Journal of Experimental Botany, Vol. 46, No. 288, pp. 759-765, July 1995
Journal of
Experimental
Botany
Striga hermonthica decreases photosynthesis in Zea
mays through effects on leaf cell structure
Lucy H. Smith 1 ' 3 , Alfred J. Keys1'4 and Michael C.W. Evans2
1
2
Department of Biochemistry and Physiology, IACR - Rothamsted, Harpenden, Hertfordshire AL5 2JQ, UK
Department of Biology, Darwin Building, University College, Gower Street, London WC1E6BT, UK
Abstract
Symptoms exhibited by infected host plants include stunting, wilting, leaf chlorosis, and yield reduction (Doggett,
Maize seedlings were grown in pots either with or
1965; Kim, 1991). Infection decreases internode expanwithout preconditioned seeds of the parasitic weed,
sion and leaf area (Press and Stewart, 1987) and,
Striga hermonthica. After between 4 and 8 weeks, net
depending on the nutritional status, alters the partitioning
photosynthesis in the leaves of maize plants infected
of dry matter within the host (Cechin and Press, 1993).
with Striga decreased compared to leaves of uninfecKim (1991) has reported chlorosis of the leaves of the
ted control plants. The activities of four enzymes of
host plant. All of these symptoms become severe after
photosynthetic metabolism were, however, little affecemergence of the Striga plants above the soil surface.
ted by infection. A pulse-chase experiment using 14 C0 2
From this stage the high rates of transpiration by Striga
showed that C4 acids were the main early products of
(Press et al, 1989) result in competition with the host for
assimilation even when the rate of photosynthesis was
water and probably nutrients.
much decreased by infection, but more radioDrennan and El Hiweris (1979) showed that concentraactivity appeared in glycine and serine than in leaves
tions of growth regulating substances in sorghum were
of healthy maize plants. Leaves of infected maize
altered as a result of infection by Striga hermonthica, but
required longer to reach a steady rate of photosynsuggested this change was a consequence of water stress
thesis upon enclosure in a leaf chamber than leaves
rather than transport of regulators from the parasite.
of uninfected plants after similar treatment.
Musselman (1980) suggested that a toxin produced in the
Electron microscopy of transverse sections of the
parasite and transported to the host may be responsible
leaves of infected maize indicated that the cell walls
for the symptoms observed. Several studies have conin the bundle sheath and vascular tissue were less
firmed the transport of various substances from host to
robust than in leaves of healthy plants. The results
parasite (Okonkwo, 1966; Press et al., 1989; Smith and
suggest that infection with Striga causes an increase
Stewart, 1990), but less has been published concerning
in the permeability of cell walls in the bundle sheath,
transport from parasite to host.
leakage of CO2 from the bundle sheath cells and
Press et al. (1987) reported that when Sorghum bicolor
decreased effectiveness of C4 photosynthesis in host
cv. CSH1 was infected with S. hermonthica, in glasshouse
leaves.
conditions, its rate of photosynthesis decreased. Clark
et al. (1994) found no decrease in the rate of photosynKey words: Zea mays, Striga hermonthica, photosynthesis, thesis by young leaves of sorghum cv. Tienmarifing, due
photorespiration, enzyme activity.
to infection of plants by Striga under field conditions and
suggest that the difference between their results and those
obtained in glasshouse conditions may be either because
Introduction
of the different varieties used or because growth in pots
Striga hermonthica is a serious weed pathogen on maize introduces stresses not experienced under field conditions.
crops grown in Africa (Musselman, 1980; Mwanza, 1991). Tuohy et al. (1987) and Graves et al. (1990, 1992) showed
3
4
Present address: Department of Biochemistry, University of Glasgow, Glasgow G12 8QQ, UK.
To whom correspondence should be addressed. Fax: + 44 1582 760 981.
© Oxford University Press 1995
Downloaded from http://jxb.oxfordjournals.org/ at Penn State University (Paterno Lib) on September 12, 2016
Received 28 November 1994; Accepted 10 March 1995
760
Smith et al.
Materials and methods
Plant material and growth conditions
Seeds of Zea mays (L.) variety 8338-1 were surface-sterilized
by shaking with H2O/sodium hypochlorite solution >5 per
cent available chlorine (9:1, v/v) for 20min, washed with
distilled water and germinated on moist glass fibre paper at
37 °C. When the primary roots of the seedlings were approximately 5 cm in length (approximately 3d), the seedlings were
placed on metal grids over beakers containing 20% Long
Ashton nutrient solution (Hewitt, 1966, Tables 40 and 41) in
which roots were immersed. Plants were grown for 7 d in a
glasshouse, with minimum day and night temperatures of 25 °C
and 15 °C, respectively. A minimum photosynthetic flux density
of 400 ^mol m" 2 s~ 1 during a 16 h photoperiod was ensured
by supplementary sodium lamps from 04.00 h to 20.00 h. Seeds
of Striga hermonthica were surface-sterilized for 3 min in the
diluted sodium hypochlorite solution described above and
washed with distilled water. They were preconditioned for 7 d
on moist glass fibre paper at 37 °C in the dark.
At the end of the 7 d period 12 maize seedlings were selected,
and each was planted in a 25.5 cm diameter pot containing
3.75 dm3 of a mixture of sand, loam, and peat (7:3:3, by vol.).
The pots were first filled to within 15 cm of the final surface.
Striga seeds, treated as described above, were transferred to six
fresh glass fibre filter discs which were placed on the temporary
surface in six of the pots. The maize seedlings were supported
touching the glass fibre discs and filling of the pots was
completed. The plants were grown on in the glasshouse under
the conditions described above. They were watered daily and
supplemented twice-weekly with 500 cm3 of 20% Long Ashton
solution.
In this way, a sequence of sowings was established of batches
of six maize plants without Striga seeds in the growing medium
and six plants with. The methods adopted ensured rapid and
certain infection with Striga during the early phase in the
growth of the host maize plant. The batches of 12 plants were
grown in a random arrangement on a bench 1.6 x 1.8 m.
Because the conditions were not fully controlled, there were
seasonal variations in light intensity and temperature that
changed the growth of plants and the rate of development of
symptoms of infection from batch to batch. We report results
from six batches of plants sown in April 1991, and in January,
March, May, July, and September 1992. The first batch was
used to investigate the photosynthetic mechanism by studying
the products of assimilation of 14CO2 by pulse-chase. The
second and third batches were used to measure photosynthetic
rates and activities of chosen enzymes of photosynthetic
metabolism. The three later batches provided the leaf tissue
samples for electron microscopy. The pulse-chase study was
made when the strongest infecting Striga shoot had emerged
15 cm above the soil level and thus when host symptoms were
severe. Observations with this and other early batches of plants
showed that, under the growth conditions used, symptoms of
infection usually appeared well before emergence of shoots of
the parasite. Subsequent studies have, therefore, mainly involved
earlier stages of infection.
Pulse-chase experiments on maize leaves
Experiments using 14CO2 were conducted in the glasshouse
used for growth of the plants between 6 and 7 h into the
photoperiod (i.e. between 10.00 h and 11.00 h). Care was taken
to position the leaf so that the incident PPFD was near to
400ftmol quanta m" 2 s~ 1 . The leaf temperature was between
34 and 38 °C; well above the minimum day temperature at this
stage in the photoperiod. A 1000-gauge polyethylene bag was
slipped over a leaf and sealed round the base of the leaf by
pressure from foam plastic stuck to strips of wood held against
the mouth of the bag by rubber bands. Residual air was
evacuated through a plastic connector sealed into the wall of
the bag. Air (500 cm3) containing a total of 6.5 /*mol of CO2,
including 97.5 (xCi (3.61 MBq) of 14CO2, was injected quickly
into the bag. The leaf was allowed to photosynthesize with the
14
CO2 for 10 s. The air with residual 14CO2 was then evacuated
to a soda-lime tower, the bag was removed from the leaf and
photosynthesis was allowed to continue in the ambient air for
the chase period. In some experiments a 58 min chase was given
following a longer pulse of 14CO2 (2 min). At the end of the
chase period, treated leaves were detached and immediately
frozen in liquid nitrogen. Soluble metabolites were extracted
from the leaf tissue, by the method described by Redgwell
(1980). Cellulose TLC in two dimensions (Waidyanatha et al.,
1975) was used to separate the products of photosynthesis.
Radioactive compounds on the chromatograms were detected
by autoradiography and appropriate areas of the thin layers
were removed for determination of 14C using a scintillation
spectrometer (Waidyanatha et al., 1975).
Gas exchange measurements
Foliar carbon dioxide exchange rates were measured using a
portable infra-red gas analyser (LCA-2, Analytical Development
Company (ADC), Hoddesdon, UK) together with a modified
Parkinson chamber (ADC) for narrow leaves supplied with dry
inlet air containing 340 fimol mol ~' CO2 from a cylinder.
Illumination (400/xmol quanta m~ 2 s~') was from a quartz
halogen lamp supported directly above the leaf chamber (Young
et al., 1989). The partial pressure of CO2 entering and leaving
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decreases in photosynthesis at saturating photon flux
densities in sorghum, millet and cowpea infected with
Striga in a glasshouse. The visible symptoms of infection
evident in the field and in glasshouses suggest that rate
of photosynthesis per unit leaf area must eventually be
affected and the stunting and wilting of host plants must
result in a decrease in canopy photosynthesis.
Some preliminary studies of the path of carbon assimilation in leaves of maize plants infected with
S. hermonthica indicated a slight change in functioning
of the C4 pathway (Mansfield et al., 1990). Because leaves
of infected plants retained more 14C in malate and less in
alanine after a long chase period, it was suggested that
the rate of decarboxylation of malate or the transport of
pyruvate from the bundle sheath chloroplasts was
decreased. We report now the results of a more detailed
investigation of the pathway of carbon assimilation in
the leaves of infected maize plants, further measurements
of photosynthetic rate, and measurements of the activities
of two leaf photosynthetic enzymes from mesophyll
tissue, PEP carboxylase (EC 4.1.1.31) and pyruvate P{
dikinase (EC 2.7.9.1), and two from bundle sheath
tissue, ribulose-l,5-6£yphosphate carboxylase/oxygenase
(Rubisco; EC 4.1.1.39) and NADP-linked malic enzyme
(NADP-ME; EC 1.1.1.40). A preliminary account of part
of this research was given by Smith and Keys (1992).
Photosynthesis by Striga hermonthica
the cuvette together with the photon flux density were recorded
using a data logger (ADC). The data were later used to
compute CO2 exchange rates on a leaf area basis using the
equations described by von Caemmerer and Farquhar (1981).
Measurements were made in the morning at least 6-7 h into
the photoperiod and at air temperatures of 34-38 °C.
761
l
Table 1. Percentage distribution of *C among CA acids
(malate + aspartate), phosphate esters, sugars, and in
glycine+serine in extracts of leaves from infected and control
maize plants
The leaves had been allowed to photosynthesize for 10 s or 2min
(58 min chase only) in air containing M CO 2 (pulse) followed by
photosynthesis in ambient air (chase) for the times shown
Electron microscopy
Treatment Fraction
Chase period (min)
0
4
0.5
0.75
1 2
58
C in fraction (% of total extracted)
Control
Malate + aspartate 76.5 30.2 49.5 46.6 24.4 4.4 1.1
Phosphate esters 21.4 62.2 39.0 43.0 35.4 4.0 0.0
Sugars
1.1 7.0 S.8 7.7 35.9 86.5 97.1
Glycine + serine
0.4 0.5 0.6 0.7 2.4 2.2 0.4
Others
0.6 0.1 2.1 2.0 1.6 2.9 1.5
Infected
Malate + aspartate 73.3 17.2 44.3 30.3 9.0
Phosphate esters 23.5 65.8 38.4 47.3 27.3
Sugars
2.4 10.2 4.0 12.6 46.7
Glycine + serine
0.4 3.2 2.7 5.4 12.0
Others
0.4 3.6' 10.6* 4.4' 5.0*
0.5 0.8
0.7 0.1
92.3 95.9
5.5 0.8
1.0 0.5
' Mainly glycerate.
Enzyme activities
Between days on which gas exchange measurements were made,
5 cm2 leaf discs were removed from the youngest fully expanded
leaves by freeze-clamping and were stored in liquid nitrogen
until required. Leaf discs were extracted by a modification
of the method of Ashton et al. (1990). Each frozen leaf disc
was ground in 300 mm3 buffer containing 50mol m~3
HEPES-KOH, pH7.5; 5 mol m~3 MgCl2; lOmol m~3 DTT;
and 1 mol m
EDTA at room temperature. Subsequent
operations involving the use of this extract were at between 15
and 25 °C. The suspension was passed through a 100 fun nylon
mesh filter, and centrifuged for 2min at lOOOOxg. The
supernatant was desalted by passage through a 2 cm3 column
of G-25 Sephadex (Pharmacia). The diluted solution of proteins
was used for the spectrophotometric determination of the
activity of PEP carboxylase, Rubisco, pyruvate P| dikinase, and
NADP-ME at 25 °C following the methods of Ashton et al.
(1990).
Results
the total radioactivity recovered from the chromatograms.
The values shown in the column headed 'zero' chase time
are typical of three separate experiments and for 58 min
for two separate experiments each for control and infected
plants. The values for intermediate times are results from
single samples. At the end of the 58 min chase the
allocation of 14C among the fractions in the leaves was
similar for infected and control plants. Mansfield et al.
(1990) observed decreased labelling of alanine with an
increase in malate in leaves of infected plants after a
prolonged chase. After 1 and 2 min chase periods in the
present experiments (Table 1) there was more radioactivity in glycine and serine in leaves of infected plants
suggesting an increase in flux through the photorespiratory pathway due to partial failure of the CO2
concentrating mechanism.
Pulse-chase experiments
Photosynthesis rate measurements
Autoradiograms of the two-dimensional TLC plates used
to analyse total extracts showed a pattern of 14C incorporation normal for C4 photosynthesis with high initial
levels of isotope in C4 acids and subsequent increases in
sucrose and phosphate esters during the chase period. No
qualitative differences were observed in the distribution
of 14C among photosynthetic products in leaves of
infected and control plants for any of the chase periods,
but quantitative differences were found on measuring
radioactivity in the compounds separated by TLC. Table 1
shows the percentage allocation of 14C into sugars, C4
acids, glycine and serine, and phosphate esters for the
various chase periods calculated from the sum of the
amounts of radioactivity in substances of each group and
Figures la and b show how the rate of photosynthesis
changed with time for leaves of control and infected
maize plants. In Fig. la the rates of photosynthesis
obtained are initially much lower than those in Fig. lb
although the final rates were similar. The difference is
attributed to the more favourable light intensities for
growth of the young plants in the period from April to
June when the second experiment (Fig. lb) was made. In
the first experiment (Fig. la) the reduction in photosynthesis in infected maize plants began 32 d after planting
with Striga seeds; in the second experiment (Fig. lb) the
reduction in host photosynthesis began 39 d after planting. At the end of the period over which measurements
were made, the differences in photosynthesis between
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Samples were taken from three batches of plants sown as
described above. Usually the samples were taken 7-8 weeks
after exposure of the maize seedlings to Striga, but for the
batch of plants sown in July 1992, samples were taken at both
7 and 11 weeks. On each occasion samples were taken from
leaves of three control and three infected plants. Pieces of fresh
leaf approximately 1 mm2 from halfway along youngest fully
expanded leaves, clear of the mid-rib, were fixed in 2.5%
glutaraldehyde in 0.2 M phosphate buffer, pH 7.2, for 2 h,
stained in 1% OsO4 for 2 h, dehydrated to acetone and
embedded in Agar 100 resin (Agar Scientific Ltd., Stansted,
Essex, UK). Sections were cut with freshly prepared glass
knives using an Ultracut Microtome (Reichert-Jung, Vienna,
Austria). The sections were stained on grids with uranyl acetate
and lead citrate and viewed using a Philips 201 Electron
Microscope.
762
Smith et al.
12
T 8
I
individual plants in the time taken for the appearance of
visible symptoms of infection. The number of emerged
Striga shoots per infected maize plant appeared to have
little effect on the observed rate of photosynthesis for
leaves of the host plant (see also Press and Stewart, 1987).
Three individual maize plants, each supporting one
emerged Striga plant, had the following rates of photosynthesis on consecutive sampling dates, 4.7, 1.8 and 8.1,
and 8.7, 4.2 and 0.7 ^mol CO2 m" 2 s~\ respectively. On
the following sampling date, leaves on two of the three
plants were no longer photosynthesizing.
Electron microscopy
In the course of making the measurements of photosynthetic rate, we noticed that leaves of infected plants took
much longer to reach a steady rate of photosynthesis
following enclosure in the leaf chamber than leaves of
control plants. The effect was clear at early stages in the
appearance of symptoms of infection and was taken to
indicate some mechanical weakness in leaves of infected
plants. This hypothesis was investigated by studying ultrathin transverse sections of the leaves in the electron
microscope. Plate 1 shows sections of leaves, typical of
30 to 40 examined, from control and infected plants taken
before emergence of the parasite. The bundle sheath and
vascular cells of leaves of infected plants are distorted in
the section and their walls appear thinner than for corresponding cells in the section from the leaf of a control
plant. Measurements from an enlargement of the photograph in Plate 1 gave an average wall thickness of 0.6 ^m
for control and 0.4 ^m for bundle sheath cells of leaves
of infected plants. Since structural elements of the leaf
seemed to be affected by infection of plants with Striga,
it seemed possible that there may also be changes in the
enzyme activities. The activities of two enzymes known
to be located in the bundle sheath and two in the
mesophyll cells were measured.
Enzyme activities
12
3 0 4 0
S)
TO
Time (Days After Planting)
Fig. 1. Rates of photosynthesis by leaves of maize plants grown in the
presence (O) or absence ( • ) of Striga hermonthica. Each point
represents the mean rate for the youngest folly expanded leaves from
six plants ± the standard error of the mean. Experiment 1 (a) involved
measurements made in February to early April and experiment 2 (b)
involved measurements made in late April to early June. Arrows show
the point at which an infecting Striga first emerged above the soil. All
six maize plants sown with seed of the parasite supported emerged
Striga plants within the next 10 d.
In the first experiment (Fig. 2a, b) the enzyme activities
in control and infected plants followed the same trends
with plant age with no significant differences between the
two sets of plants. In the second experiment (Fig. 2c, d),
as with photosynthetic rates, the enzyme activities were
higher because of the better growing conditions. PEP
carboxylase activity in leaves from infected plants was
higher in early samples than in the corresponding leaves
of control plants. At day 36 both NADP-ME and Rubisco
measurements were higher in leaves of infected plants.
None of the differences in activities of the four enzymes
between leaves from infected and control maize plants
were significant (7*=0.05). The measured activities of
PEP carboxylase and NADP-ME were more than
adequate for the corresponding observed rates of
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leaves of control and infected plants were compared using
analysis of variance unpaired r-tests. The differences in
rates of photosynthesis between control and infected
maize plants were significant (P = 0.05) from day 43 in
the first experiment (Fig. la), and from day 50 in the
second experiment (Fig. lb). Figure 1 shows that Striga
plants had not emerged until after the first signs of
decreased photosynthesis. In the plants to which Fig. lb
refers, symptoms of infection by Striga were obvious
when measurements were begun. There was a darkening
of the leaves and a characteristic stripy appearance.
Photosynthesis measurements were also made on all
leaves of control and infected plants (data not shown),
and values obtained showed that the decrease in photosynthesis in infected maize plants was not restricted to
the young leaves only, but was a phenomenon affecting
all leaves. These data also showed that the rates of
photosynthesis in both control and infected plants were
highest in the youngest fully expanded leaves, and
decreased as the leaf became older. Thus further investigations mostly involved the youngest fully expanded
leaves on the plants. There was considerable variation
between individual plants in the photosynthetic rate
observed and this was more pronounced in leaves from
the infected plants (Fig. 1) because of variation among
Photosynthesis by Striga heimonthica 763
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Plate 1. Electron micrographs of transverse sections through leaves of control (top) and Sfr^a-infected (bottom) maize plants. X = xylem,
P = phloem, BS = bundle sheath cell, M=mesophyll cell, ch=chloroplast, w = cell wall, and n = nucleus.
764 Smith et al.
photosynthesis, activities of Rubisco were generally just
sufficient, but activities of pyruvate P; dikinase were not
adequate, and lower than activities usually reported for
maize leaves, but similar for control and infected maize
plants. The decrease in photosynthesis due to infection
with Striga is not explained by a shortage of activities of
these particular proteins.
150
100
'«
50
Discussion
The amount of radioactivity in glycine and serine
during pulse-chase experiments has been used in the
characterization of C3, C4 and C3-C4 intermediate mechanisms of photosynthesis (Holaday and Chollet, 1983;
Apel et al., 1988). The amounts of radioactivity in these
amino acids can not be taken as a quantitative measure
of photorespiration, but we know that in healthy maize
leaves the incorporation of carbon into them responds to
external O2 and CO2 in a manner suggesting a slow flux
through the photo respiratory pathway (Hickman and
Keys, 1972). The results suggest that in leaves of maize
plants infected with Striga the flux is increased, indicating
a lower CO2 concentration in cells of the bundle sheath
containing Rubisco. Increased oxygenase activity, and
increased flux to glycollate, glycine and serine are the
result. The presence of increased radioactivity in glycerate,
the final product in the photorespiratory cycle, may be
taken as further evidence of increased photorespiratory
activity. We did not measure compensation concentrations
of CO2, or other parameters that would indicate increased
photorespiratory activity, but became concerned with leaf
structure because of changes in leaf appearance as an
early symptom of infection and the rather obvious
changes in the strength of leaves of infected plants that
30
40
50
60
150
(b)
I 100
50
3 0 4 0
50
60
Time (Days After Ranting)
300
(c)
200
100
50
80
(d)
'200
100
3 0 4 0
50
60
Time (Days After Planting)
Fig. Z Activities of PEP carboxylase ( • ) , Rubisco (O), pyruvate P,
dikinase ( • ) and NADP malic enzyme (D) in leaves of maize plants
grown in the absence (a, c) and presence (b, d) of Striga hermonthica.
Each point is the mean enzyme activity in the extract from 5 cm2 of
leaf taken from the youngest fully expanded leaves from six plants ± the
standard error where this is larger than the symbol used. Experiment I
(a, b) involved measurements in February to early April and experiment 2 (Fig. 2c, d) involved measurements in April to early June. The
emergence of Striga above the soil is as indicated in Fig. 1.
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Under the glasshouse growth conditions employed, infection of maize plants with Striga hermonthica does decrease
the rate of photosynthesis per unit leaf area relative to
leaves of control uninfected maize plants. The objective
of the investigation was to discover the mechanism by
which Striga infection causes decreases in photosynthetic
rate in leaves of its host. Three lines of evidence lead us
to the conclusion that the mechanism involves effects on
the internal leaf structure. Firstly, we noticed that leaves
of infected plants responded adversely to enclosure in leaf
chambers so that it took longer than with leaves from
healthy plants to obtain a steady rate of photosynthetic
carbon assimilation. Secondly, we found increased incorporation of 14C from 14CO2 in the light into glycine and
serine in leaves of infected plants. The third line of
evidence is presented through electron micrographs of
transverse sections of leaves of infected and control plants.
There is a typical distortion of cell outlines due to
infection with Striga and a tendency to thinner cell
walls, especially in the vascular bundles and bundle
sheath tissue.
Photosynthesis by Striga hermonthica
Acknowledgements
We thank our colleagues at UCL and RES for useful discussions.
Especially we thank J. Franklin and his staff at RES for much
help in the culture of plants. We thank the AFRC for financial
support (studentship reference P020CS).
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we believed to be responsible for slow equilibration upon
attachment of leaf chambers. The evidence from the
electron micrographs is consistent with inadequacies in
the cell structure of the bundle sheath to retain high
concentrations of CO2 to suppress the oxygenase activity
of Rubisco. Measurement of four enzyme activities essential for C4 photosynthesis showed that these are not
decreased by infection. Taken in combination with the
earlier evidence that transport processes related to bundle
sheath metabolism might be involved in the adverse effects
of infection by Striga on host photosynthesis (Mansfield
et al., 1990), our results suggest that future studies should
be directed at measurements of photorespiration, changed
anatomical structure of the leaves and altered permeability of the bundle sheath walls, rather than further concern
with photosynthetic rates per unit leaf area.
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