Biochemistry of Herbicides Affecting Photosynthesis Kenneth Wright and J
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Biochemistry of Herbicides Affecting Photosynthesis Kenneth Wright and J. R. Corbett Fisons Ltd., Chesterford Park Research Station, Saffron Walden, Essex, CB10 1XL, U.K. Z. Naturforsch. 34 c, 966 — 972 (1979) ; received May 24, 1979 Herbicides, Photosynthesis, Pigment Synthesis, Inhibition This paper reviews the inhibitory effects of herbicides at three locations within photosynthetic electron transport, on photophosphorylation, and on pigment synthesis. 1. Introduction photosystem I, usually DCPIP or ferricyanide in an uncoupled system). Examples of the well known clas This paper is an introduction to the primary ses are given by Draber et al. [2]. The common effects of herbicides on photosynthetic electron structural requirements for activity in many chemical transport, photophosphorylation and pigment syn series have been pointed out [2, 6 — 8]; essentially thesis. Herbicides are not known to have primary inhibitors have a lipophilic moiety near the group effects on transcription, translation or carbon fixa — C ( = X) — N = (X = 0 or NH). One of the substi tion, and the inhibition of lipid synthesis by the tuents on the nitrogen is often H but this is not thiolcarbamates will not be considered since it is obligatory [2]. Some exceptions to these simple not restricted to the chloroplast. We will be con criteria will be mentioned later. cerned mainly with the primary biochemical elfects Location. The DCMU site is close to photosystem of compounds so far as they are known, since re ports of gross effects on whole plants do not provide II (see [1] for summary of early evidence) and leads which can be of use in seeking out new active most workers believe that DCMU blocks electron transfer from the primary acceptor of photosystem II herbicides. We will need to concentrate on the most (Q) to plastoquinone [9] though there may also be recent developments; a previous review [1] considers an effect on the water-splitting reaction [10]. Much the earlier work. Throughout we shall be empha progress on the detailed location is reported else sizing information that might aid the synthesis of where in this volume. The hatched area in Fig. 1 new herbicides. indicates the proteinaceous shield which is part of a model of the acceptor side of photosystem II 2. Compounds interfering with electron transport developed by Renger [11]. He suggests that DCMU (Fig. 2) interacts at this site by binding to the protein, because once the shield had been digested with Most herbicides in use today kill their target trypsin, several inhibitory effects of DCMU were weeds by interaction with photosynthetic electron no longer seen. Other research groups have now transport [2, 3], summarized in Fig. 1 [4]. For a examined additional electron transport inhibitors summary of the minority views on the organisation using this technique. All “DCMU-site” inhibitors of electron transport see [5]. The heavy arrows behave in the same way; trifluralin (1), nitrofen indicate the three sites we shall consider. (3), and perhaps ioxynil (5) do not (see [12] and 2.1. The DCMU site other papers in this volume). Many classes of compound are now know to Direct evidence that many Hill reaction inhibitors inhibit the Hill reaction (electron transfer between bind at the same site has recently been obtained in H20 and an electron acceptor acting before or after the elegant experiments of Tischer and Strottman [13]. They studied the binding of radioactive atra- zine (7), metribuzin (9) and phenmedipham (10) Abbreviations: DBMIB, 2,5-dibromo-3-methyl-6-isopropyl-p- benzoquinone; DCMU, 3-(3',4'-dichlorophenyl)-l,l-dimethyl- to chloroplast fragments and established (i) that urea; DCPIP, dichlorophenolindophenol; DNOC, 4,6-di- these compounds and DCMU compete directly with nitro-o-cresol; EPTC, ethyl-N,N-di-ra-propylthiolcarbamate. one another for the same site and (ii) that the bind Reprint requests to Dr. K. Wright. ing constants calculated directly from studies with 0341-0417 I 79 / 1100-0966 $ 01.00/0. radioactive compound or indirectly from competi- K. Wright and J. R. Corbett • Biochemistry of Herbicides Affecting Photosynthesis 967 BIPYRIDYLIUMS “ 0*5 *o-V 0-5 Fig. 1. Diagrammatic represen tation of the electron transport pathway of photosynthesis. See, for instance, reference [4] for further details and sources. The sites considered in the text are SITE It SITE I marked. CF3-^^-NPr2 Me-^^-NH.CHEt2 NO, NO* Me NO- 1 2 3 R =R =ci 4 R’ = CF3;R2= N 0 2 OH Cl R* N ^ N Et.NH^TJ ^ k. ^ nhNH,R.r NN SM6 RJ 5 R1 =R2=I;R3=CN 7 R=Pr 9 £ R' = R3=N 02;R2=Me 8 R = Et O NH co °-<S> lü ] ^ jo ? B>C° SR’ . _ T T \11, N Fig. 2. Structures of compounds inter- Me Me O.CO.NH H *fenng • with-.u electroni . transport. * (see/ 1 1 10B '-nPD2-c text). 1, trifluralin; 2, penoxalin; 3, l v I I \ £ ~ r' ~ * nitrofen; 4, fluorodifen; 5, ioxynil; 6, IO R'-'Pr DNOC; 7, atrazine; 8, simazine; 9, 2 metribuzin; 10, phenmedipham; 11, R =CH2C(CI)=CHCI bentazon; 12, EPTC; 13, diallate. 968 K. Wright and J. R. Corbett • Biochemistry of Herbicides Affecting Photosynthesis tion experiments were the same as the inhibition a lesser extent, fluorodifen are modest inhibitors of constants computed from Hill reaction inhibition plant mitochondrial electron transport (I50 for nitro data. Hence this site at which all the compounds fen 27 — 74 fM , depending on the substrate; [19]), compete is almost certainly the site at which inhibi so this might contribute to their herbicidal effect. A tion is brought about. further suggestion is that the compound acts as an Information about the DCMU site has recently energy-transfer inhibitor (see section 3). been provided by Machado and Amtzen et al. ([1 4 ], Reason why plants are killed. Although inhibition and see this volume). They discovered that triazine at the diuron site would cause depletion of ATP and resistance displayed by the weed Chenopodium NADPH2 death is probably not due to “starvation” album was due to a change in the chloroplast bind but rather to damage following a failure of the ing site so that binding of atrazine (7) was greatly mechanism that normally protects the photosynthetic decreased whilst DCMU binding was unaffected. apparatus against excessive illumination [20]. Taken together with the results described above it Stanger and Appleby [21] suggested that the seems likely that the various classes of compound damage was initiated by the lade of NADPH2 bind to different overlapping parts of a protein re required to maintain the protective carotenoid pig ceptor site so as to bring about inhibition of electron ments in the reduced form. Ridley [20], however, transfer [15]. suggests that when DCMU blocks electron transport Compounds which might inhibit the Hill reaction. conformational changes in the membrane that allow Although bentazon (11) has been shown to be a spillover of excitation energy from the antennae Hill reaction inhibitor [16], it was less effective units serving PS II to those serving PS I are pre than the inhibitors considered so far (e. g. 50% vented. Protection via the normal mechanism in inhibition of methyl viologen reduction at 200 j u m ) volving carotenoids is then no longer adequate and and the inhibition was, unusually, progressive with pigment breakdown ensues. When electron transport time; Böger et al. [17] suggested from their work between the photosystems resumes following the on algal chloroplasts and whole algae that a me addition of, e. g. a donor between the photosystems, tabolite may have been responsible. the conformational change which allows spillover Van Rensen et al. [18] measured the effects of can occur again and protection is restored. DNOC (6) on the Hill reaction using a variety of Both schemes are consistent with the results of conditions. The uncoupled ferricyanide Hill reac Moreland and Hill [3] who incubated isolated tion was the most sensitive, 50% inhibition being chloroplasts with DCMU in the light and in the caused at about 1 //M with uncoupling effects at dark, and then washed the chloroplasts to determine higher concentrations. Trebst and Draber [15] have if any irreversible inhibition had occurred. Less recently carried out regression analyses on Hill activity was restored to chloroplasts kept in the light, reaction inhibition results from a considerable presumably due to pigment breakdown. However, number of 2,6-disubstituted-4-nitrophenols and have when the experiment was conducted with simazine shown that the shape of the substituents was impor (8) the same restoration of activity was found after tant rather than their hydrophobic parameters. The both treatments. If both these compounds do bind authors postulate that the nitrophenols bind to a to the same site [13], the precise cause of death different site on the shielding protein (from DCMU may not be the same in each case; this warrants and other Hill reaction inhibitors) although the further investigation. same inhibitory effect on electron transport is in 2.2. The action of the bipyridylium herbicides duced. Diphenyl ethers also inhibit the Hill reaction, but The basic mechanism of action of these com the reported I50 values are perhaps a little high pounds has been quite well understood for some (nitrofen (3) 22 —23//M; but cf. fluorodifen (4), time although the details of the toxic species and 4.5 —5.6//M; [19]), and, like the dinitrophenols, their effects are still under investigation. The herbi they do not fit the structural requirements for the cides interact with photosynthetic electron transport DCMU site. Further, van Assche [12] found that as indicated in Fig. 1. Structural requirements for nitrofen did not compete with labelled DCMU for activity are known [22] and the sequence of events binding to chloroplast membranes.