tinhibition and stimu

P

ht Ucie

nd

literature can help to understand the two contrastingfaces of growth control by ethylene. Here, we propose a

the strongly enhanced shoot elongation of semi-aquatic

elongation was also reported for leaves of Poa species [21],

Opinion TRENDS in Plant Science Vol.11 No.4 April 2006Corresponding author: Voesenek, L.A.C.J. (l.a.c.j.voesenek@bio.uu.nl).biosynthesis and signaling components, see Box 1 [25]) can affect both cell expansion and the rate ofphotosynthesis. These processes control growth ratesand growth responses to internal and environmentalsignals. Understanding the complex interplay betweenethylene signaling and other signal transduction path-ways should help us to understand the processes throughwhich ethylene can exert its, sometimes opposing, effectson whole-plant growth.

Stimulation versus inhibition of growthEthylene is generally considered growth inhibitory [6],with the triple response of dark-grown seedlings, firstdiscovered in Pisum sativum [7], as the classical example.

Rumex palustris roots [22] and roots of Cucumis sativus[23]. Stems and petioles can show similar growth-inhibitory responses to ethylene [24]. In accordance withthis, ethylene overproduction reduces internode length intransgenic tobacco (Nicotiana tabacum) [25] and overallstature in the eto1 Arabidopsis mutant [8]. Furthermore,the Arabidopsis constitutive ethylene signaling mutantctr1 is significantly dwarfed with unexpanded leaves anda greatly reduced cell size [26]. By contrast, ethylene-insensitive mutants (e.g. etr1-1 and ers1) were reported tobe considerably larger than wild-type plants [19,27], evenin the absence of exogenous ethylene treatment. Thelarger leaf area is thought to be the result of an increase incell size [19,27]. The larger leaf area of ethylene-we discuss how the plant hormone ethylene (for

environmental cues. In light of recent developments,

reversible response can be observed within 15 min afterthe start of ethylene treatment [20]; rapid inhibition ofhypothesis that integrates growth inhibition andgrowth stimulation into one biphasic ethylene responsemodel. Focusing on photosynthesis and cell expansion,we highlight several mechanisms through which ethyl-ene affects plant growth, thereby interacting withvarious other signal transduction routes.

Plant growthWhole-plant growth in terms of biomass accumulationresults from the combination of CO2 fixation byphotosynthesis, carbon loss by respiration, and uptakeof minerals [1]. At the cellular level, cell expansion is akey-factor determining organ growth and morphologicaladjustments that optimize growth in response toRonald Pierik1*, Danny Tholen1,2*, Hendrikand Laurentius A.C.J. Voesenek1

1Plant Ecophysiology, Institute of Environmental Biology, Utrec2Present address: Department of Biology, Graduate School of S560-0043, Japan3Department of Experimental Plant Ecology, Institute for Water a1, 6525 ED Nijmegen, The Netherlands

The gaseous plant hormone ethylene modulates manyinternal processes and growth responses to environ-mental stimuli. Ethylene has long been recognized as agrowth inhibitor, but evidence is accumulating thatethylene can also promote growth. Therefore, theconcept of ethylene as a general growth inhibitorneeds reconsideration: a close examination of recentThe Janus face of eplants as the most pronounced example [9].Biomass accumulation, expressed as relative growth

rate, of ethylene-insensitive genotypes differs remarkablylittle, if at all, from wild-type growth rates under near-optimal growth conditions [10] (Figure 1a). However,ethylene-insensitive plants can have severely reducedgrowth rates when, for example, competing for light indense canopies (Box 2 [1018]; Figure 1b). To understandthe opposing data on growth control by ethylene, wewill discuss several examples of negative and positiveethylene effects and integrate them in a model forethylene responsiveness.

Growth inhibitionThe severe reduction of hypocotyl elongation in dark-grown seedlings has proven a useful trait to identifyethylene-insensitive mutants in Arabidopsis [8,19]. Thishylene: growthlationoorter1, Eric J.W. Visser3

niversity, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlandsnce, Osaka University, 1-1 Machikaneyama, Toyonaka, Osaka,

Wetland Science, Radboud University Nijmegen, Toernooiveld

In Arabidopsis, this response consists of a thickenedhypocotyl, inhibition of hypocotyl and root elongation, andexaggerated apical hook formation [5,8] (Figure 1e).However, there are an increasing number of reportsshowing ethylene-induced stimulation of growth, withtype could result from the slightly extended leaf expansionperiod that was observed in ethylene-insensitive mutants

* These authors contributed equally to this article.Available online 10 March 2006

www.sciencedirect.com 1360-1385/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2006.02.006insensitive Arabidopsis mutants compared with wild

Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 177Box 1. Ethylene biosynthesis, perception and signal

transduction

Figure I schematically represents ethylene biosynthesis, perceptionand signal transduction, finally leading to the regulation ofethylene-responsive gene expression. Ethylene is produced frommethionine (Met): the conversion of S-adenosyl-methionine (SAM)to 1-aminocyclopropane-1-carboxylic acid (ACC) is the first dedi-cated step, which is facilitated by a family of ACC synthases (ACS)[2]. This conversion is regarded as rate-limiting in ethylenebiosynthesis; detailed information on when and where ethyleneis produced has recently come to light from GUS reporter studieson the family of ACS genes in Arabidopsis [4]. ACC is thenconverted into ethylene by ACC oxidase [2]. The ethylene produced[28]. This would mean that the difference in leaf areabetween ethylene sensitive and insensitive plants mightonly become apparent in fully expanded leaves ratherthan in those still growing. However, such size differencesmust be interpreted cautiously because ethylene can, forexample, easily accumulate when plants are grown inclosed tissue-culture containers, which can significantlyinhibit leaf expansion of wild-type plants [10]. Analternative explanation for the reported increased leafsize of ethylene-insensitive plants might be an increase inthe cell expansion rates. Unfortunately, no detailedmeasurements of cell-elongation rates in leaves ofethylene-insensitive plants are available to date, therefore

is perceived by a family of ethylene-binding receptors (includingETR1) that show strong sequence similarity to bacterial two-component histidine (His) kinases and which are located in theendoplasmic reticulum [5]. Upon ethylene binding, these receptorsare inactivated and can therefore not activate the protein kinaseCTR1 (constitutive triple response) anymore. As a result, therepression of the membrane protein EIN2 (ethylene insensitive)by CTR1 is relieved. The resulting activation of EIN2 in thepresence of ethylene stabilizes the EIN3 (and tentatively the EIN3-like EIL family) transcription factor, which brings ethylene signaltransduction into the nucleus. Regulation of EIN3 abundanceoccurs through modulation of the SCF complex-mediated ubiqui-tination of this protein, involving the two ethylene-specific F-boxproteins EBF1 and EBF2, allowing targeted breakdown of the EIN3protein [3,5]. EIN3 regulates among others the transcription ofseveral members of the EREBP family of transcription factors,including ERF1 and EDF1 to EDF4, and, as a result, the transcriptionof numerous ethylene-related genes is regulated [5].

TRENDS in Plant Science

EIN2

EIN3, EIL

ACC oxidase

ACC synthase

ACC

SAM

Ethylene

CTR1

EBF1/2

MET

Ethylene-responsive

genes

ERS1, ERS2, ETR1, ETR2, EIN4

ERF1, EDF1/4

Figure I. Scheme representing key events in ethylene signaling and production.

www.sciencedirect.comthe precise effect of endogenous ethylene on cell expansionin leaves remains uncertain.

Growth stimulationInhibition of hypocotyl growth in response to ethylene isnotuniversal anddepends onexternal conditions: althoughhypocotyl elongation can be inhibited in dark-grownseedlings, it is stimulated by ethylene in Arabidopsisseedlings grown in the light [29]. To increase complexityeven further, this growth stimulation is more pronouncedin seedlings grown in conditions where nutrient avail-ability is low compared with those grown in nutrient-richconditions [29]. Light quality can also affect the response toethylene: ethylene-induced stem elongation in tobacco(Figure 1d) is stronger in light with a low red:far-redratio than in light with a high red:far-red ratio [15]. A closeexamination of the literature shows that leaf, stemand rootelongation can all be positively affected by ethylene, butmostly only at relatively low concentrations of the hormone(typically below 0.1 ml lK1). These growth-stimulatoryeffects of ethylene have been reported for a wide varietyof species, such as tobacco [12], wheat (Triticum aestivum)[30], and Arabidopsis [29]. Other species display growth-stimulation at high ethylene concentrations, ratherthan the low concentrations mentioned above. Thesespecies typically occur in frequently flooded habitats,where shoot elongation can re-establish contactwith the atmosphere, and include rice (Oryza sativa)[31] and Rumex palustris [32], as well as O20 other,less-intensively investigated, wetland species (reviewedin [9]).

Biphasic modelTo explain the differential responses to ethylene, wepropose a biphasic model based on earlier suggestions[33,34], with low levels of ethylene promoting and highlevels inhibiting growth (Figure 2). We hypothesize thatthe exact range of ethylene concentrations that areneeded to stimulate or inhibit growth in plants are theintegrative result of environmental conditions, internalsignals (e.g. hormones) and species-specific character-istics tentatively related to selection pressure in theirhabitat of origin. For example, in aquatic and semi-aquatic species, high endogenous ethylene concen-trations are reached during submergence (up to10 ml lK1 [35]). The ethylene doseresponse relationshipin these species shows a growth stimulatory phaseextending well into the high ethylene concentrationrange (up to 10 ml lK1 or more; Figure 2e). Anotherextreme in such a biphasic model would representplants that display growth inhibition at all ethyleneconcentrations applied and where the growth-stimu-latory phase has perhaps become too small to benoticeable (e.g. Figure 2b). We hypothesize thatethylene doseresponse curves for many species willbe positioned somewhere between these two extremes,displaying the two phases (Figure 2a). This has, forexample, been shown for leaf growth rates of twoPoa species [21], primary leaf area in Helianthus

annuus [34], stem elongation in a Stellaria longipesecotype [36], root elongation in rice [33], and coleoptile

Opinion TRENDS in Plant Science Vol.11 No.4 April 2006178Ethylene sensitive Ethylene insensitive

Arabidopsis

Nicotiana

(a)length of a wheat cultivar [30] (Figure 2d). Onclose inspection, this biphasic pattern can in somecases even be observed for a component of thetriple response: hypocotyl elongation in etiolated Arabi-dopsis seedlings [37,38] (Figure 2c). Less-extreme caseswith growth stimulation at low ethylene concentrationsand a lack of stimulation at higher ethylene concen-trations were reported recently for petiole [15] andstem elongation [12] in tobacco. Obviously, growthstimulation by ethylene will mostly be foundonly when relatively low, physiologically relevant,ethylene concentrations are applied. In many publishedexperiments, this is not the case, particularlywhen the ethylene precursor ACC or the ethylene-

(c)

(f)

0

Air Ethylene

(e) Air Ethylene

Petunia

Figure 1. Effects of ethylene insensitivity and ethylene application on plant morphology.

(tobacco) and Petunia are similar in size to their equally aged wild-type counterparts

Ref. [10]). (b) When grown together with their wild-type counterpart (tall, green individ

artificially highlighted in purple) are severely suppressed (modified, with permission,

Arabidopsis (Col-0) showing hyponastic growth after ethylene exposure (5 ml lK1) for 24

plants (5 days at 0.2 ml lK1 ethylene). (e) Dark-grown Rumex palustris seedlings showin

reduced hypocotyl elongation, increased radial swelling and exaggerated apical hook for

ethylene concentrations in older tobacco plants.

www.sciencedirect.com(b)releasing compound ethephon are used, whichgive relatively uncontrolled and high ethylene concen-trations. We expect that for most terrestrialspecies, these concentrations will be in thegrowth-inhibiting phase of the ethylene biphasicresponse curve.

A mechanistic understanding of this biphasic ethyl-ene response concept is yet to emerge. However, acareful consideration of the various physiological pro-cesses through which ethylene affects growth can serveas a first step to understand and guide the much-needed research into the mechanistic basis of theopposing effects of ethylene on plant growth. We will,therefore, discuss (i) the role of ethylene in modulating

0.1 0.5 1.0 4.0

Ethylene

(d) Air Ethylene

(a) Ethylene-insensitive (mutant or transgenic) genotypes of Arabidopsis, Nicotiana

when grown under near-optimal conditions (reproduced, with permission, from

uals) under strong competitive pressure, ethylene-insensitive plants (two of them

from Ref. [12]). (cf) Effects of exogenous ethylene on several plant species. (c)

h. (d) Ethylene-induced hyponasty and stem elongation in relatively young tobacco

g the triple response (7 days on MS plates in the dark with or without 20 mM ACC):

mation. (f) Dose-dependency for shoot elongation after 7-days exposure to different

de

ptiesatht wtiolingcomnopn orogingose

E

stan

Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 179Figure I. Ethylene promotes shade avoidance in canopies. Plant growth in denseBox 2. Ethylene involvement in the optimization of growth in

The low endogenous ethylene levels in plants growing under near-oethylene-sensitive and ethylene-insensitive genotypes of several speciwhen conditions are less optimal, a functional ethylene perception ptobacco plants suffer severe growth reduction when competing for lighenhances elongation growth and amore-vertical, hyponastic leaf orientapalustris [16] and Arabidopsis [17]. Furthermore, intact ethylene signaspectral quality caused by nearby neighbors in tobacco [14], which is acresponses help to place the photosynthesizing leaves higher in the caplants growing in dense stands can be further enhanced by reallocatiolight-exposed leaves higher in the canopy [13]. This re-allocation of nitrelatively mature leaves [11,28]. Thus, ethylene stimulates the positioninvestment of photosynthetic resource in those relatively light-expdense canopies.photosynthesis, (ii) how ethylene affects cell expansionand (iii) interactions of ethylene with other growth-regulating hormones.

Ethylene and carbon gainOne of the factors determining whole-plant growth iscarbon gain through photosynthesis. A well-establishedmechanism that controls photosynthetic activity and geneexpression is the down-regulation of Calvin-cycle enzymesby carbohydrate end-products [39]. Abscisic acid (ABA)has been identified as an important signaling componentin this feedback mechanism [4042]. In addition, ethylenecan also influence the sensitivity of a plant to sugar:ethylene-insensitive plants are more sensitive to endo-genous glucose, whereas application of an ethyleneprecursor decreases the sensitivity of a plant to glucose[41,43]. This interaction also works the other way aroundbecause glucose can negatively affect the stability of theEIN3 protein, thereby reducing the sensitivity of a plant toethylene [44]. The increased glucose-sensitivity can resultin increased carbohydrate suppression of photosynthesisin ethylene-insensitive plants. Indeed, ethylene-insensi-tive Arabidopsis and tobacco both show a reduced rate ofphotosynthesis per unit area [10]. Moreover, young, non-senescent leaves of the Arabidopsis etr1-1 mutant have alower in vitro carboxylation rate than wild-type leaves [28]and the photosynthetic capacity is also reduced in thismutant [45]. Similar results were found in tobacco wherethe lower carboxylation capacity of an ethylene-

hyponastic leaf movement. These shade-avoidance responses are stimulated by ethyle

of nitrogen from older, senescing leaves to younger, more active leaves. This process

www.sciencedirect.comnse canopies

mal conditions probably have only mild effects on growth becausehave comparable growth rates under those conditions [10]. However,way can be vital for plant growth. For example, ethylene-insensitiveith wild-type neighbors [12]. In wild-type tobacco, exogenous ethylenen [12], which shows similarity to ethylene-induced responses in Rumexstimulates these shade-avoidance responses to changes in the lightpanied by enhanced ethylene production rates [15]. Shade-avoidancey where light conditions are most favorable [18]. Photosynthesis byf photosynthetic resources from older, shaded leaves to these young,en is caused by senescence, which can also be induced by ethylene inof young leaves in favorable light conditions and can also stimulated leaves (Figure I), which can further facilitate photosynthesis in

TRENDS in Plant Science

N

thylene

ds is enhanced by shade-avoidance responses, including petiole elongation andinsensitive genotype correlates with decreased Rubiscocontent (D. Tholen, unpublished). We suggest thatincreased sugar sensitivity could contribute to the reducedphotosynthetic capacity in ethylene-insensitive plants,although this might also be related to reduced nitrogenallocation to younger leaves resulting from the delayedsenescence described for the Arabidopsis etr1-1 mutant[28] (Box 2). Interestingly, endogenous glucose concen-trations can be positively correlated with ethyleneproduction in rice, and external sugar application in thisspecies significantly stimulates ethylene production [46].It has, therefore, been hypothesized that increasedethylene production might be central in promoting growthunder circumstances where leaf glucose concentrationsare high, such as in rice plants growing in elevatedatmospheric CO2 levels [47]. These results indicate thatalthough ethylene is generally associated with the break-down of the photosynthetic machinery in the process ofsenescence [6], it might also help maintain a higher rate ofphotosynthesis at elevated endogenous glucose levels.

As well as affecting carboxylation capacity, ethylenecan also alter the rate of photosynthesis by affectingthe diffusion rate of CO2 from the atmosphere to theintercellular cavities. Ethylene-insensitive Arabidopsisetr1 mutants have a smaller stomatal aperture than dowild-type plants [48]. Furthermore, short-term ethyleneexposure results in increased stomatal conductance inPopulus tremuloides seedlings [49]. A study on Brassicajuncea confirmed that enhanced stomatal conductance at a

ne [12,14]. Ethylene can also stimulate senescence, which involves a reallocation

improves whole-plant carbon gain in dense stands [13].

Opinion TRENDS in Plant Science Vol.11 No.4 April 2006180(a)

l)

200range of ethylene concentrations stimulated photosynthesis[50], but high ethylene concentrations reduced stomatalconductance in this species [50], as well as in Glycine max[51],whichreduced the rate ofphotosynthesis.Theseresultssuggest that the effect of ethylene on stomatal conductanceis concentration dependent [50], and might follow thebiphasic response model (Figure 2a).

707580859095

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lll

Figure 2. Ethylene biphasic response model. The biphasic ethylene response model su

(a) Hypothetical doseresponse curves might be shifted along the x-axis because of env

IIV show variation in ethylene doseresponse relationships, which are illustrated in (be

set at 5!10K3 ml lK1 ethylene as the ambient ethylene concentration, but this control co

from the air. (b) Root elongation in cucumber (reproduced, with permission, from Ref.

permission, from Ref. [37]). (d) Coleoptile length in the wheat HongMangMai cultivar (re

(reproduced, with permission, from Ref. [32]).

www.sciencedirect.comEthylene and growth at the cellular levelPlant growth at the cellular level requires a coordinatedbalance of cell expansion and cell division. The best-knowngrowth-inhibiting effect of high ethylene concentrations isthe triple response of dark-grown seedlings, which isthought to result from a reduction of cell expansion inresponse to ethylene in Arabidopsis [5]. Most other

Arabidopsis

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103 102 101 100 101Ethylene (l l1)

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ggests dose-dependency of growth inhibition and growth stimulation by ethylene.

ironmental conditions, species-specific characteristics and internal signals. Curves

)with examples of published data on different species and traits. Control values are

ncentration was even lower in (c) and (d) as ethylene was experimentally removed

[23]). (c) Hypocotyl length in dark-grown Arabidopsis seedlings (reproduced, with

produced, with permission, from Ref. [30]). (e) Petiole elongation in Rumex palustris

Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 181ethylene-mediated growth responses also occur at the cellexpansion level, although ethylene can affect cell divisionas well [52].

Cell expansion is driven by turgor pressure anddepends on cell wall extensibility, which can be regulatedby cell wall-modifying proteins such as expansins [53].Ethylene-inducibility has been shown for expansins indifferent systems, including banana fruit (MaEXP1 [54]),abscising Sambucus nigra leaves (SniEXP2 and SniEXP4[55]), elongating rachises of the semi-aquatic fernRegnellidium diphyllum (RdEXP1 [56]), and elongatingshoots of submerged Rumex palustris (RpEXPA1 [57]) andrice (OsEXPB [58]). Furthermore, ethylene was recentlyshown to induce apoplastic acidification in Rumexpalustris [57], which would help to increase cell wallextensibility because expansins are active at low pH [53].

In roots, ethylene inhibits elongation but stimulatesradial swelling, tentatively improving the mechanicalstrength of roots in resistant soil [59]. This has beenassociated with a change in the directional orientation ofmicrofibrils and microtubules [60]. In normally elongatingroot cells, these are in a transverse orientation andethylene treatment changes this into a longitudinal orrandom orientation [61]. However, inhibition of cellelongation appears to take place earlier than thefinalization of the microtubule reorientation process,suggesting that the reorientation might not be theprimary cause of altered growth [61].

Interactions of ethylene with other hormonesAs discussed above, ethylene-mediated growth adjust-ments mainly take place at the cell expansion level, atleast partly by modifying cell wall extensibility. This canresult from interactions with other hormones includingABA, gibberellic acid (GA) and auxin, which will bediscussed below.

Abscisic acidWhen plants are drought-stressed, the reduced turgorpressure tends to slow down cell elongation. To maintainroot growth under such conditions, enhanced cell wallloosening is required. Accumulation of ABA in drought-stressed plants prevents excessive ethylene production,which would normally inhibit root growth [62,63].Alternatively, ethylene can affect ABA levels. ABAconcentrations in Arabidopsis etr1 and ein2 ethylene-insensitive mutants [63,64] and in ethylene-insensitivetransgenic tobacco (D. Tholen, unpublished) are higherthan in wild-type plants. This is consistent with increasedtranscript levels of the ABA biosynthesis gene ZEP1 inein2 and suggests that the absence of a functionalethylene signal-transduction pathway stimulates ABAbiosynthesis [64,65]. The increased ABA levels in ethyl-ene-insensitive plants might be responsible for theobserved increase in sugar sensitivity [41]. Alternatively,sugars can also promote ABA biosynthesis [65], and thehigh ABA concentration might therefore also result fromincreased sugar sensitivity in ethylene-insensitive plants.High ethylene concentrations in submerged Rumex

palustris and deep-water rice lead to strong growthenhancement, which has been functionally associated

www.sciencedirect.comwith a rapid decrease in endogenous ABA levels [31,66].Rumex acetosa, a species from rarely flooded habitats,does not show this reduction of endogenous ABA or anincrease in petiole elongation under high ethyleneconcentrations [66]. It would be interesting to know iflower ethylene concentrations in this species might down-regulate endogenous ABA levels and subsequently stimu-late petiole elongation.

Gibberellic acidA decrease in ethylene-induced endogenous ABA inR. palustris is required to reach increased bioactive GAlevels [66,67]. In addition, GA responsiveness is increasedby ethylene in this species as well as in submerged rice[31], and the resulting increased GA action allowsethylene-induced shoot elongation. A similar ethylene-GA interaction could also be involved in phytochrome-mediated stem elongation in tobacco [15]. The preciseidentity of this interaction is unknown but might occur ina downstream part of the GA signal transduction routewhere targeted breakdown of the growth-inhibitingDELLA proteins regulates cell elongation. The stabilityof DELLA proteins is not only affected by GA but also byethylene, as was shown during ethylene-induced growthinhibition in dark-grown Arabidopsis seedlings [68],providing a molecular point of crosstalk between thetwo hormones.

AuxinDELLA protein stability is also controlled by auxin [69], ahormone that frequently interacts with ethylene responses.Indeed, Arabidopsis apical hook formation in etiolatedseedlings involves auxin and ethylene [70], as well as GAand the DELLA proteins [68]. Ethylene and auxin also bothregulate low nutrient-induced lateral root formation [71].Interactions between these two hormones have beendescribed for root hair growth [72], adventitious rootformation [73] and root elongation [74]. Ethylene andauxin interactively stimulate hypocotyl elongation in thelight [75], petiole elongation during submergence [76] andphototropism [77]. This implies tight interactions betweenethylene and auxin transport, signaling and/or biosyn-thesis. Indeed, ethylene can affect auxin distribution in theArabidopsis apical hook [70] and in gravistimulated maize(Zea mays) roots [78] to facilitate tropic responses. Recentdata suggest that ethylene can affect auxin biosynthesis inroots [38]. Vice-versa, it is well known that auxin stimulatesethylenebiosynthesis [6] throughtranscriptional regulationof several ACC-SYNTHASE (ACS) genes [4].

ConclusionsSince the discovery of the first ethylene-insensitivemutant in Arabidopsis, considerable progress has beenmade in identifying the ethylene perception pathway andin unraveling the extensive interactions between ethyleneand other plant hormones. We have integrated thisknowledge to enhance our understanding of how ethyleneaffects whole-plant growth. In contrast to manyother plant hormones, ethylene is not indispensable for

whole-plant growth under favorable conditions. Ethyleneis better seen as playing a more-subtle role in

that regulate the stimulatory part of the curve are

Opinion TRENDS in Plant Science Vol.11 No.4 April 2006182growth-inhibitory concentration. Such genome-wide geneexpression studies would be a step forward towardsunraveling signal transduction components specificallyinvolved in the stimulatory and inhibitory phases ofethylene responses.

AcknowledgementsWe thank Ton Peeters, Robert Vreeburg and Liesje Mommer forhelpful comments on a draft of this manuscript. We acknowledgesupport by the Dutch Science Foundation [PIONIER grant no.80074470 (L.A.C.J.V.), grant no. 80533463 (D.T.) and grant no.80533464 (R.P.)].

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The Janus face of ethylene: growth inhibition and stimulationPlant growthStimulation versus inhibition of growthGrowth inhibitionGrowth stimulationBiphasic model

Ethylene and carbon gainEthylene and growth at the cellular levelInteractions of ethylene with other hormonesAbscisic acidGibberellic acidAuxin

ConclusionsPerspectivesAcknowledgementsReferences