Comparative effects of auxin transport inhibitors

Transcription

Tree Physiology 23, 785–791
© 2003 Heron Publishing—Victoria, Canada
Comparative effects of auxin transport inhibitors on rhizogenesis and
mycorrhizal establishment of spruce seedlings inoculated with
Laccaria bicolor
ANA RINCÓN,1 OUTI PRIHA,1 BRUNO SOTTA,2 MAGDA BONNET 2 and FRANÇOIS LE
TACON 1,3
1
Unité Mixte de Recherches Interactions Arbres-Microorganismes, INRA Centre de Nancy, 54280 Champenoux, France
2
UMR de Physiologie Cellulaire et Moléculaire des Plantes, CNRS et Université PARIS VI, 4 place Jussieu, Tour 53, 75005 Paris, France
3
Author to whom correspondence should be addressed ([email protected])
Received April 10, 2002; accepted January 11, 2003; published online July 1, 2003
Summary We compared the effects of two auxin transport
inhibitors (2,3,5-triiodobenzoic acid (TIBA) and 1-N-naphthylphthalamic acid (NPA)) on rhizogenesis and mycorrhizal
establishment of Picea abies L. (Karst.) seedlings inoculated
with Laccaria bicolor S238N (Maire) Orton. Inoculation of
seedlings with L. bicolor under in vitro conditions strongly increased host root and shoot growth. Although TIBA had no effect on taproot growth, NPA decreased taproot growth and
deformed the root apex into a globular shape in both non-inoculated seedlings and seedlings inoculated with L. bicolor. Inoculation with L. bicolor strongly increased lateral rhizogenesis
of the seedlings, and application of 100 µM indole-3-acetic
acid (IAA) partially reproduced this effect. Although TIBA
completely inhibited the stimulatory effect of L. bicolor on lateral root formation, NPA inhibited it only partially. Both TIBA
and NPA counteracted the effect of exogenous IAA on lateral
rhizogenesis. Inoculation with L. bicolor significantly increased shoot growth and seedling dry biomass, whereas application of exogenous IAA had no effect on either parameter.
There was no effect of NPA on shoot growth and biomass production. The presence of TIBA completely prevented the development of ectomycorrhizal structures (mantle and Hartig
net). In the presence of NPA, the number of seedlings colonized by the fungus was reduced and the degree of development of ectomycorrhizal structures was variable, but not
completely prevented. In medium lacking tryptophan, neither
TIBA nor NPA inhibited the release of IAA produced by
L. bicolor in pure culture. When 100 µM tryptophan was added
to the medium, TIBA significantly increased the amount of
IAA released by the fungus, whereas NPA had no significant
effect. We conclude that fungal IAA plays an important role in
plant rhizogenesis and in the establishment of ectomycorrhizal
symbiosis.
Keywords: ectomycorrhizas, NPA, TIBA.
Introduction
Auxin, one of the most widely studied phytohormones, is involved in important developmental processes such as cell
elongation, cell division, differentiation of vascular tissues and
lateral root formation (Lomax et al. 1995). Lateral roots initiate from founder cells in the pericycle, the layer surrounding
the vascular cylinder of the root. In response to stimulation by
an auxinic signal, these cells undergo dedifferentiation and
proliferate to form the lateral root primordium (Goldsmith
1993, Reed et al. 1998). Transport of auxin is polar from the
sites of synthesis in the shoot tips toward the roots (Lomax et
al. 1995). Although auxin transport in roots is less clear, two
directions of transport have been reported: an auxin flow in the
central cylinder toward the root apex (acropetal transport) and
an opposite flow in the epidermal and cortical cells to the
root–shoot junction (basipetal transport) (Jones 1998). Auxin
influx into the cells takes place by proton motive force,
whereas auxin efflux is mediated by a complex auxin carrier
comprising at least two polypeptides (Morris et al. 1991,
Palme and Gälweiler 1999) and localized at the basal end of
the plasma membrane (Swarup et al. 2000, Parry et al. 2001).
This auxin transport system has been demonstrated by using
auxin antagonists that interfere with the influx mechanisms
(Parry et al. 2001) and by using auxin transport inhibitors
(2,3,5-triiodobenzoic acid (TIBA) and 1-N-naphthylphthalamic acid (NPA)) that interfere with the action of the efflux
carriers (Estelle 2001). The existence of a lateral indole-3-acetic acid (IAA) transport system, proposed by Epel et al. (1992),
has been confirmed recently by Friml et al. (2002), who have
identified the auxin transport regulator PIN3 as a component
of the lateral IAA transport system in Arabidopsis roots.
Auxin transport inhibitors can also affect other plasma-membrane proteins (H+-ATPase and a syntaxin) as well as membrane-trafficking processes (Geldner et al. 2001, Rashotte et
al. 2001). Although these so-called specific inhibitors of auxin
efflux appear to have a broader action on membrane trafficking than previously thought, they continue to be used to study
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RINCÓN, PRIHA, SOTTA, BONNET AND LE TACON
how ectomycorrhizal fungal auxin is involved in lateral rhizogenesis and in ectomycorrhizal establishment.
Because most ectomycorrhizal fungi synthesize and excrete
auxin (Ulrich 1960, Ek et al. 1983, Frankenberger and Poth
1987, Gay et al. 1989), it has been assumed that they influence
plant root morphology, particularly through the stimulation of
lateral root formation. Several authors have demonstrated that
auxin and ethylene induce the formation of ectomycorrhizallike structures in Pinus species (Rupp and Mudge 1985, Gruhn
et al. 1992, Kaska et al. 1999). Furthermore, fungal auxin
probably plays an important role as a signaling molecule in the
formation of typical ectomycorrhizal structures (mantle and
Hartig net). Gay et al. (1994, 1995) showed that auxin overproducing mutants of Hebeloma cylindrosporum increased
mycorrhizal activity and formed a multi-seriated Hartig net on
Pinus pinaster Ait. roots. On the other hand, Hampp et al.
(1996) showed that ectomycorrhizas formed in vitro by aspen
seedlings that over-expressed bacterial auxin synthesis genes
did not differ from those formed by wild plants. Based on the
finding that an auxin transport inhibitor (TIBA) blocks mantle
and Hartig net formation in different ectomycorrhizal associations, it has been suggested that fungal auxin transport has a
significant role in ectomycorrhizal establishment (KarabaghliDegron et al. 1998, Rincón et al. 2001, Niemi et al. 2002). Together, these results indicate the important role of fungal auxin
delivery and transport in the host root in the establishment of
ectomycorrhizas (Barker and Tagu 2000).
Our objective was to determine the effect of another auxin
transport inhibitor, 1-N-naphthylphthalamic acid (NPA), on
Picea abies L. (Karst.) growth and mycorrhizal colonization
by the fungus Laccaria bicolor S238N (Maire) Orton. The
effect of NPA was compared to that of TIBA in an attempt to
elucidate the role of fungal auxin on host development and
ectomycorrhizal establishment.
Materials and methods
Biological material
Picea abies seeds were surface disinfected by shaking for
35 min in 30% (v/v) H2O2 and rinsed in several changes of
sterile distilled water. Disinfected seeds were germinated in
15% (w/v) water–agar medium at 25 °C in the dark.
Strain S238N of L. bicolor was cultured on Pachlewski agar
medium (P5) at 25 °C (Pachlewski and Pachlewska 1974).
Four weeks before inoculation, plugs of actively growing
mycelium collected from the edges of the colonies were transferred individually to fresh P5 medium covered by a cellophane sheet.
Seedling culture and inoculation
Once germinated, P. abies seedlings (2–3 cm root length)
were transferred to petri dishes (14-cm diameter) containing
60 ml of Shemakhanova medium (Shemakhanova 1962, modified by Duponnois and Garbaye (1991)) covered by a cellophane sheet. Roots were covered with a damp filter paper to
avoid desiccation, and two cotton rolls were put in each petri
dish to prevent water accumulation. In all experiments, seedlings were grown in a climate chamber with a 16-h photoperiod of 50 W m –2 and a day/night temperature of 20/24 °C.
The bottom half of each petri dish was wrapped in aluminum
foil to protect roots from direct light. Seedlings were inoculated with a 4-week-old L. bicolor S238N colony that was
placed in direct contact with the taproot.
Application of auxin transport inhibitors (ATIs) and
experimental designs
Effects of NPA and TIBA on the development of non-inoculated P. abies seedlings and seedlings inoculated with
L. bicolor S238N were studied in two experiments. Experiment 1, which lasted 7 weeks, consisted of four treatments: (1)
non-inoculated control; (2) control + NPA; (3) L. bicolor
S238N; and (4) L. bicolor S238N + NPA. In Experiment 2,
which lasted 6 weeks, effects of TIBA and NPA were compared only on inoculated P. abies seedlings. There were three
treatments: (1) L. bicolor S238N; (2) L. bicolor S238N +
TIBA; and (3) L. bicolor S238N + NPA. In both experiments, a
minimum of 25 replicates was analyzed per treatment.
The TIBA and NPA were dissolved in absolute ethanol
(0.02 and 0.01 M, respectively) and added to sterilized culture
medium to obtain a final concentration of 10 µM. Control
treatments received the same volume of absolute ethanol
without inhibitor.
In both experiments, taproot length, number of lateral roots,
lateral root elongation, epicotyl length and number of needles
of the seedlings were measured weekly. At the end of the experiments, the number of mycorrhizas formed was assessed
with a stereomicroscope, and seedling root and shoot dry
masses were determined. In treatments inoculated with
L. bicolor (with or without ATI), mantle and Hartig net development was determined by light microscopy studies of a root
segment (3–4 mm long) sampled in the elongation zone of the
taproot. A minimum of 10 root samples was studied per treatment. Root segments were embedded in EPON resin and
semi-thin sections (0.4 µm) were contrasted with toluidine
blue before microscopic observation.
To mimic the effect of the fungus and determine whether
IAA counteracted the effect of NPA, we conducted an experiment with the following treatments: (1) control; (2) control +
NPA; (3) L. bicolor; (4) L. bicolor + NPA; (5) exogenous IAA;
and (6) IAA + NPA. Each treatment had 25 replicates.
The IAA was dissolved in absolute ethanol (0.2 M) and
added to the autoclaved medium to obtain a final concentration
of 100 µM. All control treatments received the same volume of
absolute ethanol without inhibitor. Chemicals were purchased
from Sigma-Aldrich (St. Louis, MO).
Taproot length, number of lateral roots, epicotyl length and
number of needles of the seedlings were measured weekly
during the 6-week experiment. At the end of the experiment,
seedling root and shoot dry masses were determined.
Measurement of IAA production by L. bicolor S238 N in the
presence of ATIs and tryptophan
Four-week-old colonies of L. bicolor S238 N were floated on
TREE PHYSIOLOGY VOLUME 23, 2003
AUXIN TRANSPORT INHIBITORS AND MYCORRHIZAS
787
the surface of 15 ml of Shemakanova liquid medium placed in
85-mm diameter petri dishes in the presence and absence of
10 µM TIBA or NPA and with and without 100 µM tryptophan.
The control media without inhibitors were supplemented with
0.5 ml l –1 of absolute ethanol. The fungal cultures, four per
treatment, were incubated in darkness at 25 °C for 3 weeks and
then analyzed for IAA and pH.
Samples were filter-sterilized and stored at –30 °C. After
tritiated IAA was added to estimate recovery rate, samples
were purified by reverse-phase HPLC (0.2% (v/v) formic
acid:methanol gradient) and methylated with diazomethane.
They were then subjected to ELISA using specific antibodies
as described by Julliard et al. (1992). The competition step was
performed at 4 °C for 12 h with polyclonal anti-IAA rabbit antiserum obtained as described by Maldiney et al. (1986). After
washing, anti-hormone antibodies bound to the wells of the
microtitration plates were labeled with goat anti-rabbit immunoglobulin peroxidase reagent, and 0.5 mg ml –1 of 2,2′-azinobis (3-ethylbenzothiazoline-6-sulfonic acid) (Sigma-Aldrich)
was added in perborate buffer (pH 4.6) as an enzyme substrate.
The coloration resulting from the enzymatic reaction was
measured spectrophotometrically at 405 nm. Calculations
were made by referring to a calibration curve established for
each microtitration plate with a curvilinear regression of magnitude four obtained from the mean of four standard curves.
There were five replicates per sample of medium. Results were
expressed in pmol ml –1 of medium.
Statistical analysis
Data were analyzed by one-way ANOVA and differences
among treatments were separated by Bonferroni’s test (P =
0.05).
Figure 1. Effects of Laccaria bicolor S238N inoculation and 1-Nnaphthylphthalamic acid (NPA) application on Picea abies seedlings
during 7 weeks of growth: (A) taproot elongation and (B) mean number of lateral roots per seedling. At each time, means with the same
letter were not significantly different according to the Bonferroni test
(P = 0.05). Symbols: 䉬 = control; 䊏 = control + NPA; 䉱 = L. bicolor;
and × = L. bicolor + NPA.
Results
Effects of L. bicolor S238N on seedling development
Seedlings inoculated with L. bicolor showed significantly
slower taproot growth than non-inoculated seedlings, but there
were no significant fungal effects on taproot length at the end
of the experiment (Figure 1A). Seedlings inoculated with
L. bicolor had more lateral roots than non-inoculated seedlings
(Figure 1B), and this effect became significant 2 weeks after
inoculation. At the end of the experiment, seedling shoot
growth and dry biomass were significantly increased by
L. bicolor (data not shown).
Effects of NPA on seedling development
Application of NPA significantly reduced taproot length of
non-inoculated seedlings (Figure 1A) and the root apex was
deformed into a globular shape. The NPA treatment had no
significant effect on the number of lateral roots produced by
non-inoculated seedlings (Figure 1B). Inoculation with L. bicolor S238N attenuated the deformation of the root apex in
NPA-treated seedlings, but did not entirely prevent it. The
stimulatory effects of the fungus on taproot elongation and lateral root formation were significantly decreased by NPA (Fig-
ures 1A and 1B). In seedlings inoculated with L. bicolor, 30%
of the lateral roots formed were less than 2 mm in length, 50%
were between 2 and 5 mm long, 10% were between 0.5 and
1 cm long and 10% were longer than 1 cm (data not shown).
Elongation of lateral roots of seedlings in the L. bicolor + NPA
treatment was inhibited, so that all lateral roots were less than
2 mm long. Moreover, most of the lateral roots formed in seedlings in the L. bicolor + NPA treatment were distributed in
clusters along the main root in the zones colonized by the fungus (Figure 2). Application of NPA had no significant effect on
shoot growth of non-inoculated seedlings, but it slightly reduced the stimulatory effect of the fungus on shoot growth
(data not shown). Seedling dry biomass was unaffected by
NPA.
Effects of exogenous IAA and NPA application on seedling
development
Similar to the effect produced by L. bicolor, exogenous application of 100 µM IAA significantly slowed taproot growth
during the first 3 weeks, but no significant treatment differences were detected at the end of the experiment (Figure 3A).
Exogenous IAA significantly increased the number of lateral
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
788
Figure 3. Effects of Laccaria bicolor S238N inoculation, exogenous
indole-3-acetic acid (IAA, 100 µM) and 1-N-naphthylphthalamic acid
(NPA, 10 µM) application on Picea abies root development after 6
weeks of growth. (A) Taproot length and (B) mean number of lateral
roots per seedling. Means with the same letter were not significantly
different according to the Bonferroni test (P = 0.05). Bars indicate
standard errors of the means.
among seedlings. In some cases, the mantle and the Hartig net
were overdeveloped, whereas other seedlings showed only an
incipient mantle (Figure 4).
Figure 2. Distribution pattern of lateral roots and mycorrhizas of
Picea abies seedlings inoculated with Laccaria bicolor S238N in the
absence (A) and presence (B) of 1-N-naphthylphthalamic acid. Asterisks denote the mycelium of L. bicolor.
roots, but not as much as the fungus (Figure 3B). Exogenous
IAA did not increase epicotyl length or shoot or root biomass,
whereas L. bicolor increased all of these parameters (data not
shown). The NPA treatment significantly reduced taproot
length of seedlings in all treatments (Figure 3A), and significantly inhibited the stimulation of lateral root production due
to IAA or L. bicolor (Figures 3A and 3B). Proportionally, the
decrease was significantly lower in inoculated seedlings than
in non-inoculated seedlings.
Effects of NPA on mycorrhizal formation
In our in vitro system, the taproot cortex of inoculated P. abies
seedlings was colonized by L. bicolor S238N with a well-developed mantle and Hartig net. At the end of the experiment,
all inoculated seedlings were mycorrhizal, but in the presence
of NPA, the number of mycorrhizal seedlings was reduced to
39%. The percentages of mycorrhizal lateral roots in seedlings
in the L. bicolor and L. bicolor + NPA treatments were 56 and
35%, respectively. In the L. bicolor + NPA treatment, great
variability in mantle and Hartig net development was observed
Comparison of effects of TIBA and NPA on the development
of inoculated seedlings
After 6 weeks of growth, the taproot cortex of inoculated control seedlings was colonized by L. bicolor S238N with a
well-developed mantle and Hartig net. Application of TIBA
completely inhibited Hartig net formation and mantle development. In contrast, some inoculated seedlings treated with
NPA showed well-developed ectomycorrhizal structures after
5 weeks of growth (Figure 4).
Although TIBA had no effect on taproot length, NPA
slightly decreased taproot length, resulting in a deformed root
apex. The number of lateral roots was decreased more by
TIBA than by NPA (Figure 5). Application of TIBA or NPA
slightly reduced shoot growth, whereas seedling root and
shoot dry masses were unaffected (data not shown).
Production of IAA by pure cultures of L. bicolor in the
presence of ATIs and tryptophan
In medium lacking tryptophan, the amount of IAA released by
the fungus into the medium was unaffected by TIBA or NPA
(Figure 6). When 100 µM tryptophan was added to the culture
medium, the release of IAA by the fungus increased 100-fold
(Figure 6). In medium containing 100 µM tryptophan, NPA
had no significant effect on fungal IAA excretion, whereas
TIBA significantly increased it.
789
Figure 4. Colonization of Picea abies
taproot by Laccaria bicolor S238N for
(A) control seedlings inoculated with
L. bicolor, (B) seedlings inoculated
with L. bicolor + 2,3,5-triiodobenzoic
acid and (C–F) seedlings inoculated
with L. bicolor +1-N-naphthylphthalamic acid. Abbreviations: Cc = cortical
cells; rh = root hair; m = mantle; and
Hn = Hartig net. Arrows point to isolated hyphae (20×).
Figure 5. Effects of 2,3,5-triiodobenzoic acid (TIBA) and 1-N-naphthylphthalamic acid (NPA) on the mean number of lateral roots produced by Picea abies seedlings inoculated with Laccaria bicolor
S238N during 6 weeks of growth. Means with the same letter were not
significantly different according to the Bonferroni test (P = 0.05).
Symbols: 䉬 = L. bicolor; 䊏 = L. bicolor + TIBA; and 䉱 = L. bicolor +
NPA.
Discussion
Inoculation of P. abies seedlings with L. bicolor S238N under
in vitro conditions greatly increased host root and shoot
growth. Although TIBA had no effect on taproot length, NPA
decreased it and usually deformed the root apex into a globular
shape. Similar root apex deformation has been described
for Arabidopsis roots grown on medium containing NPA
(Ruegger et al. 1997, Mattson et al. 1999). The NPA may alter
the structure of the root apex by inhibiting IAA basipetal transport (Casimiro et al. 2001) and modifying the IAA distribution
gradient in the root (Mattson et al. 1999, Berleth et al. 2000).
We observed an effect of NPA on root apex deformation in
non-inoculated as well as inoculated seedlings, implying that
NPA affects the distribution of endogenous auxin in P. abies
seedlings.
Shoot growth and biomass accumulation were significantly
increased in seedings inoculated with L. bicolor S238N. Exogenous IAA did not reproduce this fungal effect, whereas NPA
slightly affected shoot growth but not biomass production.
These results indicate that the fungal-induced growth enhancement of the host is related mainly to nutritional processes.
Inoculation of seedlings with L. bicolor S238N strongly increased lateral rhizogenesis, as previously described by
Karabaghli-Degron et al. (1998). These authors also showed
that the presence of 100 µM IAA in the culture medium partially reproduced the effect of L. bicolor on lateral root formation. We confirmed that TIBA inhibited this fungal-induced
stimulation of lateral root formation. Similar to TIBA, NPA
counteracted the stimulatory effect of exogenous IAA on lat-
790
Figure 6. Effects of 2,3,5-triiodobenzoic acid (TIBA) and 1-N-naphthylphthalamic acid (NPA) on the production (nM) of indole-3-acetic
acid (IAA) by pure cultures of Laccaria bicolor S238N in the absence
(A) and presence (B) of 100 µM tryptophan. Means with the same letter were not significantly different according to the Bonferroni test
(P = 0.05). Bars indicate standard errors of the means.
eral root production. The NPA, however, only partially inhibited the fungal-induced stimulation of seedling rhizogenesis.
Some lateral roots were formed in the presence of NPA, but
they were organized in clusters along the taproot and their
elongation was inhibited. Casimiro et al. (2001) showed that,
in Arabidopsis roots, NPA did not affect acropetal transport,
but inhibited basipetal transport. Reed et al. (1998) suggested
that only acropetal auxin transport was involved in lateral root
formation. In our experiments, reorganization of the sites
where lateral roots were initiated indicates that NPA could disturb the auxin concentration gradient in the root. We speculate
that the presence of NPA blocks auxin transport, causing accumulation of IAA at sites in the root close to the central cylinder
and subsequent local division of several pericycle cells, leading to lateral root initiation in the area. Furthermore, the
NPA-induced increase in IAA concentration in the zone of
root initiation could prevent the later elongation of lateral
roots.
The addition of ATIs did not significantly affect the release
of IAA by pure cultures of L. bicolor. When tryptophan, a
precursor of IAA synthesis, was added to the medium, the
presence of TIBA significantly increased the amount of IAA
produced by the fungus, whereas NPA had no effect. Fungal
IAA could be released by passive diffusion or by a carrier-mediated process. Because passive diffusion is unlikely to occur
on account of the difference in pH between the fungal cytoplasm (neutral) and the exocellular medium (~3 at the end of
the experiment) (Gay 1986), we hypothesize that the release of
fungal IAA is mediated by a carrier. However, this hypothetical carrier was unaffected by TIBA and NPA. Because neither
TIBA nor NPA inhibited the release of fungal IAA, and TIBA
actually stimulated it, the effects of these ATIs may be restricted to the transport of fungal IAA to the seedling root. Our
results suggest that, without an additional source of auxin provided by the fungus, the host cannot transport enough auxin to
the roots to allow the differentiation of pericycle cells and subsequent lateral root initiation. Fungal auxin has to be transported by a lateral pathway through the plant root cortex
toward the vascular tissues. Once in the central cylinder, fungal auxin could be incorporated into the acropetal IAA stream
responsible for lateral root formation (Reed et al. 1998) or
could reach the target cells directly. Application of TIBA or
NPA significantly reduced the stimulatory effect of the fungus
on plant rhizogenesis. Similar to TIBA (Karabaghli-Degron et
al. 1998), NPA neutralized the stimulatory effect of exogenous
IAA on lateral root production. These results support the hypothesis that fungal IAA is actively transported through the
root cortex.
As reported by Niemi et al. (2002), the formation of ectomycorrhizal structures (mantle and Hartig net) was completely
prevented by TIBA. In the presence of NPA, the number of
seedlings colonized by fungus and the percentage of mycorrhizas were greatly reduced. The degree of development of
ectomycorrhizal structures was variable, but not completely
prevented by NPA. In several samples, mantle and Hartig net
were overdeveloped, perhaps indicating a localized accumulation of IAA (Gay et al. 1994) in response to NPA, which disturbs the auxin concentration gradient. Geldner et al. (2001)
showed that auxin transport inhibitors affected other plasmamembrane proteins. So we cannot exclude the possibility that
TIBA and NPA had other effects on rhizogenesis and mycorrhizal establishment besides inhibiting IAA transport and
modifying the IAA gradient. For example, these compounds
may inhibit the production of elicitors from the host toward the
fungus. Rincón et al. (2001) showed that the presence of the
host increased the production of fungal polysaccharidic fibrils,
allowing hyphal aggregation and attachment to the roots.
Treatment with TIBA inhibited this host effect and the plant–
fungus recognition process leading to ectomycorrhizal formation. We hypothesize that TIBA inhibited plasma-membrane
proteins responsible for the production of host elicitors
allowing fungal attachment to the root, whereas NPA did not at
the concentration used.
The differential effects of TIBA and NPA on the stimulatory
effect of the fungal partner on host lateral root formation and
mycorrhizal development could be useful in the investigation
of ectomycorrhizal establishment and lateral transport of IAA.
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Comparative effects of auxin transport inhibitors

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