmonate Pg, PtPa RNA blot 14-3-3 Increase [121,122]

Abbreviations: At, Arabidopsis thaliana; Os, Oryza sativa (rice); St, Solanum tuberosum (Potato); Le, Lysopersicum esculentum (tomato); Nt, Nicotiana tabacum (tobacco); Gh,

Gossypiumhirsutum (cotton); Pg, Piceaglauca (Spruce); PtPa, Populus tremulaP. alba (Poplar hybrid); 2D-GE, 2-dimensional gel electrophoresis; MS, mass spectrometry.

to photoperiod. DNA insertional mutants ofthe 14-3-3 and 14-3-3 isoforms in Arabidopsis (a long day plant) show a delay

in flowering of35 days under long-day conditions [52]. In con-

trast, heterozygous mutation ofGF14C in rice (a short day plant),

causes earlierflowering by 1217 days whereas overexpression ofGF14C causes a 520 daydelay in flowering under short day condi-

tions [53]. Y2H assays have demonstrated that 14-3-3s can interact

with proteins involved in the photoperiodic control of flowering,

such as Arabidopsis CONSTANS (CO) [52] and FLOWERING LOCUS

T (FT), as well as with FT orthologs in rice (heading date 3A, Hd3A)

and tomato (self-pruning, SP) [54]. The interaction with Hd3a was

confirmed using in vitro pull-down assays and bimolecular fluo-

rescence complementation (BiFC) assays in rice protoplasts [53].

In Arabidopsis, 14-3-3 and 14-3-3 mutant plants also displayaltered hypocotyl growth under red light suggesting a possible role

in the phytochrome B signaling pathway [52].

Arabidopsis 14-3-3s can also bind the phototropin 1 (phot1)

protein kinase which is involved in blue light signaling. The func-

tional role ofthis binding is unclear as plants expressing a mutantform ofphot1 that cannot bind 14-3-3s did not display any blue

light related phenotypes such as defects in stomatal opening, pho-

totropism, leafflattening and chloroplast accumulation [55,56].

4. Primarymetabolism

A common finding from 14-3-3 client screening studies in

plants using affinity purification (AP) is that most identified clients

fall into the category ofprimary metabolism, especially carbohy-

drate metabolism [1,3,5]. This has led to some suggestions that

plants make broader use of 14-3-3s in metabolism than animals

[3,57]. However, it has been argued that there may be bias in AP

studies towards high abundance proteins and there is often little

overlap in the clients identified when using different techniques

to identify clients [58]. In fact, in a comparison ofY2H and AP in

young barley leaves, of132 proteins identified by Y2H and over

150 identified by AP, only 10 proteins were common to both.

The proteins identified using Y2H fell mainly into the category of

signal transduction whereas for AP the main category identifiedwas primary metabolism [4]. A recent study to compare in vivo

14-3-3 complexes purified from plant and mammalian cell lysates

identified proteins involved in similar biological processes, but

in plants a greater proportion of proteins involved in primary

metabolism were identified.

Despite the potential biases ofthese client identification stud-

ies, 14-3-3s do clearly play a role in primary metabolism [reviewed

in 59]. Some ofthe most extensively studied 14-3-3 clients are

enzymes involved in carbon and nitrogen metabolism, for exam-

ple, sucrose phosphate synthase (SPS), nitrate reductase (NR) and

glutamine synthetase [reviewed in 60]. 14-3-3s are thought to play

a key role in the inhibition ofNR in the dark which prevents the

build-up ofpotentially toxic nitrites that cannot be further metab-

olized under dark conditions [61]. The effect of 14-3-3 bindingon the activity of SPS, an enzyme involved in the later stages of

sucrose synthesis, remains controversial [62,63]. In addition, there

is evidence for variation in the binding affinity ofdifferent 14-3-3

isoforms for NR andSPS [64,65]. Direct evidenceforarole of14-3-3s

in metabolism comes from several overexpression or knockdown

studies in potato. Downregulation of14-3-3s ledto increased activ-

ity ofSPS, NR and starch synthase (SS) as well as increased starch,

nitrate and sucrose levels [66]. A general pattern ofreduced 14-3-

3 levels leading to increased starch, protein and lipid content has

been noted althoughnot always consistent among different exper-

imental setups [6668]. A role in starch synthesis has also been

demonstrated following downregulation ofeither 14-3-3 or 14-3-3 in Arabidopsis which led to increasedstarchaccumulation and

an altered starch structure [69].

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F.C. Denison et al. / Seminars inCell &Developmental Biologyxxx (2011) xxxxxx 5

The discoverythat plant 14-3-3s canbindto AMP,whichinhibits

binding to certain clients [7073], suggests that 14-3-3 activity

could be affected by the metabolic status of the cell and that

14-3-3s may act as sensors of the cells energy status [59]. Fur-

thermore, the implication of 14-3-3s in pathways affecting both

sugar synthesis (SPS) and sugar storage (starch synthesis), as well

as nutrient uptake (via H-ATPase) and metabolism (NR) has led to

the suggestion that 14-3-3s are part of a global control mecha-

nism for coordinating the energy/nutrient status ofthe cell so that

energyreservesareappropriatelypartitioned [60,74]. Indeed, 14-3-

3 client binding was lost in Arabidopsis cells that had been starved

ofsugars [75].

5. Hormone signaling pathways

A number of14-3-3 roles in physiological processes may be at

least partly due to their effects on the regulation ofhormone signal-

ing pathways. Recent studies in Arabidopsis and rice have shown

that 14-3-3s are involved in negative regulation ofbrassinosteroid

signaling by anchoring the BRZ1 and BRZ2/BES1 transcription fac-

tors in the cytoplasm [7680]. In the absence ofbrassinosteroids

(BR), the BRZ1 and BRZ2/BES1 transcription factors are continu-

ously phosphorylated by BIN2 kinase. 14-3-3 binds to BRZ1 andBRZ2/BES1 in the phosphorylated state and exports them out of

the nucleus to the cytoplasm where they are degraded by the

proteasome. In the presence ofBR, BIN2 kinase is inactivated by

BSU1-mediated dephosphorylation. Unphosphorylated and thus

active BRZ1 and BRZ2/BES1 remain in the nucleus and bind to DNA

initiating the transcription ofthe BR-responsive genes [81]. AICAR

treatment to disrupt 14-3-3-client interactions, or the expression

of mutant versions ofBRZ1 or BRZ2/BES1 that are unable to bind

14-3-3, results in the accumulation of these transcription factors

in the nucleus. Plants expressing these mutants show phenotypes

indicative of constitutive BR signaling [7680]. Brassinosteroids

have been implicated in a number ofplant processes such as vas-

cular differentiation, cell elongation, pollen tube growth and stress

responses [reviewed in 82].A number ofrecent studies have linked 14-3-3s to ABA signal-

ing. Some ofthe main functions ascribed to ABA include response

to abiotic/biotic stress and seed development and dormancy

[reviewed in 83]. 14-3-3 expression has been shown to be affected

by ABA in diverse tissues and processes, ranging from guard

cells and stomatal closure, to seed dormancy and germination

[10,84,85]. In one study, the level and time course ofupregulation

in response to ABA varied between 14-3-3 isoforms (at the RNA

and protein level) in barley embryonic root [10].

14-3-3s appear to be involved in the ABA-mediated signaling

pathway that leads to alterations in transcription. Direct evidence

for this comes from the RNAi downregulation of individual 14-

3-3 isoforms in the aleurone layer of barley seeds which was

shown to alter the transcription of an ABA-regulated gene [10].One potential point of14-3-3 interaction in the ABA signaling path-

way is with the AREB/ABF/ABI5-like transcription factors that bind

to ABA-response elements. A Y2H study with five barley 14-3-3

isoforms and cDNA from young barley leaves or seeds identified

four AREB/ABF/ABI5-like transcription factors (ABF1, ABF2, ABF3,

ABI5) as 14-3-3 clients. A mutated form ofone ofthese, ABI5, that

could not interact with 14-3-3 was reduced its ability to transac-

tivate an ABA responsive promoter in the presence ofViviparous

1 (VP1), a transcriptional co-activator [4,10]. In fact, VP1 has also

been shown to interact with 14-3-3s in a Y2H study [86] and it

has been suggested that 14-3-3s may act as adaptors between VP1

and AREB/ABF/ABI5 family members [87]. Studies in cotton and

rice have also identified ABA-response element transcription fac-

tors as potential 14-3-3 clients in Y2H assays [8,88]. 14-3-3s have

been found in transcriptional complexes at the ABA-responsive

Em1 promoter in embryos [86,89]. In vivo, ABA-response element

transcription factors are thought to be phosphorylated by SnRK2

protein kinases. These kinases are activated as a result ofABA sig-

naling [90]. The phosphorylation, by SnRK2.6, ofa peptide derived

from the ABF3 transcription factor increased binding to 14-3-3

in vitro. In vivo, this phosphorylation occurred in response to ABA

which increased ABF3 stability. This effect was reduced with a

mutant version ofABF3 lacking the 14-3-3 binding site suggest-

ing that 14-3-3s may act by preventing ABF3 degradation by the

proteasome [91]. Post translational modification of14-3-3s them-

selves may also be mediated by ABA in a tissue-specific manner. In

barley, ABA treatment inhibits the proteolytic truncation ofthe 14-

3-3A isoform in the embryonic root [10]. This truncation has been

associated with embryo germination [92].

Giberellic acid (GA) has been implicated in plant elongation,

the promotion of seed germination and the onset of flowering

[reviewed in 93]. In a recent study, GA treatment influenced the

expression ofsome (but not all) ofthe five barley 14-3-3 isoforms,

but regardless ofwhether transcription ofthe isoform was induced

or repressed by GA treatment, there were no apparent changes in

14-3-3 protein levels in embryos [94]. 14-3-3s have been shown

to play a role in the post translational modification of an impor-

tant GA-associated transcription factor, repression ofshoot growth(RSG). RSG controls GA biosynthesis by a feedback mechanism and

is phosphorylated as a result ofincreased GA levels. 14-3-3s bind

the phosphorylated form ofRSG and sequester it in the cytoplasm

where it is unable to activate the transcription ofa GA biosynthetic

enzyme [95,96]. The kinase that phosphorylates RSG at Ser114 to

facilitate 14-3-3 binding is a calcium-dependent protein kinase

(CDPK) [97]. Silencingofindividualbarley isoformsin the seedaleu-

rone layer causes a reduction in GA dependent expression ofthe

gene encoding-amylase, which in turn inhibits seed germination[98]. It has been suggested that 14-3-3s are involved in cross-talk

between ABA and GA pathways, which play an antagonistic role in

seed germination, with the most likely point of interaction being

the ABF transcription factors which are involved in both hormone

signaling pathways [94].

6. Cell growth and division

The deletion of individual isoforms in plants has not been

reported to lead to any dramatic growth or developmental pheno-

types, probably due to functional redundancy.On the other hand, it

has been reported thatwhen a wholephylogenetic clade is silenced

in Arabidopsis this leads to a severe and ultimately fatal devel-

opmental delay [2]. It has been proposed that 14-3-3s may allow

the growth and development ofcells to be co-ordinated with the

metabolicstatus ofthe plant as well as environmentalstresses [80].

One aspect ofplant growth in which 14-3-3s have been recently

implicated is cell elongation. The expressionofall six cotton 14-3-3isoforms increases during the elongation phase offiber develop-

ment. Furthermore, individual overexpression of three of these

isoforms in yeast cells can induce longitudinal growth. Data from a

Y2H assay between 14-3-3s and a cotton fiber cDNA library led the

authors to suggest mechanisms by which 14-3-3s may contribute.

These included the regulation ofhormone signaling pathways, reg-

ulation ofMyb transcription factors and alterations in activity of

the H+-ATPase activity leading to pH changes and subsequently

structural changes ofthe cell wall [8].

A number of recent studies in lily have suggested 14-3-3s

may play a role in the germination and elongation of pollen.

Immunoblotting studies in pollen grains showed dynamic changes

in the localization of 14-3-3s in the cytoplasm, plasma mem-

brane, membranes of several organelles and in the extracellular

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