The Janus face of ethylene: growth

inhibition and stimulation

Ronald Pierik
1*
, Danny Tholen
1,2*
, Hendrik Poorter
1
, Eric J.W. Visser
3
and Laurentius A.C.J. Voesenek
1
1
Plant Ecophysiology, Institute of Environmental Biology, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands
2
Present address: Department of Biology, Graduate School of Science, Osaka University, 1-1 Machikaneyama, Toyonaka, Osaka,
560-0043, Japan
3
Department of Experimental Plant Ecology, Institute for Water and Wetland Science, Radboud University Nijmegen, Toernooiveld
1, 6525 ED Nijmegen, The Netherlands
The gaseous plant hormone ethylene modulates many
internal processes and growth responses to environ-
mental stimuli. Ethylene has long been recognized as a
growth inhibitor, but evidence is accumulating that
ethylene can also promote growth. Therefore, the
concept of ethylene as a general growth inhibitor
needs reconsideration: a close examination of recent
literature can help to understand the two contrasting
faces of growth control by ethylene. Here, we propose a
hypothesis that integrates growth inhibition and
growth stimulation into one biphasic ethylene response
model. Focusing on photosynthesis and cell expansion,
we highlight several mechanisms through which ethyl-
ene affects plant growth, thereby interacting with
various other signal transduction routes.
Plant growth
Whole-plant growth in terms of biomass accumulation
results from the combination of CO
2
xation by
photosynthesis, carbon loss by respiration, and uptake
of minerals [1]. At the cellular level, cell expansion is a
key-factor determining organ growth and morphological
adjustments that optimize growth in response to
environmental cues. In light of recent developments,
we discuss how the plant hormone ethylene (for
biosynthesis and signaling components, see Box 1 [2
5]) can affect both cell expansion and the rate of
photosynthesis. These processes control growth rates
and growth responses to internal and environmental
signals. Understanding the complex interplay between
ethylene signaling and other signal transduction path-
ways should help us to understand the processes through
which ethylene can exert its, sometimes opposing, effects
on whole-plant growth.
Stimulation versus inhibition of growth
Ethylene is generally considered growth inhibitory [6],
with the triple response of dark-grown seedlings, rst
discovered in Pisum sativum [7], as the classical example.
In Arabidopsis, this response consists of a thickened
hypocotyl, inhibition of hypocotyl and root elongation, and
exaggerated apical hook formation [5,8] (Figure 1e).
However, there are an increasing number of reports
showing ethylene-induced stimulation of growth, with
the strongly enhanced shoot elongation of semi-aquatic
plants as the most pronounced example [9].
Biomass accumulation, expressed as relative growth
rate, of ethylene-insensitive genotypes differs remarkably
little, if at all, from wild-type growth rates under near-
optimal growth conditions [10] (Figure 1a). However,
ethylene-insensitive plants can have severely reduced
growth rates when, for example, competing for light in
dense canopies (Box 2 [1018]; Figure 1b). To understand
the opposing data on growth control by ethylene, we
will discuss several examples of negative and positive
ethylene effects and integrate them in a model for
ethylene responsiveness.
Growth inhibition
The severe reduction of hypocotyl elongation in dark-
grown seedlings has proven a useful trait to identify
ethylene-insensitive mutants in Arabidopsis [8,19]. This
reversible response can be observed within 15 min after
the start of ethylene treatment [20]; rapid inhibition of
elongation was also reported for leaves of Poa species [21],
Rumex palustris roots [22] and roots of Cucumis sativus
[23]. Stems and petioles can show similar growth-
inhibitory responses to ethylene [24]. In accordance with
this, ethylene overproduction reduces internode length in
transgenic tobacco (Nicotiana tabacum) [25] and overall
stature in the eto1 Arabidopsis mutant [8]. Furthermore,
the Arabidopsis constitutive ethylene signaling mutant
ctr1 is signicantly dwarfed with unexpanded leaves and
a greatly reduced cell size [26]. By contrast, ethylene-
insensitive mutants (e.g. etr1-1 and ers1) were reported to
be considerably larger than wild-type plants [19,27], even
in the absence of exogenous ethylene treatment. The
larger leaf area is thought to be the result of an increase in
cell size [19,27]. The larger leaf area of ethylene-
insensitive Arabidopsis mutants compared with wild
type could result fromthe slightly extended leaf expansion
period that was observed in ethylene-insensitive mutants
Corresponding author: Voesenek, L.A.C.J. (l.a.c.j.voesenek@bio.uu.nl).
* These authors contributed equally to this article.
Available online 10 March 2006
Opinion TRENDS in Plant Science Vol.11 No.4 April 2006
www.sciencedirect.com 1360-1385/$ - see front matter Q 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2006.02.006
[28]. This would mean that the difference in leaf area
between ethylene sensitive and insensitive plants might
only become apparent in fully expanded leaves rather
than in those still growing. However, such size differences
must be interpreted cautiously because ethylene can, for
example, easily accumulate when plants are grown in
closed tissue-culture containers, which can signicantly
inhibit leaf expansion of wild-type plants [10]. An
alternative explanation for the reported increased leaf
size of ethylene-insensitive plants might be an increase in
the cell expansion rates. Unfortunately, no detailed
measurements of cell-elongation rates in leaves of
ethylene-insensitive plants are available to date, therefore
the precise effect of endogenous ethylene on cell expansion
in leaves remains uncertain.
Growth stimulation
Inhibition of hypocotyl growth in response to ethylene is
not universal anddepends onexternal conditions: although
hypocotyl elongation can be inhibited in dark-grown
seedlings, it is stimulated by ethylene in Arabidopsis
seedlings grown in the light [29]. To increase complexity
even further, this growth stimulation is more pronounced
in seedlings grown in conditions where nutrient avail-
ability is low compared with those grown in nutrient-rich
conditions [29]. Light quality canalso affect the response to
ethylene: ethylene-induced stem elongation in tobacco
(Figure 1d) is stronger in light with a low red:far-red
ratio than in light with a high red:far-red ratio [15]. Aclose
examinationof the literature shows that leaf, stemandroot
elongation can all be positively affected by ethylene, but
mostly only at relatively lowconcentrations of the hormone
(typically below 0.1 ml l
K1
). These growth-stimulatory
effects of ethylene have been reported for a wide variety
of species, such as tobacco [12], wheat (Triticum aestivum)
[30], and Arabidopsis [29]. Other species display growth-
stimulation at high ethylene concentrations, rather
than the low concentrations mentioned above. These
species typically occur in frequently ooded habitats,
where shoot elongation can re-establish contact
with the atmosphere, and include rice (Oryza sativa)
[31] and Rumex palustris [32], as well as O20 other,
less-intensively investigated, wetland species (reviewed
in [9]).
Biphasic model
To explain the differential responses to ethylene, we
propose a biphasic model based on earlier suggestions
[33,34], with low levels of ethylene promoting and high
levels inhibiting growth (Figure 2). We hypothesize that
the exact range of ethylene concentrations that are
needed to stimulate or inhibit growth in plants are the
integrative result of environmental conditions, internal
signals (e.g. hormones) and species-specic character-
istics tentatively related to selection pressure in their
habitat of origin. For example, in aquatic and semi-
aquatic species, high endogenous ethylene concen-
trations are reached during submergence (up to
10 ml l
K1
[35]). The ethylene doseresponse relationship
in these species shows a growth stimulatory phase
extending well into the high ethylene concentration
range (up to 10 ml l
K1
or more; Figure 2e). Another
extreme in such a biphasic model would represent
plants that display growth inhibition at all ethylene
concentrations applied and where the growth-stimu-
latory phase has perhaps become too small to be
noticeable (e.g. Figure 2b). We hypothesize that
ethylene doseresponse curves for many species will
be positioned somewhere between these two extremes,
displaying the two phases (Figure 2a). This has, for
example, been shown for leaf growth rates of two
Poa species [21], primary leaf area in Helianthus
annuus [34], stem elongation in a Stellaria longipes
ecotype [36], root elongation in rice [33], and coleoptile
Box 1. Ethylene biosynthesis, perception and signal
transduction
Figure I schematically represents ethylene biosynthesis, perception
and signal transduction, nally leading to the regulation of
ethylene-responsive gene expression. Ethylene is produced from
methionine (Met): the conversion of S-adenosyl-methionine (SAM)
to 1-aminocyclopropane-1-carboxylic acid (ACC) is the rst dedi-
cated step, which is facilitated by a family of ACC synthases (ACS)
[2]. This conversion is regarded as rate-limiting in ethylene
biosynthesis; detailed information on when and where ethylene
is produced has recently come to light from GUS reporter studies
on the family of ACS genes in Arabidopsis [4]. ACC is then
converted into ethylene by ACC oxidase [2]. The ethylene produced
is perceived by a family of ethylene-binding receptors (including
ETR1) that show strong sequence similarity to bacterial two-
component histidine (His) kinases and which are located in the
endoplasmic reticulum [5]. Upon ethylene binding, these receptors
are inactivated and can therefore not activate the protein kinase
CTR1 (constitutive triple response) anymore. As a result, the
repression of the membrane protein EIN2 (ethylene insensitive)
by CTR1 is relieved. The resulting activation of EIN2 in the
presence of ethylene stabilizes the EIN3 (and tentatively the EIN3-
like EIL family) transcription factor, which brings ethylene signal
transduction into the nucleus. Regulation of EIN3 abundance
occurs through modulation of the SCF complex-mediated ubiqui-
tination of this protein, involving the two ethylene-specic F-box
proteins EBF1 and EBF2, allowing targeted breakdown of the EIN3
protein [3,5]. EIN3 regulates among others the transcription of
several members of the EREBP family of transcription factors,
including ERF1 and EDF1 to EDF4, and, as a result, the transcription
of 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.
Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 177
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length of a wheat cultivar [30] (Figure 2d). On
close inspection, this biphasic pattern can in some
cases even be observed for a component of the
triple response: hypocotyl elongation in etiolated Arabi-
dopsis seedlings [37,38] (Figure 2c). Less-extreme cases
with growth stimulation at low ethylene concentrations
and a lack of stimulation at higher ethylene concen-
trations were reported recently for petiole [15] and
stem elongation [12] in tobacco. Obviously, growth
stimulation by ethylene will mostly be found
only when relatively low, physiologically relevant,
ethylene concentrations are applied. In many published
experiments, this is not the case, particularly
when the ethylene precursor ACC or the ethylene-
releasing compound ethephon are used, which
give relatively uncontrolled and high ethylene concen-
trations. We expect that for most terrestrial
species, these concentrations will be in the
growth-inhibiting phase of the ethylene biphasic
response curve.
A mechanistic understanding of this biphasic ethyl-
ene response concept is yet to emerge. However, a
careful consideration of the various physiological pro-
cesses through which ethylene affects growth can serve
as a rst step to understand and guide the much-
needed research into the mechanistic basis of the
opposing effects of ethylene on plant growth. We will,
therefore, discuss (i) the role of ethylene in modulating
(b)
(c)
(f)
0 0.1
0.5 1.0
4.0
Air Ethylene
Ethylene
(e) Air Ethylene
(d) Air Ethylene
Ethylene sensitive Ethylene insensitive
Arabidopsis
Nicotiana
Petunia
(a)
Figure 1. Effects of ethylene insensitivity and ethylene application on plant morphology. (a) Ethylene-insensitive (mutant or transgenic) genotypes of Arabidopsis, Nicotiana
(tobacco) and Petunia are similar in size to their equally aged wild-type counterparts when grown under near-optimal conditions (reproduced, with permission, from
Ref. [10]). (b) When grown together with their wild-type counterpart (tall, green individuals) under strong competitive pressure, ethylene-insensitive plants (two of them
articially highlighted in purple) are severely suppressed (modied, with permission, from Ref. [12]). (cf) Effects of exogenous ethylene on several plant species. (c)
Arabidopsis (Col-0) showing hyponastic growth after ethylene exposure (5 ml l
K1
) for 24 h. (d) Ethylene-induced hyponasty and stem elongation in relatively young tobacco
plants (5 days at 0.2 ml l
K1
ethylene). (e) Dark-grown Rumex palustris seedlings showing the triple response (7 days on MS plates in the dark with or without 20 mM ACC):
reduced hypocotyl elongation, increased radial swelling and exaggerated apical hook formation. (f) Dose-dependency for shoot elongation after 7-days exposure to different
ethylene concentrations in older tobacco plants.
Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 178
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photosynthesis, (ii) how ethylene affects cell expansion
and (iii) interactions of ethylene with other growth-
regulating hormones.
Ethylene and carbon gain
One of the factors determining whole-plant growth is
carbon gain through photosynthesis. A well-established
mechanism that controls photosynthetic activity and gene
expression is the down-regulation of Calvin-cycle enzymes
by carbohydrate end-products [39]. Abscisic acid (ABA)
has been identied as an important signaling component
in this feedback mechanism [4042]. In addition, ethylene
can also inuence the sensitivity of a plant to sugar:
ethylene-insensitive plants are more sensitive to endo-
genous glucose, whereas application of an ethylene
precursor decreases the sensitivity of a plant to glucose
[41,43]. This interaction also works the other way around
because glucose can negatively affect the stability of the
EIN3 protein, thereby reducing the sensitivity of a plant to
ethylene [44]. The increased glucose-sensitivity can result
in increased carbohydrate suppression of photosynthesis
in ethylene-insensitive plants. Indeed, ethylene-insensi-
tive Arabidopsis and tobacco both show a reduced rate of
photosynthesis per unit area [10]. Moreover, young, non-
senescent leaves of the Arabidopsis etr1-1 mutant have a
lower in vitro carboxylation rate than wild-type leaves [28]
and the photosynthetic capacity is also reduced in this
mutant [45]. Similar results were found in tobacco where
the lower carboxylation capacity of an ethylene-
insensitive genotype correlates with decreased Rubisco
content (D. Tholen, unpublished). We suggest that
increased sugar sensitivity could contribute to the reduced
photosynthetic capacity in ethylene-insensitive plants,
although this might also be related to reduced nitrogen
allocation to younger leaves resulting from the delayed
senescence described for the Arabidopsis etr1-1 mutant
[28] (Box 2). Interestingly, endogenous glucose concen-
trations can be positively correlated with ethylene
production in rice, and external sugar application in this
species signicantly stimulates ethylene production [46].
It has, therefore, been hypothesized that increased
ethylene production might be central in promoting growth
under circumstances where leaf glucose concentrations
are high, such as in rice plants growing in elevated
atmospheric CO
2
levels [47]. These results indicate that
although ethylene is generally associated with the break-
down of the photosynthetic machinery in the process of
senescence [6], it might also help maintain a higher rate of
photosynthesis at elevated endogenous glucose levels.
As well as affecting carboxylation capacity, ethylene
can also alter the rate of photosynthesis by affecting
the diffusion rate of CO
2
from the atmosphere to the
intercellular cavities. Ethylene-insensitive Arabidopsis
etr1 mutants have a smaller stomatal aperture than do
wild-type plants [48]. Furthermore, short-term ethylene
exposure results in increased stomatal conductance in
Populus tremuloides seedlings [49]. A study on Brassica
juncea conrmed that enhanced stomatal conductance at a
Box 2. Ethylene involvement in the optimization of growth in dense canopies
The low endogenous ethylene levels in plants growing under near-optimal conditions probably have only mild effects on growth because
ethylene-sensitive and ethylene-insensitive genotypes of several species have comparable growth rates under those conditions [10]. However,
when conditions are less optimal, a functional ethylene perception pathway can be vital for plant growth. For example, ethylene-insensitive
tobacco plants suffer severe growth reduction when competing for light with wild-type neighbors [12]. In wild-type tobacco, exogenous ethylene
enhances elongation growth and a more-vertical, hyponastic leaf orientation [12], which shows similarity to ethylene-induced responses in Rumex
palustris [16] and Arabidopsis [17]. Furthermore, intact ethylene signaling stimulates these shade-avoidance responses to changes in the light
spectral quality caused by nearby neighbors in tobacco [14], which is accompanied by enhanced ethylene production rates [15]. Shade-avoidance
responses help to place the photosynthesizing leaves higher in the canopy where light conditions are most favorable [18]. Photosynthesis by
plants growing in dense stands can be further enhanced by reallocation of photosynthetic resources from older, shaded leaves to these young,
light-exposed leaves higher in the canopy [13]. This re-allocation of nitrogen is caused by senescence, which can also be induced by ethylene in
relatively mature leaves [11,28]. Thus, ethylene stimulates the positioning of young leaves in favorable light conditions and can also stimulate
investment of photosynthetic resource in those relatively light-exposed leaves (Figure I), which can further facilitate photosynthesis in
dense canopies.
TRENDS in Plant Science
N
Ethylene
Figure I. Ethylene promotes shade avoidance in canopies. Plant growth in dense stands is enhanced by shade-avoidance responses, including petiole elongation and
hyponastic leaf movement. These shade-avoidance responses are stimulated by ethylene [12,14]. Ethylene can also stimulate senescence, which involves a reallocation
of nitrogen from older, senescing leaves to younger, more active leaves. This process improves whole-plant carbon gain in dense stands [13].
Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 179
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range of ethylene concentrations stimulatedphotosynthesis
[50], but high ethylene concentrations reduced stomatal
conductance in this species [50], as well as in Glycine max
[51], whichreducedtherateof photosynthesis. Theseresults
suggest that the effect of ethylene on stomatal conductance
is concentration dependent [50], and might follow the
biphasic response model (Figure 2a).
Ethylene and growth at the cellular level
Plant growth at the cellular level requires a coordinated
balance of cell expansion and cell division. The best-known
growth-inhibiting effect of high ethylene concentrations is
the triple response of dark-grown seedlings, which is
thought to result from a reduction of cell expansion in
response to ethylene in Arabidopsis [5]. Most other
Arabidopsis
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Figure 2. Ethylene biphasic response model. The biphasic ethylene response model suggests dose-dependency of growth inhibition and growth stimulation by ethylene.
(a) Hypothetical doseresponse curves might be shifted along the x-axis because of environmental conditions, species-specic characteristics and internal signals. Curves
IIV show variation in ethylene doseresponse relationships, which are illustrated in (be) with examples of published data on different species and traits. Control values are
set at 5!10
K3
ml l
K1
ethylene as the ambient ethylene concentration, but this control concentration was even lower in (c) and (d) as ethylene was experimentally removed
from the air. (b) Root elongation in cucumber (reproduced, with permission, from Ref. [23]). (c) Hypocotyl length in dark-grown Arabidopsis seedlings (reproduced, with
permission, fromRef. [37]). (d) Coleoptile length in the wheat Hong Mang Mai cultivar (reproduced, with permission, fromRef. [30]). (e) Petiole elongation in Rumex palustris
(reproduced, with permission, from Ref. [32]).
Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 180
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ethylene-mediated growth responses also occur at the cell
expansion level, although ethylene can affect cell division
as well [52].
Cell expansion is driven by turgor pressure and
depends on cell wall extensibility, which can be regulated
by cell wall-modifying proteins such as expansins [53].
Ethylene-inducibility has been shown for expansins in
different systems, including banana fruit (MaEXP1 [54]),
abscising Sambucus nigra leaves (SniEXP2 and SniEXP4
[55]), elongating rachises of the semi-aquatic fern
Regnellidium diphyllum (RdEXP1 [56]), and elongating
shoots of submerged Rumex palustris (RpEXPA1 [57]) and
rice (OsEXPB [58]). Furthermore, ethylene was recently
shown to induce apoplastic acidication in Rumex
palustris [57], which would help to increase cell wall
extensibility because expansins are active at low pH [53].
In roots, ethylene inhibits elongation but stimulates
radial swelling, tentatively improving the mechanical
strength of roots in resistant soil [59]. This has been
associated with a change in the directional orientation of
microbrils and microtubules [60]. In normally elongating
root cells, these are in a transverse orientation and
ethylene treatment changes this into a longitudinal or
random orientation [61]. However, inhibition of cell
elongation appears to take place earlier than the
nalization of the microtubule reorientation process,
suggesting that the reorientation might not be the
primary cause of altered growth [61].
Interactions of ethylene with other hormones
As discussed above, ethylene-mediated growth adjust-
ments mainly take place at the cell expansion level, at
least partly by modifying cell wall extensibility. This can
result from interactions with other hormones including
ABA, gibberellic acid (GA) and auxin, which will be
discussed below.
Abscisic acid
When plants are drought-stressed, the reduced turgor
pressure tends to slow down cell elongation. To maintain
root growth under such conditions, enhanced cell wall
loosening 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. ABA
concentrations in Arabidopsis etr1 and ein2 ethylene-
insensitive mutants [63,64] and in ethylene-insensitive
transgenic tobacco (D. Tholen, unpublished) are higher
than in wild-type plants. This is consistent with increased
transcript levels of the ABA biosynthesis gene ZEP1 in
ein2 and suggests that the absence of a functional
ethylene signal-transduction pathway stimulates ABA
biosynthesis [64,65]. The increased ABA levels in ethyl-
ene-insensitive plants might be responsible for the
observed increase in sugar sensitivity [41]. Alternatively,
sugars can also promote ABA biosynthesis [65], and the
high ABA concentration might therefore also result from
increased sugar sensitivity in ethylene-insensitive plants.
High ethylene concentrations in submerged Rumex
palustris and deep-water rice lead to strong growth
enhancement, which has been functionally associated
with a rapid decrease in endogenous ABA levels [31,66].
Rumex acetosa, a species from rarely ooded habitats,
does not show this reduction of endogenous ABA or an
increase in petiole elongation under high ethylene
concentrations [66]. It would be interesting to know if
lower ethylene concentrations in this species might down-
regulate endogenous ABA levels and subsequently stimu-
late petiole elongation.
Gibberellic acid
A decrease in ethylene-induced endogenous ABA in
R. palustris is required to reach increased bioactive GA
levels [66,67]. In addition, GA responsiveness is increased
by ethylene in this species as well as in submerged rice
[31], and the resulting increased GA action allows
ethylene-induced shoot elongation. A similar ethylene-
GA interaction could also be involved in phytochrome-
mediated stem elongation in tobacco [15]. The precise
identity of this interaction is unknown but might occur in
a downstream part of the GA signal transduction route
where targeted breakdown of the growth-inhibiting
DELLA proteins regulates cell elongation. The stability
of DELLA proteins is not only affected by GA but also by
ethylene, as was shown during ethylene-induced growth
inhibition in dark-grown Arabidopsis seedlings [68],
providing a molecular point of crosstalk between the
two hormones.
Auxin
DELLA protein stability is also controlled by auxin [69], a
hormone that frequently interacts with ethylene responses.
Indeed, Arabidopsis apical hook formation in etiolated
seedlings involves auxin and ethylene [70], as well as GA
and the DELLAproteins [68]. Ethylene and auxin also both
regulate low nutrient-induced lateral root formation [71].
Interactions between these two hormones have been
described for root hair growth [72], adventitious root
formation [73] and root elongation [74]. Ethylene and
auxin interactively stimulate hypocotyl elongation in the
light [75], petiole elongation during submergence [76] and
phototropism [77]. This implies tight interactions between
ethylene and auxin transport, signaling and/or biosyn-
thesis. Indeed, ethylene can affect auxin distribution in the
Arabidopsis apical hook [70] and in gravistimulated maize
(Zea mays) roots [78] to facilitate tropic responses. Recent
data suggest that ethylene can affect auxin biosynthesis in
roots [38]. Vice-versa, it is well knownthat auxinstimulates
ethylenebiosynthesis [6] throughtranscriptional regulation
of several ACC-SYNTHASE (ACS) genes [4].
Conclusions
Since the discovery of the rst ethylene-insensitive
mutant in Arabidopsis, considerable progress has been
made in identifying the ethylene perception pathway and
in unraveling the extensive interactions between ethylene
and other plant hormones. We have integrated this
knowledge to enhance our understanding of how ethylene
affects whole-plant growth. In contrast to many
other plant hormones, ethylene is not indispensable for
whole-plant growth under favorable conditions. Ethylene
is better seen as playing a more-subtle role in
Opinion TRENDS in Plant Science Vol.11 No.4 April 2006 181
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plant growth, particularly in response to stressful
environmental conditions.
Evidence is accumulating that the effect of ethylene
depends on the tissue, concentration and plant species of
interest, as well as on endogenous and environmental
signals. The proposed biphasic ethylene response model
integrates this variety in ethylene responses, but a
mechanistic basis for this diversication remains specu-
lative. It is possible that the signal transduction pathways
that regulate the stimulatory part of the curve are
different to those that regulate the inhibitory part.
Interactions between ethylene and other signal trans-
duction components (e.g. hormones, sugars and cell wall
processes) might occur only within specic ethylene-
concentration windows. For example, the ethylene-
induced reduction of endogenous ABA concentrations,
resulting in enhanced GA action, would be a candidate
mechanism for growth-stimulation by ethylene.
The ethylene concentrations at which this interaction
would occur might differ between species and
environmental conditions.
Perspectives
A species-wide screening of the ethylene concentration-
dependency of plant growth is needed to show to what
extent the biphasic ethylene response model is general.
Such broad knowledge can serve as a background to
formulate and address questions such as how different
ethylene concentrations can have opposite effects on plant
growth and how internal as well as environmental signals
modify ethylene responses at the molecular level. The
different interactions between ethylene and other internal
signals would be candidates for differentiation between
stimulatory and inhibitory effects. It would be useful to
compare gene expression patterns of two groups of plants
(for example, Arabidopsis), one treated with a growth-
stimulatory ethylene concentration and one with a
growth-inhibitory concentration. Such genome-wide gene
expression studies would be a step forward towards
unraveling signal transduction components specically
involved in the stimulatory and inhibitory phases of
ethylene responses.
Acknowledgements
We thank Ton Peeters, Robert Vreeburg and Liesje Mommer for
helpful comments on a draft of this manuscript. We acknowledge
support 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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