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Environmental and Experimental Botany 40 (1998) 197–207
Comparison of the physiological responses of Phaseolus 6ulgaris
and Vigna unguiculata cultivars when submitted to drought
conditions
Maria H. Cruz de Carvalho *, Daniel Laffray, Philippe Louguet
Laboratoire de Physiologie Ve´ge´tale,Uni6ersite´ Paris Val de Marne,A6enue du Ge´ne´ral De Gaulle,
94010
Cre´teil,France
Received 24 January 1998; received in revised form 26 May 1998; accepted 27 May 1998
Abstract
Three cultivars differing in their susceptibility to water stress were compared—Phaseolus 6ulgaris cv. Carioca
(susceptible), Vigna unguiculata cv. IT83D (intermediately tolerant) and V.unguiculata cv. EPACE-1 (tolerant)—dur-
ing an imposed water stress treatment. Variation in leaf gas exchange (i.e. assimilation and stomatal conductance) and
leaf relative water content in response to progressive substrate water depletion were investigated. To verify the extent
of the injury caused by the drought treatment, leaf gas exchange was measured after rehydration. In the three
cultivars, stomatal conductance declined before leaf relative water content was affected. P.6ulgaris showed the largest
decrease in the rate of stomatal conductance with decreasing substrate water content compared to both V.unguiculata
cultivars. Photosynthetic assimilation rates were largely dependent on stomatal aperture, but there was evidence of the
participation of non-stomatal factors in the reduction of CO
2
fixation. The response of leaf gas exchange parameters
to severe water stress conditions differed significantly between P.6ulgaris and V.unguiculata cultivars. After
rehydration, cultivars can be characterised according to the degree of injury induced by the drought treatment: V.
unguiculata cv. EPACE-1 as the least affected, V.unguiculata cv. IT83D slightly affected and P.6ulgaris cv. Carioca
strongly affected. Similar ranking was obtained with experiments previously performed at a cellular and subcellular
level. Our results confirm the utility of physiological parameters as early screening tools for drought resistance in bean
cultivars. © 1998 Elsevier Science B.V. All rights reserved.
Keywords
:
Drought; Net assimilation rate; Pennisetum americanum;Phaseolus 6ulgaris ; Stomatal conductance; Vigna
unguiculata
1. Introduction
Drought is an important factor limiting yield of
large seeded legumes such as beans, which are
widely used around the world as food crops
(Adams et al., 1985; Rachie, 1985). Screening for
drought resistant bean cultivars and the under-
Abbre6iations
:
A, assimilation rate; g
s
, stomatal conduc-
tance; RWC, relative water content; C
wp
, leaf pre-dawn water
potential.
* Corresponding author. Present address: Laboratoire de
Biochimie et Physiologie de l’Adaptation Ve´ge´tale, Universite´
Paris 7, case 7019, 2 place Jussieu, 75251 Paris cedex 05,
France. Tel.: +33 1 44273617; E-mail: cruzdeca@ccr.jussieu.fr
S0098-8472/98/$ - see front matter © 1998 Elsevier Science B.V. All rights reserved.
PII
S0098-8472(98)00037-9
M.H.Cruz de Car6alho et al.
/
En6ironmental and Experimental Botany
40 (1998) 197–207
198
standing of the mechanisms underlying this re-
sistance are of extreme importance in order to
improve the production of such food crops.
The resistance of plants to drought stress de-
pends on two main types of adaptations,
drought avoidance and drought tolerance, which
include whole plant mechanisms that provide
the plant the ability to respond and survive
drought (Shantz, 1927; Maximov, 1929; Vieira
da Silva, 1970; Levitt, 1980; Laffray and
Louguet, 1990). Different plant responses in-
duced by drought should reflect the different
adaptations, or even the lack of them.
While physiological data concerning the re-
sponses to drought of some cultivars of Phaseo-
lus 6ulgaris and Vigna unguiculata are available
(Turk et al., 1980; Parson and Howe, 1984;
Markhart, 1985; Kuppers et al., 1988), this
study provides the first comparative analysis of
sensitive and tolerant cultivars of these species.
A similar approach has been successfully used
with other crops (Kramer, 1969; Ludlow and
Muchow, 1990; Chaves, 1991; Reppelin et al.,
1997).
Among these bean cultivars (genus Phaseolus
and Vigna), differences in parameters such as
membrane integrity and protein content during
and after water stress have been previously ob-
served (Pham-Thi et al., 1990; Zuily-Fodil et al.,
1990a,b) and have been shown to be correlated
to their protoplasmic tolerance to drought
(Vasquez-Tello et al., 1990; Zuily-Fodil et al.,
1990a,b; Roy-Macauley et al., 1992). Although
such works have highlighted the potential for
selection of drought tolerant bean cultivars, as
far as we know, no relationship has yet been
made between drought tolerance at the cellular
and subcellular levels and at the whole plant
level.
The aim of this study was to detect differ-
ences between the physiological response of
these cultivars to drought, that could be linked
to the differences already found at the cellular
and subcellular level and therefore to test if
physiological parameters can be successfully
used for early screening of drought tolerant cul-
tivars of these legumes.
The underlying hypotheses of our work were
that: (1) P.6ulgaris, being the more susceptible
plant to drought, should have rapid stomata
closure and a decrease in assimilation rate; and,
conversely, (2) V.unguiculata cultivars should
maintain stomatal conductance even at lower
substrate moisture, sustaining photosynthesis
and consequently allowing better yield. To test
these hypotheses, we investigated the variations
in leaf gas exchange (i.e. net assimilation rate
and stomatal conductance) and leaf relative wa-
ter content in response to progressive soil water
depletion. According to Srivasta and Strasser
(1996), plant productivity seems to depend pri-
marily on the rate of CO
2
assimilation, so we
also studied the effect of hydraulic signals such
as variation in the leaf relative water content
(Kramer, 1969, 1988) on the rate of photosyn-
thetic carbon assimilation during drought. Fur-
thermore, to verify the extent of the injury
caused by the drought treatment, leaf gas ex-
changes were measured after rehydration.
2. Materials and methods
2.1.
Plant material,culture conditions and water
stress treatment
Experiments were performed with two culti-
vars of V.unguiculata L. (cv. EPACE-1 and cv.
IT83D from Brazil and Nigeria, respectively)
and one cultivar of P.6ulgaris L. (cv. Carioca
from Brazil).
Seeds were germinated on wet filter paper in
Petri dishes maintained at 25°C in the dark. Af-
ter 2 or 3 days, seedlings with well developed
roots and having approximately the same mor-
phological aspect were selected and cultivated in
5 l containers (one plant per container), in a
mixture of fertilised peat (TKS2
®
instant,
Floragard, UK) and sand, in a phytotron under
a photon flux density of 600 mmol photon m
−2
s
−1
at leaf level and 16 h daylight (Lamp Power
OSRAM HQI-E, 400 W). The temperature was
22– 24°C (day) and 18 – 20°C (night) and relative
humidity varied between 30 and 50%. Plants
were watered twice a week. According to the
manufacturer, mineral elements added to the
M.H.Cruz de Car6alho et al.
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En6ironmental and Experimental Botany
40 (1998) 197–207
199
peat covered the nutrient requirements for ap-
proximately 2 months so no nutrient solution
was given to the plants. After 30 days of growth,
water deficiency was started by withholding wa-
ter. The substrate surface of the containers was
covered with aluminium foil to prevent substrate
water loss by evaporation. The experiment was
replicated on five to seven plants for each culti-
var, which were analysed serially.
2.2.
Substrate characteristics
The peat/sand mixture retained much water
and allowed progressive drought establishment.
In a preliminary study, we determined a relation-
ship between substrate water content and leaf
predawn water potential, with the assumption
that the latter is identical in the substrate and in
the plant (Richter, 1997). We used Pearl millet as
a test plant due to (1) fast development of the
plants, and (2) high number of leaves allowing
daily determination of predawn leaf water poten-
tial. P.6ulgaris and V.unguiculata cultivar plants
that are 30 days old have a reduced number of
leaves and thus permit only a few measurements.
Seeds of Pearl millet (Pennisetum americanum,
(L.) Lecke) were sown on a peat and sand sub-
strate mixture (1:1, on a volume basis) in 5 l
containers and under the same experimental con-
ditions as described for P.6ulgaris and V.un-
guiculata cultivar plants. Predawn leaf water
potential (C
wp
) as well as the water content of
the substrate mixture was measured daily during
the stress treatment. Substrate water content
(H%) was determined by daily weighings. Maxi-
mum water capacity of the substrate was mea-
sured after overwatering the substrate and
leaving it to drain for 24 h. Daily measurements
of C
wp
of Pearl millet were carried out before the
light period in the phytotron with a Scholander
pressure chamber (PMS-instrument, OR)
(Scholander et al., 1965). With this preliminary
experiment, we intended to obtain a relationship
between the percentage of water available in the
substrate and its water potential supposed to be
equivalent to predawn leaf water potential, al-
lowing non-destructive determination of drought
intensity for legume treatments.
2.3.
Physiological parameters
2.3.1.
Leaf gas exchange
Stomatal conductance to water vapour (g
s
,
mol H
2
Om
−2
s
−1
) and net assimilation rates
(A,mmol CO
2
m
−2
s
−1
), were determined daily
on the first fully expanded leaf using an open-
flow gas exchange system that included two dif-
ferential infrared gas analysers (ADC, 225-MK3,
UK) for CO
2
and water vapour. During mea-
surements, leaf temperature was maintained at
2592°C under a photosynthetic photon flux
density (PPFD) of 600 mmol photon m
−2
s
−1
at leaf level (Osram lamp HMI, 1200 W). Air
containing 37592mmol mol
−1
CO
2
was in-
jected in the system at a flow rate of 0.4 l
min
−1
. Dew point of incoming air was adjusted
so as to maintain the air– leaf water vapour
pressure deficit (VPD) below 21 Pa kPa
−1
in-
side the assimilation chamber. Values of g
s
and
Awere calculated according to Von Caemmerer
and Farquhar (1981), after stabilisation of gas
exchanges within the chamber before measure-
ments.
2.3.2.
Relati6e water content
Relative water content (RWC) was calculated
according to Weatherley (1950). Leaf disks (1.5
cm diameter) were weighed immediately after
punching out (FW) and then placed in a petri
dish containing wet filter paper and kept at 4°C
in the dark. After 24 h, the turgid weight (TW)
was obtained. For the dry weight (DW), leaf
disks were oven dried for 24 h at 90°C and
weighed.
2.4.
Statistical analyses of data
A two phase exponential decay analysis was
performed on the relation between H%/C
wp
so
the substrate water potential could be estimated
from its water content. Linear regressions were
used to test the significance of the differences
between cultivars. All measurements were made
on at least five replicates of each cultivar. Statis-
tical analysis were performed using GraphPad
Prism software (version 1.01, Graphpad, 1994).
M.H.Cruz de Car6alho et al.
/
En6ironmental and Experimental Botany
40 (1998) 197–207
200
Fig. 1. Standard curve of predawn leaf water potential (C
wp
) and substrate water content (H%) obtained by a two phase exponential
decay analysis. Measurements were performed each morning during the water stress treatment, before light was switched on in the
growth chamber, on Pearl millet plants (Pennisetum americanum). The resulting equation was used to convert the H% values to C
wp
.
3. Results
3.1.
Substrate water status
Fig. 1 shows the two phase exponential de-
cay analysis obtained for the relationship be-
tween substrate water content (H%) and leaf
predawn water potential (C
wp
) of Pearl millet.
The resulting mathematical relation between
H% and C
wp
was:
C
wp
=4.640447×exp( −0.003165 ×H)
+14.454609×exp( −0.722301 ×H)
−3.738553 R
2
=0.677
This equation could then be used to estimate
substrate water potential from the H% mea-
sures made during the drought treatment on
the three cultivars (P.6ulgaris cv. Carioca, V.
unguiculata cv. IT83D and V.unguiculata cv.
EPACE-1).
3.2.
Response of stomatal conductance to
substrate water depletion
As substrate water content decreased below
20%, the stomatal conductance (g
s
) decreased
linearly to its minimum value (data not shown).
All cultivars responded in the same way. In or-
Table 1
Mean values of assimilation rates (A) and stomatal conduc-
tance (g
s
) for P.6ulgaris (P.6.) and two cultivars of V.unguic-
ulata (V.u.) in the fully hydrated state
g
s
(mol H
2
OA(mmol CO
2
m
−2
s
−1
)m
−2
s
−1
)
V.u. cv. EPACE-1 0.1590.058.391.9
7.893.0 0.1190.05V.u. cv. IT83D
P.6. cv. Carioca 10.793.6 0.1590.05
Parameters were measured using attached leaves: PPFD, 600
mmol photon m
−2
s
−1
; VPD, B21 Pa kPa
−1
; air CO
2
concen-
tration, 37592mmol mol
−1
. Values are means of measure-
ments made on four to seven independent plants with 9S.D.
M.H.Cruz de Car6alho et al.
/
En6ironmental and Experimental Botany
40 (1998) 197–207
201
Fig. 2. Effect of drought stress (expressed as relative substrate water content H%) when HB20%, on (A) leaf stomatal conductance,
g
s
, and (B) photosynthetic assimilation rate, A,oftheP.6ulgaris and V.unguiculata cultivars. Data is expressed as a percentage of
control. Measuring conditions were PPFD\600 mmol photon m
−2
s
−1
, VPDB21 Pa kPa
−1
, and air CO
2
concentration 37592
mmol mol
−1
.
M.H.Cruz de Car6alho et al.
/
En6ironmental and Experimental Botany
40 (1998) 197–207
202
der to compare better the responses of the three
cultivars, data obtained from HB20% were ex-
pressed as a percentage of the mean correspond-
ing to well hydrated plants (Table 1, Fig. 2A).
Highly significant differences were found between
the responses of P.6ulgaris and the two V.un-
guiculata cultivars (IT83D and EPACE-1) (PB
0.0001). However, differences between the V.
unguiculata cultivars were not significant (P=
0.277). P.6ulgaris showed a higher g
s
decrease
with H%: stomatal closure was achieved at H=
8%, whereas that for the V.unguiculata cultivars
at H=5– 6%.
Fig. 3A shows g
s
variation versus C
wp
. The
stomata of the V.unguiculata cv. EPACE-1 closed
completely at a lower level of C
wp
(−1.04 MPa)
than the cv. IT83-D (C
wp
=−0.91 MPa) and P.
6ulgaris cv. Carioca (C
wp
=−0.85 MPa).
Responses of g
s
to decreasing leaf RWC are
shown in Fig. 4A. In cultivars IT83D and Cari-
oca, g
s
values above approximately 0.15 mol H
2
O
m
−2
s
−1
(corresponding to well watered plants,
Table 1) were scattered over a large range of
RWC values (Fig. 4A). Below 0.15 mol H
2
Om
−2
s
−1
,g
s
and RWC decreased in parallel, as shown
by the significant relationship between them.
Stomata closed at approximately 80% RWC for
IT83-D and 75% RWC for Carioca. In the culti-
var EPACE-1, g
s
reached its minimum without
any significant change in RWC, which remained
between 85 and 90%.
3.3.
Response of net assimilation rate to substrate
water supply
Regarding net assimilation rates for HB20%,
similar results were obtained (Fig. 2B), P.6ulgaris
being significantly different from V.unguiculata
cultivars (P=0.014), but differences between the
two V.unguiculata cultivars being not significant
(P=0.319). As could be foreseen from the g
s
response, P.6ulgaris showed a decline in Ahigher
than the two V.unguiculata cultivars, and the zero
value of Awas obtained for H=9% for P.6ul-
garis and 7– 5% for the V.unguiculata cultivars.
For the two cultivars IT83D and Carioca, A
decreased in parallel with RWC, although for
Carioca, the two parameters were poorly related
(Fig. 4B). In cultivar EPACE-1, net photosyn-
thetic rate decreased without any relationship
with RWC. Table 2 shows the mean values of A
obtained 48 h after rewatering of the drought
stressed plants. The V.unguiculata cultivars recov-
ered to the initial Avalues when fully hydrated,
but P.6ulgaris did not (Table 2).
4. Discussion
In none of the cultivars was the first decline in
stomatal conductance related to variation in leaf
water content, since g
s
values above 0.15 mol H
2
O
m
−2
s
−1
were always scattered over a wide range
of leaf RWC (Fig. 4A). Furthermore, stomatal
closure in the V.unguiculata cultivar EPACE-1
was not related to any change in RWC (Fig. 4A).
These results indicate that early stomatal re-
sponses to substrate water depletion were not
triggered by changes in leaf water content, and
that RWC alone cannot be used as a drought
indicator on these legumes.
This could suggest the existence of a root-to-
leaf communication, independent of the leaf water
status, that informs the shoot about changes in
the root environment, such as increasing substrate
drought. In other species, this phenomenon has
been widely documented (Passioura, 1980; Black-
man and Davies, 1985; Gollan et al., 1986; Davies
et al., 1990; Schurr and Gollan, 1990; Davies and
Zhang, 1991; Tardieu et al., 1992). Abscisic acid
Table 2
Mean values of assimilation rates (A) and stomatal conduc-
tance (g
s
) for P.6ulgaris (P.6.) and two cultivars of V.unguic-
ulata (V.u.) after rewatered for 48 h
g
s
(mol H
2
OA(mmol CO
2
o
m
−2
s
−1
)m
−2
s
−1
)
V.u. cv. EPACE-1 10.391.1 0.1190.08
0.2490.0811.393.2V.u. cv. IT83D
6.993.2 0.1290.03P.6. cv. Carioca
Parameters were measured using attached leaves: FD, 600
mmol photon m
−2
s
−1
; VPD, B21 Pa kPa−
1
; air CO
2
concentration, 37592mmol mol
−1
. Values are means of
measurements made on four to seven independent plants with
9S.D.
M.H.Cruz de Car6alho et al.
/
En6ironmental and Experimental Botany
40 (1998) 197–207
203
Fig. 3. Effect of drought stress (expressed as leaf predawn water potential C
wp
, obtained from H% by Eq. (2)) when HB20%, on
(A) leaf stomatal conductance, g
s
, and (B) photosynthetic assimilation rate, A,oftheP.6ulgaris and V.unguiculata cultivars. Data
is expressed as a percentage of control. Measuring conditions were PPFD\600 mmol m
−2
s
−1
, VPDB21 Pa kPa
−1
, and air CO
2
concentration 37592mmol mol
−1
.
M.H.Cruz de Car6alho et al.
/
En6ironmental and Experimental Botany
40 (1998) 197–207
204
Fig. 4. Stomatal conductance (A) and net assimilation rate (B) versus leaf relative water content (RWC) measured on drought
stressed leaves of P.6ulgaris cv. Carioca and V.unguiculata cv. IT83D and cv. EPACE-1. Measuring conditions were PPFD\600
mmol photon m
−2
s
−1
, VPDB21 Pa kPa
−1
, and air CO
2
concentration 37592mmol mol
−1
.
M.H.Cruz de Car6alho et al.
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En6ironmental and Experimental Botany
40 (1998) 197–207
205
might be a stomatal mediator in these plants as in
many others (Zhang and Davies, 1987; Neales et
al., 1989; Davies et al., 1990; Davies and Zhang,
1991; Ribaut and Pilet, 1991; Blum and Johnson,
1993).
The differences between responses of the three
cultivars were only detected in severe water stress
conditions (when HB20%). However, the relation
A/g
s
between control plants (Table 1) indicate that
both V.unguiculata cultivars are photosynthetically
more efficient than the P.6ulgaris cultivar regard-
ing stomatal conductance. When Hdecreased from
20 to 15%, relative g
s
for the V.unguiculata cv.
EPACE-1 decreased to 50% and that in the cv.
IT83D to 30%, while for the P.6ulgaris it still
remained at 70% (Fig. 2A). It has already been
shown that P.6ulgaris, sensitive to drought, keeps
its stomata open at lower C
wp
than the more
resistant drought avoiding species P.acutifolius
(Parson and Howe, 1984; Markhart, 1985). Never-
theless, P.6ulgaris which showed greater values of
g
s
when compared to V.unguiculata cultivars
(Table 1), also showed a greater rate of reduction
in g
s
(Fig. 2). Complete stomatal closure was
obtained for higher %Hand C
wp
in P.6ulgaris than
in V.unguiculata cultivars (Fig. 2A and Fig. 2B).
These results confirmed that stomatal adjustment
may be a common response in a drought avoidance
adaptation: our results agree with field yields which
have indicated that P.6ulgaris is a more drought
sensitive plant than V.unguiculata (Turk et al.,
1980; Parson and Howe, 1984). Both V.unguiculata
cultivars, IT83D and EPACE-1, showed a better
capacity for stomatal adjustment by maintaining
their stomata partially open as stress increased and
simultaneously a drought avoiding strategy by the
early regulation of stomata aperture.
Stomatal closure is, nonetheless, only one aspect
in the whole response of the plant to drought which
includes also metabolic and morphogenetic pro-
cesses. During water stress, the decline of the CO
2
fixation rate is supposed to depend on a direct
inhibition of photosynthesis (a non-stomatal com-
ponent) and on stomatal closure (the stomatal
component). V.unguiculata cv. EPACE-1 and
IT83D had a lower decrease in their net photosyn-
thetic rates than the P.6ulgaris cultivar Carioca
(Fig. 2B and Fig. 3B). This could be explained
either by the fact that they maintained their stom-
ata slightly opened when substrate dehydration was
severe, or because their photosynthetic activity was
less affected than in P.6ulgaris. Our results indi-
cated that the photosynthetic activity ceased in V.
unguiculata cultivar IT83D and P.6ulgaris cultivar
Carioca when their stomata were still opened, while
the V.unguiculata cultivar EPACE-1 maintained its
photosynthetic activity even at negligible stomatal
aperture (Fig. 2B). Calculation of internal CO
2
concentration (C
i
) during the drought treatment
are not given here because of probable non-uniform
stomatal closure (known as patchiness), which
usually leads to an over-estimation of C
i
values
under ambient CO
2
concentration (Downton et al.,
1988; Chaves, 1991).
To investigate the extent to which photosynthesis
was coupled to stomatal response, Awas plotted
versus g
s
. Reduction in g
s
induced a decline in A
for all three cultivars (Fig. 5). Even if g
s
affects A
(Fig. 5), it is not sure that a causal relationship
exists, although several authors think so (Kuppers
et al., 1988; Laffray and Louguet, 1990; Chaves,
1991; Chaves and Pereira, 1992). Therefore, by
preventing dehydration, stomatal closure is also the
prominent factor responsible for the reduction in
the assimilation rates of CO
2
, as generally accepted.
On the other hand, Avalues obtained after
rehydration clearly indicate that the damage in the
photosynthetic apparatus caused by drought was
very pronounced in the case of the P.6ulgaris
cultivar (Table 2), indicating the existence of non-
stomatal factors limiting photosynthetic activity
during drought. Lower levels of Afor both V.
unguiculata cultivars during stress were due to
stomatal closure, hence indicating a mechanism of
drought avoidance simultaneously to drought
tolerance.
Our results showed that the hypotheses initially
proposed have been verified: P.6ulgaris, being the
more sensitive to drought, had a more rapid
stomata closure and a decrease in the assimilation
rate during drought when compared to the more
resistant V.unguiculata cultivars, which controlled
stomatal adjustment and therefore sustained pho-
tosynthesis longer. Our results also correlate well
with the differences previously found for these
M.H.Cruz de Car6alho et al.
/
En6ironmental and Experimental Botany
40 (1998) 197–207
206
Fig. 5. Net assimilation rate versus leaf diffusive conductance,
measured on drought stressed leaves of P.6ulgaris cv. Carioca
and V.unguiculata cv. IT83D and cv. EPACE-1. Measuring
conditions were PPFD\600 mmol photon m
−2
s
−1
, VPDB21
Pa kPa
−
1, and air CO
2
concentration 37592mmol mol
−1
.
bean cultivars at cellular and subcellular levels.
This work enabled us to further understand the
physiological response to water stress of these
legumes and to demonstrate that Aand g
s
mea-
sured during and after a water stress treatment
seem to be reliable physiological parameters to be
used in early screening for tolerant bean cultivars.
Acknowledgements
The authors wish to thank L. Espindola-Dar-
venne for her help with the measurements of leaf
gas exchange. Gratitude is due to Prof. Vieira da
Silva and J. Cardoso-Vilhena for critical discus-
sion and help. This work was supported by a
grant from the ‘Centre d’Etude Re´gional pour
l’Ame´lioration de l’Adaptation a`laSe´cheresse’-
CERAAS, Bambey– Se´ne´gal (Program STD3-UE-
D6 XII).
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