Energy Transfer Inhibition Induced by Nitrofen
Bernhard Huchzermeyer
Botanisches Institut, A rbeitsgruppe für Biochemie der Pflanzen, Tierärztliche Hochschule, Bünte­
weg 17d, D-3000 Hannover, Bundesrepublik D eutschland
Z. Naturforsch. 37 c, 787-792 (1982); received April 30/June 8, 1982
Herbicides, Nitrofen, Energy Transfer Inhibition, Photophosphorylation, N ucleotide Exchange
The herbicide nitrofen was shown to act as an energy transfer inhibitor. The results proved
nitrofen to act by inhibiting nucleotide exchange on the chloroplast coupling factor. A strong
correlation was found between the inhibition o f phosphorylation, ATPase activity, and nucleotide
exchange. These results are discussed in terms of a regulatory effect o f tightly bound A D P on the
enzymatic activity o f the chloroplast coupling factor.
Introduction
tors, covalent binding o f the carbodiim ide D C C D to
CF 0 [8—10] and interaction with tributyltin chloride
Nitrofen is used to control annual w eeds in cul­
[ 11, 12] inhibit the former reaction, w hile others
tures o f parsley, onion, carrot, celery, and rice [ 1].
affect C F j, e.g. phlorizin [13—16], D io-9 [1 7 —19],
Until now its m ode o f action is a controversial
tentoxin [2 0 -2 7 ], and a number o f 3'-esters o f A D P
question. The main herbicidal effect o f nitrofen may
[28].
probably be located in the photosynthetic apparatus
Chloroplast ATPase is a latent enzym e which
[2], Besides chlorophyll bleaching [3 - 5] and electron
needs activation in order to display its catalytic
transport inhibition [2, 4] nitrofen causes energy
activity. Physiological activation results from m em ­
brane energization [29, 30]. R ecently it was shown
transfer inhibition [4, 6]. From their own results Lam­
that activation is paralleled by energy dependent
bert et al. [6] concluded that nitrofen must be com ­
release o f tightly bound A D P from C F Xand deacti­
petitive to A D P but not to phosphate in the process
o f photophosphorylation. This result is rather sur­
vation to the reverse reaction [30 —32]. Probably the
prising and therefore particularly interesting because f rate o f photophosphorylation is usually controlled by
enzyme activation rather than by fatigue num ber o f
o f the lack o f structural sim ilarity between the sub­
strate ADP and the inhibitor nitrofen. However, a
the enzyme [29, 33]. Inhibition o f ATPase activation
competitive type o f inhibition could also be caused
as well as ATPase reaction would o f course affect the
by other effects than substrate displacem ent from
rate o f photophosphorylation and produce the
characteristics o f energy transfer inhibition (i.e. in­
the catalytic site [7]. In this paper, the m echanism o f
energy transfer inhibition by nitrofen is studied in
hibition o f coupled electron transport).
greater detail.
The goal o f the present study was to localize the
effect o f nitrofen with regard to the partial reactions
The terminal process o f photophosphorylation
may be subdivided into two partial reactions, I) H + mentioned earlier.
translocation through the C F0-part o f the ATPase
complex, and II) the ATP synthase reaction catal­
Methods
ysed by C F ^ O f the known energy transfer inhibi-
Abbreviations: C F 15 chloroplast coupling factor; D CM U,
3-(3,4-dichlorophenyl)-l,l-dim ethylurea; D CPIP, 2,6-dichlorophenol-indophenol; Fecy, K3[Fe(CN )8]; I50, inhibitor
concentration causing 50% o f m aximum effect; MV,
methylviologen, paraquat, N,N'-dimethyl-4,4'-bipyridinium
dichloride; nitrofen, 2,4-dichlorophenyl-4'-nitrophenylether
= Tok®; PMS, phenazine methosulfate; tricine, N -tris(hydroxymethyl)methylglycine.
Reprint requests to Dr. B. Huchzermeyer.
0341-0382/82/0900-0787
$ 0 1.3 0/0
Chloroplast isolation from spinach leaves was
carried out as described by Strotmann et al. [34]. For
chlorophyll determination A m on ’s m ethod [35] was
employed.
N on-cyclic electron transport from water to fer­
ricyanide was measured by follow ing the decrease in
420 nm absorbance in a spectrophotom eter (PM Q II,
Zeiss) with cross illum ination equipm ent for one
minute (continuous registration). The cross illu-
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B. Huchzermeyer • Energy Transfer Inhibition Induced by Nitrofen
mination equipm ent contains a 2 mm heat filter
(Schott) within a cooled lense system. The red
actinic light (filter RG 630, Schott) was 870 W /m 2,
measured within the reaction cuvette, which was
kept at a temperature o f 20 °C. The reaction
medium contained 25 m M tricine buffer, pH 8.0,
50 m M NaCl, 5 m M M gCl2, 5 m M Pi, pH 8.0, 0.5 m M
ADP, 1 m M K 3[F e(C N )6], and 12 to 20 ng chloro­
phyll in a total volum e o f 2 ml.
For the m easurement o f non-cyclic phosphoryla­
tion the m edium contained 5 m M 32P-labeled phos­
phate (1.8M B q/m l, Amersham Buchler). The reac­
tion was stopped after one minute by addition o f
HC10 4 at a final concentration o f 0.3 m . After cen­
trifugation (2 minutes at 10000 x g ) an aliquot was
analyzed for organic phosphate em ploying the
method o f Strotmann [36].
For measurement o f uncoupled electron transport,
CFj stripped chloroplasts were prepared as de­
scribed by Tischer and Strotmann [37]. C yclic phos­
phorylation was measured with 50 ^im PMS instead
o f Fecy. Photosystem I dependent phosphorylation
was followed in a system containing 20 hm D C M U ,
5 m M ascorbate, 0.2 m M D CPIP, and 0.2 m M MV
instead o f Fecy. In the sam e system, electron trans­
port was followed by m easuring the consum ption o f
0 2 with a Clark type electrode.
Trypsin activated ATPase activity o f isolated C F t
was measured as described by Strotmann et al. [38]
and Hesse et al. [39]. Light triggered ATPase was
measured as described by Schumann and Strotmann
[31]: Chloroplasts were illum inated for one m inute in
a water bath at 20 °C with white light (1200 W /m 2)
mg
o f a commercial lantem -slide projector. The reaction
medium contained 25 m M tricine buffer, pH 8.0,
5 m M MgCl2; 50|im PMS, 20 j im D C M U , and 0.13
to 0.15 mg chlorophyll per ml. After 5 seconds in the
dark, a sample o f the activated chloroplasts was
injected into the ATPase test m edium , containing no
PMS but 0.5 m M ATP labelled by y-[32P]ATP
(3 —4 KBq/ml).
Kinetic measurements o f light induced exchange
o f ADP on membrane bound CFj was m easured
using the method o f Strotmann et al. [40]. Light
dependent proton transport across the thylakoid
membranes was measured with a glass electrode at
20 °C in a medium containing 50 m M N aC l, 5 m M
MgCl2, 50 hm PMS, and 60 to 80 |ig chlorophyll in a
final volume o f 3 ml. Illum ination was performed
employing a commercial lantern-slide projector. The
red actinic light (filter R G 630, Schott) was
935 W /m 2, measured inside the temperature con­
trolled (20 °C) glass reaction chamber.
Results
1. Nitrofen as an inhibitor o f photosynthetic
electron transport
Energy transfer inhibition by nitrofen is superim ­
posed by direct inhibition o f electron transport [2 ,
41]. The latter effect can be isolated by follow ing
uncoupled electron transport from water to Fecy.
Half maximal inhibition is achived by 10|iM nitro­
fen. Congruent to earlier results [2] no inhibition o f
uncoupled photosystem I electron transport from
chi
(pM atrazine)
-1
Fig. 1. Double-reciprocal plot of atrazine
binding to C F^stripped chloroplasts com ­
peting with 4|iM (a ), 2( im (□), and 1 hm (v )
nitrofen or without addition o f nitrofen (o).
Chlorophyll content was 27 ng/m l. Experi­
mental conditions corresponded those o f un­
coupled electron transport m easurem ent with
the exception of the electron acceptor being
omitted.
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B. Huchzermeyer • Energy Transfer Inhibition Induced by Nitrofen
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Table I: Inhibition of electron transport through photo­
system I. The reaction m edium contained 25 mM tricine
buffer, pH 8.0, 50 mM N aCl, 5 mM MgCl 2, 5 mM ascorbate,
pH 8.0, 0.2 mM MV, 0.2 mM DCPIP, 15 ng/m l chlorophyll,
and 0.2 mM A DP and 5 mM phosphate, pH 8.0, when m ea­
suring phosphorylation. As the herbicide and D CPIP were
dissolved in methanol, all sam ples contained 5% (v/v) m e­
thanol. Uncoupled chloroplasts were prepared as described
by Tischer and Strotm ann [37] from the same leaves in p a ­
rallel. Electron transport was m easured by following O 2
consumption in Clark type 0 2 electrode.
(imol O 2 consum ed
mg Chi • h
Conditions
Non-phosphorylating
Phosphorylating
Uncoupled
40 |iM nitrofen
control
37.4
37.6
76.5
162.3
497.0
496.4
inhibition
-
52.9%
-
DCPIP to MV was obtained (Table I), indicating
that the site o f nitrofen inhibition is around photo­
system II. Fig. 1 shows that nitrofen is a com petitive
inhibitor in the binding o f 14C-labeIled atrazine. The
calculated K x is 11 hm. It appears therefore that the
site o f electron transport inhibition by nitrofen is
identical with the D C M U binding site.
2. N itrofen actin g as an en erg y tran sfer in h ib ito r
In contrast to the uncoupled system, photosystem-I dependent electron transfer in the presence o f
Pi and A D P is dim inished by the herbicide (Table I)
with an I50 o f 1.5 hm. The sam e value is obtained all
the same whether PMS m ediated photophosphory­
lation or non-cyclic electron transport m ediated
phosphorylation in a water-ferricyanide system are
measured. Accordingly, this effect o f nitrofen may
be ascribed to energy transfer inhibition. Lambert
et al. [6] found that inhibition o f phosphorylation by
nitrofen is com petitive to A D P. This result is con­
firmed by double-reciprocal plots o f our own ex­
periments. But a D ixon-plot o f these experim ents
indicates partial com petitive inhibition with respect
to ADP interacting with CF! (Fig. 2). As a working
hypothesis derived from the Briggs-Haldane form o f
an enzyme reaction, the occurance o f a C F r A D P
complex during ATP-synthesis is postulated. This is
in good agreement with m odels based on experi­
mental results o f Boyer et al. [42] and Bickel-Sandkötter and Strotmann [43]. On the basis o f this
— 1------ ’
-------1-
1------ 1------ 1------ 1—
10
(jM n itro fe n
Fig. 2. Dixon plot o f a phosphorylation experiment. The
reaction medium contained 25 mM tricine buffer, pH 8.0,
50 mM NaCl, 5 mM MgCl2, 5 mM phosphate, pH 8.0, 20 (iM
DCMU, 50 |iM PMS, 20 ng/m l chlorophyll, 10 mM glucose,
20 units/ml hexokinase, and nitrofen as indicated. M e­
thanol content was constant 2% (v/v). A D P concentrations
were 2 hm ( a ) , 5 (iM (□ ), 10 hm ( a ) , and 15 |iM ( o ) respec­
tively.
assumption, the shown results indicate that nitrofen
binds as well to CF! as to C F i-A D P -com plex w ith ­
out forming a ternary dead-end-com plex but reduc­
ing turnover rate. On the other hand, the inhibition
kinetics are com plicated with regard to the substrate
Pi. At Pi concentrations less than 150 (iM the effect o f
nitrofen is not m anifest any more, indicating that
phosphate binding and even phosphoryl transfer
may be unaffected. The observed phosphorylation
rates o f 161 (imol ATP per mg chi and hour (150 |im
Pi) down to 43 nmol ATP per mg Chi and hour
(20 (im Pi) were not inhibited by addition o f 12|iM
nitrofen any more. Therefore our further interest
was focused on nitrofen interactions with nucleotide
dependent reactions.
3. E ffect o f nitrofen on ex ch a n g e o f tig h tly b o u n d
adenine nucleotides a n d on A T P h yd ro lysis
In addition to the catalytic A D P binding site, CFi
contains a regulatory site which binds A D P and
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pmol ATP
nmol ADP
B. Huchzermeyer • Energy Transfer Inhibition Induced by Nitrofen
ATPase activity
R elease of tightly bound [8-^C]A D P
Fig. 3. Correlation between the activation o f ATPase
activity (upper part) and liberation o f tightly bound
nucleotides (lower part) with ( a ) and w ithout (o) addition
of 12 (iM nitrofen, respectively, during the activation step.
The reaction m edium contained 25 m M tricine buffer,
pH 8.0, 5 m M MgCl2, 50 u m PMS, 20 |iM D C M U , and
28 ng/ml chlorophyll. The chloroplasts had been preloaded with [8-14C]ADP as described by Schum ann and
Strotmann [31]. Employing their m ethod, each sam ple was
split into two portions. One was applied in an ATPase
experiment, the other one was analysed for liberated ADP.
probably ATP too [34, 42 - 45]. This site changes its
affinity to the ligand in energized and de-energized
membranes. Tightly bound nucleotides present in
the de-energized state are liberated or exchanged,
respectively, when the thylakoid m em branes are
energized by light [34, 46], pH jum p [34, 47] or
external electrical fields [29]. It has been shown that
energy induced release o f bound A D P is related to
the induction o f ATPase activity (“light-triggered
ATPase”) and re-binding o f A D P causes deactiva­
tion o f the enzyme [31, 32, 48]. Probably the sam e
mechanism is also involved in the control o f phos­
phorylation [29, 49].
Fig. 3 shows the effect o f nitrofen on the kinetics
o f the release o f tightly bound [ 14C ]A D P and con­
comitant activation o f ATPase activity. Both reac­
tions are inhibited in parallel. U nder the em ployed
conditions (PMS m ediated electron transport) an
inhibition o f electron transport can be excluded (s.
Table I) so that the observed effect m ust be at­
tributed to a reaction related to the ATPase com plex
itself.
A nucleotide binding site o f CF! which has been
depleted by membrane energization, can be re-filled
with ADP yielding a tightly bound nucleotide again
[40]. This reaction is independent o f energy input
and virtually irreversible in non-energized conditions
[44 - 46]. F ig 4 shows that the rate o f re-binding o f
[14C]ADP is inhibited by nitrofen, too.
In Fig. 5 the effect o f nitrofen on the rate o f ATP
hydrolysis induced by pre-illum ination is shown.
The herbicide is added after the light pre-treatm ent
in order to exclude superposition o f the nitrofen
Fig. 4. Binding o f [8-14C]ADP to A DP depleted
membranes. Chloroplasts had been illum inated
in the absence o f added nucleotides for one
minute. When light was switched off, F C C P at a
final concentration o f 30 |iM was added. 5 sec­
onds later ADP was added at a final concentra­
tion of 23.1 hm. This instant corresponds to zero
on the time scale. At indicated incubation inter­
vals samples were analysed for bound nucleo­
tides as described elsewhere [34]. The control
experiments (o) contained m ethanol w ithout ad ­
dition of nitrofen, in the parallel experim ent
nitrofen at a final concentration o f 5 hm was
added (□).
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B. Huchzermeyer • Energy Transfer Inhibition Induced by Nitrofen
791
/jm d ATP hydrolyzed
mg chl- h
Fig. 5. Inhibition o f light triggered ATPase by
addition of nitrofen. ATPase was activated in the
absence of herbicide as described by Schum ann
and Strotmann [31]. Afterwards activated chloro­
plasts were injected into an ATPase test m edium
containing 25 m M tricine buffer, pH 8.0, 5 m M
MgCl2, 1 m M ATP, 87 ng/m l chlorophyll, and
nitrofen as indicated. M ethanol content was kept
constant 2% (v/v).
effect on ATPase activation. N evertheless inhibition
o f ATP hydrolysis is apparent under these con d i­
tions. However, maximum inhibition is not m ore
than 50%.
Discussion
The presented results show nitrofen to inhibit the
overall reaction o f photophosphorylation at two
sites:
I) nitrofen inhibits electron transport and shows
typical reactions o f a photosystem II herbicide;
II) nitrofen acts like an energy transfer inhibitor.
The experiments should yield som e more insight
into the mode o f action resulting the latter effect.
Nitrofen did not only cause an inhibition o f p h oto­
phosphorylation but also o f light triggered ATPase
activity and nucleotide exchange. D iscussing the
results a central reaction inhibited by nitrofen should
be found.
The first experiments showed a partial com p eti­
tive effect o f nitrofen with respect to A D P taking
part in photophosphorylation. The participation o f
phosphate in this reaction was not at all affected. To
get an idea o f the mechanism o f inhibition, the
following very sim plified sequence o f reactions
leading to phosphorylation o f A D P is introduced:
A D P + C F j A A D P ---C F j ^ A D P-C Fj A productCFj A product- - -CFj A product -I- CFj
Remembering the theoretical considerations con­
cerning a partial com petitive inhibition, one can
demand nitrofen affecting the steps 1, 2 or 3. But if
nitrofen should affect step 3, com petition like Line­
weaver-Burk plots would not have been found. This
means nitrofen inhibits step 1 or 2. Em ploying our
methods, it is im possible to differentiate between
these two steps. One only can see the overall reaction
o f these two steps in terms o f nucleotide exchange
on C F j.
From our experience with phosphorylation ex­
periments one would rather say nitrofen affects
affinity o f CFj to nucleotides (or the binding con­
stants) than the maximal phosphorylation rate. But,
due to the mechanism o f partial com petitive in hibi­
tion, another possibility has to be mentioned: R e­
tarded activation o f a portion o f the CFj population
o f each thylakoid would pretend a reduced affinity.
The experiments reported by Strotmann et al. [49]
proved the necessity o f an activation o f CFj before
ATP synthesis or hydrolysis, respectively, can be
catalysed. As shown by the results presented, the
postulated activation steps o f both reactions are
inhibited by addition o f nitrofen. The activation o f
the enzyme is paralleled by a liberation of, up to that
moment, tightly bound ADP. From these connec­
tions it seems reasonable that the I50 were deter­
mined to be in the range o f 2 hm for inhibition o f
ATP synthesis, ATP hydrolysis, and nucleotide
exchange respectively.
Another effect o f nitrofen is the deletion o f the
regulatory effect o f A D P on the size o f the trans­
membrane proton gradient. As the experim ents con­
cerning measurement o f proton gradient were car­
ried out em ploying non-phosphorylating conditions,
one can only speculate about the possible connec­
tions between enhancement o f proton gradient and
regulation o f the enzym atic activity o f C F j. As a
matter o f fact, nitrofen concentrations in the range o f
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B. Huchzermeyer • Energy Transfer Inhibition Induced by Nitrofen
2|iM were found to result 50% deletion o f A D Peffect. This can be understood as a reference to a
correlation between these effects. Further experi­
ments concerning this problem will be carried out.
A cknow ledgem ents
I
return thanks to Professor Dr. H. Strotmann,
University o f Düsseldorf, for his interest in my ex-
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