Biochemical Responses Induced by Herbicides - American Chemical

4 The Role of Light and Oxygen in the Action of Photosynthetic Inhibitor Herbicides A L A N D. DODGE

Downloaded by FUDAN UNIV on February 21, 2017 | http://pubs.acs.org Publication Date: February 11, 1982 | doi: 10.1021/bk-1982-0181.ch004

University of Bath, School of Biological Sciences, Claverton Down, Bath, Avon BA2 7AY, United Kingdom

P h y t o t o x i c symptoms of i n j u r y caused by h e r b i c i d e s that inhibit c h l o r o p l a s t e l e c t r o n t r a n s p o r t , such as the ureas, t r i a z i n e s , and h y d r o x y b e n z o n i t r i l e s , are promoted by both light and oxygen. When carbon d i o x i d e fixation is prevented, excess excitation energy leads to the generation of longer lived triplet c h l o r o p h y l l . I f unquenched by c a r o t e n o i d s , this may directly induce proton a b s t r a c t i o n from u n s a t u r a t e d f a t t y a c i d s or s i n g l e t oxygen might be generated which induces lipid peroxide formation. Lipid p e r o x i d a t i o n leads to cellular d e s t r u c t i o n and death. H e r b i c i d e s that d i v e r t p h o t o s y n t h e t i c e l e c t r o n t r a n s p o r t , such as the bipyridyls paraquat and diquat, yield the superoxide a n i o n . Superoxide l e v e l s produced overtax the normal defense mechanisms. More t o x i c species such as hydroxyl free r a d i c a l s are a l s o probably produced which instigate lipid p e r o x i d a t i o n and lead to cellular d i s o r g a n i z a t i o n and death. James Franck wrote i n 1949 (1) " . . . i t i s one of the m i r a c l e s of photosynthesis that the p l a n t can use a dye able to f l u o r e s c e i n the presence of oxygen, predominantly f o r the purpose of r e d u c t i o n , and i s able to hold the process of photooxidation i n check so that damage i s prevented or minimized even under severe conditions". I t i s evident that the c h i o r o p l a s t i s endowed with p r o t e c t i v e devices that are able to l i m i t damage except under extreme c o n d i t i o n s . Such s i t u a t i o n s are promoted by the presence of photosynthetic i n h i b i t o r h e r b i c i d e s . In the normal c h i o r o p l a s t , l i g h t energy (hv) absorbed by pigments and i n p a r t i c u l a r by the c h l o r o p h y l l s (Chl) causes _g e x c i t a t i o n to the s i n g l e t s t a t e . This s h o r t - l i v e d s t a t e (^10 sec) i s quenched by r a p i d energy t r a n s f e r to c h l o r o p h y l l i n the reaction centers. I f unquenched, intersystem c r o s s i n g may lead to the generation of the longer l i v e d t r i p l e t s t a t e (^10~3 s e c ) .

0097-6156/82/0181 -0057$05.00/0 © 1982 American Chemical Society Moreland et al.; Biochemical Responses Induced by Herbicides ACS Symposium Series; American Chemical Society: Washington, DC, 1982.

58

BIOCHEMICAL RESPONSES INDUCED BY HERBICIDES

ί

.S.C

l

Chl + hv

3

Chl

Chl

T r i p l e t c h l o r o p h y l l can be harmlessly quenched by c h i o r o p l a s t carotenoid pigments (2) d i s s i p a t i n g the e x c i t a t i o n energy (3). I f t r i p l e t c h l o r o p h y l l i s unquenched, energy t r a n s f e r from t h i s pigment t o ground s t a t e oxygen may generate s i n g l e t oxygen ( Û 2 ) . T h i s i s g e n e r a l l y termed a type 2 r e a c t i o n . 1


3

3

Chl + 0

^

2

Chl +

0

l

2

S i n g l e t oxygen may a l s o be quenched by cartenoids (4) and by f r e e r a d i c a l scavengers l o c a t e d w i t h i n the c h i o r o p l a s t t h y l a k o i d s , such as α-tocopherol (5). During a c t i v e photosynthesis, oxygen concentrations w i t h i n the c h i o r o p l a s t may be higher than the surrounding cytoplasm (6) and e l e c t r o n leakage from the thylakoids could y i e l d the superoxide anion r a d i c a l (θ£~) (7). I t i s p o s s i b l e that t h i s could be formed during normal p s e u d o c y c l i c e l e c t r o n t r a n s p o r t (8). Although the superoxide r a d i c a l i s apparently l e s s t o x i c than s i n g l e t oxygen, i t s t o x i c i t y may be r e l a t e d to the generation of more t o x i c species such as hydroxyl f r e e (OH*) r a d i c a l s . The c h i o r o p l a s t possesses an e f f i c i e n t superoxide scavenging system i n the form o f Cu-Zn superoxide dismutase (SOD) (9) to p r o t e c t against t h i s p o t e n t i a l t o x i c species. Of

+ 0 2 ~ + 2H

+

S

Q

D

»» H 0 2

2

+0

2

The dismutating a c t i v i t y of bound manganese ( 1 0 ) may a l s o be important. The generation o f hydrogen peroxide i n t h i s r e a c t i o n may be t o l e r a t e d by the presence of a d d i t i o n a l enzyme systems that c a t a l y s e the d e s t r u c t i o n of H2O2 (11): ( i ) ascorbate peroxidase, ( i i ) dehydroascorbate reductase, and ( i i i ) g l u t a t h i o n e reductase. Η

2θ2^ν

H 0^ 2

(i)

^.Ascorbate

^-^glutathione

*Dehydroascorbate>^glutathione (ii)

(ΟΧ)-ν.

•NADPH

( r e d ) i f *NADP

+

(iii)

The p o t e n t i a l hazards of oxygen and l i g h t might seem to be exacerbated by low carbon d i o x i d e concentrations w i t h i n the chioroplast. This might be minimized by p h o t o r e s p i r a t i o n (12) whereby under low carbon d i o x i d e concentrations, oxygen r e a c t s with the carbon d i o x i d e acceptor molecule r i b u l o s e bisphosphate to form 3-phosphoglycerate and 2-phosphoglycollate. Further metabolism of phosphoglycollate r e c y c l e s carbon d i o x i d e to the c h i o r o p l a s t (13).

Moreland et al.; Biochemical Responses Induced by Herbicides ACS Symposium Series; American Chemical Society: Washington, DC, 1982.

4.

DODGE

Photosynthetic Inhibitor Herbicides


E l e c t r o n Transport

59

Inhibitors

A large number of h e r b i c i d e s i n c l u d i n g the phenylureas, ^ - t r i a z i n e s , u r a c i l s , triazinones, hydroxybenzonitriles, pyridazinones, and a c y l a n i l i d e s i n h i b i t photosynthetic e l e c t r o n t r a n s p o r t ( H i l l Reaction). The s i t e of a c t i o n i s g e n e r a l l y thought to be a p r o t e i n component l o c a t e d on the outside of the t h y l a k o i d membrane (14) and a f f e c t i n g a p o i n t between the h y p o t h e t i c a l Q and Β components of the e l e c t r o n transport chain. As a r e s u l t of t h i s i n t e r a c t i o n , e l e c t r o n transport ceases. This leads to a r a p i d i n h i b i t i o n of carbon d i o x i d e f i x a t i o n that proceeds at a s i m i l a r r a t e i r r e s p e c t i v e of whether the leaves are incubated i n darkness or l i g h t (15) (Table I ) . An i n t e r r u p t i o n of photosynthesis w i l l e v e n t u a l l y lead to a r e d u c t i o n of food reserves and subsequent s t a r v a t i o n . The appearance of phytot o x i c symptoms, such as c h l o r o p h y l l bleaching, i s c l e a r l y promoted by l i g h t (L5, _16, 17) (Figure 1). The i n h i b i t i o n of e l e c t r o n flow w i l l prevent photosynthetic oxygen e v o l u t i o n , but the c h i o r o p l a s t envelope probably provides l i t t l e r e s i s t a n c e to inward oxygen d i f f u s i o n . Experiments have demonstrated that with both monuron and i o x y n i l , i n c u b a t i o n of cotyledons under argon reduced, but d i d not prevent the r a p i d d e s t r u c t i o n of c h l o r o p h y l l (Figure 2) (18). Promotion of the t o x i c a c t i o n of photosynthetic i n h i b i t o r h e r b i c i d e s by l i g h t may be i n i t i a l l y a s c r i b e d to type 1 reactions. T r i p l e t c h l o r o p h y l l , without the involvement of oxygen, may d i r e c t l y i n i t i a t e e l e c t r o n or hydrogen a b s t r a c t i o n from p a r t i c u l a r l y s u s c e p t i b l e molecules (e.g., unsaturated f a t t y acids (LH)) to y i e l d l i p i d f r e e r a d i c a l s .

LH

L-

Once i n i t i a t e d , subsequent propagation r e a c t i o n s i n v o l v i n g oxygen may generate more f r e e r a d i c a l s that a t t a c k unsaturated l i p i d s i n a chain r e a c t i o n of gathering momentum.

L" + 0

L02*

2

L0 * + LH 2

»» L* + LOOH

The production of l i p i d hydroperoxides (LOOH) a l s o may be achieved by the d i r e c t i n t e r a c t i o n of s i n g l e t oxygen with s a t u r a t e d f a t t y acids (19).

LH +

0

L

2

LOOH


un


60


TABLE I Carbon d i o x i d e f i x a t i o n by f l a x cotyledons measured by an IRGA with i l l u m i n a t i o n of 115 Wm , p r e v i o u s l y incubated with 1 0 M monuron i n the dark or l i g h t of 5.25 or 30 Wm"", from P a l l e t t and Dodge (15) -2

_3

2

Incubation Time (Min)

ymol C02/g.F.Wt./h Dark

5.25

2

Wm'

2

30 WnT

0

68.0

68.0

68.0

15

18.6

11.1

15.4

30

3.2

3.5

2.2

60

2.3

1.9

0.9

120

0.0

0.0

0.0




DODGE

Figure 1. The chlorophyll content of flax cotyledons incubated on water (A) or 10' M monuron (B), in the dark (Φ) or with light of 5.25 Wm' (A) or 30 Wrn «Π5λ 3

2


2



o-i

.

0

48

H 96

Incubation Time (h)

Figure 2. The effect of a 10 M solution of ioxynil (A) or monuron (B) on the chlorophyll content of flax cotyledons incubated in sealed conicalflaskscontaining air (%) or argon (O)with light of 30 Wm (IS). 3

2



4.

DODGE


63

C h i o r o p l a s t t h y l a k o i d membranes are composed of an almost equal percentage of p r o t e i n and l i p i d . The a c y l l i p i d s of the c h i o r o p l a s t membrane a r e h i g h l y unsaturated; f o r example, around 80% of the f a t t y a c i d component i s the 18:3 unsaturated l i n o l e n i c a c i d . The consequences of l i p i d p e r o x i d a t i o n r e a c t i o n s are (a) the promotion of membrane d e s t r u c t i o n which i n part may be v i s i b l y demonstrated as c h l o r o p h y l l l o s s , and observed by e l e c t r o n microscopy as a d i s o r g a n i z a t i o n of t h y l a k o i d s and other c e l l u l a r membranes (18); and (b) the l i p i d hydroperoxides undergo fragmentation producing short chain hydrocarbons such as ethane (20, 21). Experiments with both monuron and i o x y n i l showed that the l o s s of c h l o r o p h y l l i n f l a x cotyledons was preceded by the breakdown of carotenoid pigments, e s p e c i a l l y the carotenes, suggesting that t h i s p r o t e c t i v e system was over-taxed and destroyed. This was followed by a r a p i d formation of ethane (18) (Figures 3 and 4). Experiments i n which monuron t r e a t e d leaves were t r e a t e d with the s i n g l e t oxygen quencher DABCO ( d i a z o b i c y c l o octane) showed a l i m i t e d c o n t r o l of c h l o r o p h y l l breakdown (22) (Table I I ) . Many experiments i n t o the secondary e f f e c t s of photos y n t h e t i c i n h i b i t o r h e r b i c i d e s have been performed with i s o l a t e d chloroplasts. I s o l a t e d c h l o r o p l a s t s provide a convenient system f o r studying the generation and quenching o f s i n g l e t oxygen. Recent experiments with pea c h l o r o p l a s t s i l l u m i n a t e d i n the absence of an e l e c t r o n acceptor have shown that both c h l o r o p h y l l and l i n o l e n i c a c i d breakdown was retarded by the s i n g l e t quenchers DABCO and c r o c i n (23). Further work showed that l i n o l e n i c a c i d breakdown and ethane generation i n i s o l a t e d c h i o r o p l a s t t h y l a k o i d s was promoted by the a d d i t i o n of the s i n g l e t oxygen generator rose bengal immobilized on DEAE-sepharose (24). Divertors of Electron

Transport

The i n t e r a c t i o n of b i p y r i d y l h e r b i c i d e s (paraquat and diquat) with photosynthesis i s d i f f e r e n t from that of the e l e c t r o n transport i n h i b i t o r s . These compounds, with h i g h l y negative redox p o t e n t i a l s (paraquat E ^ " 446mV; diquat E Q 349mV), i n t e r a c t i n the v i c i n i t y of f e r r e d o x i n causing a d i v e r s i o n o f e l e c t r o n flow from the u l t i m a t e e l e c t r o n acceptor NADP . This was c l e a r l y seen i n paraquat-treated p l a n t m a t e r i a l as a progressive i n h i b i t i o n of carbon dioxide uptake (25) (Figure 5). Although carbon d i o x i d e uptake r a p i d l y ceased, e l e c t r o n flow from water continued f o r some time u n t i l t h i s system was t o t a l l y i n a c t i v a t e d by the general d e s t r u c t i o n of c e l l u l a r i n t e g r i t y (25). Paraquat (and/or diquat) i s reduced by a one e l e c t r o n t r a n s f e r t o give the paraquat f r e e - r a d i c a l . Under anaerobic c o n d i t i o n s t h i s r a d i c a l can accumulate (26, 27). However, i n the presence of oxygen, which should be p l e n t i f u l i n the v i c i n i t y o f the t h y l a k o i d i n the e a r l y stages of paraquat




Incubation time (h)

Figure 3. The effect of 10' M monuron on pigment content and ethane generation of flax cotyledons incubated at 30 Wm' . Pigment levels are expressed as a percent age of the levels at 0 h. Key: carotenes, ·; xanthophylls, A; chlorophyll, |; and ethane generation, Ο (IS). 3

2



DODGE


Incubation time (h)

Figure 4. The effect of 10~ M ioxynil on pigment content and ethane generation of flax cotyledons incubated at 5.25 Wm . Pigment levels are expressed as a per centage of the levels at 0 h. Key: carotenes, ·; xanthophylls, A; chlorophyll, |/ and ethane generation, Ο (IS). 3

2




66

TABLE I I The e f f e c t o f DABCO ( 1 0 " % ) on the c h l o r o p h y l l content of f l a x cotyledons incubated on monuron ( 1 0 " % ) f o r 96 h a t 5.25 Wm", from Youngman e t a l . (22) 2

Treatment

mg c h l o r o p h y l l / g . f r e s h wt.

Water

1.735

Monuron

1.184

DABCO

1.610

Monuron + DABCO

1.598



4.

DODGE


67

Hours Paraquat Treatment

Figure 5. Carbon dioxide uptake and evolution by paraquat-treatedflaxcotyledons, incubated on paraquat (10~ M) in either light of 5.25 Wm (O) or darkness (%). The uptake and evolution of the cotyledons were estimated after treatment 4

(25).


2

68


treatment, the reduced paraquat was superoxide : PQ

PQ'

+

2 +

+ 0

r a p i d l y r e o x i d i z e d to y i e l d

+ e"

2

PQ'

+

PQ

2 +

+

0 " 2


The a c t i v i t y of these h e r b i c i d e s i s known to be promoted by oxygen (28, 29, 30). I t has a l s o been demonstrated that c h l o r o s i s i s promoted by i n c r e a s i n g l i g h t (see Figure 11 f o r Conyza) but diminished i n the presence of an e l e c t r o n transport i n h i b i t o r (28) (Figure 6). A d d i t i o n a l l i n e s of evidence f u r t h e r i n d i c a t e the importance of superoxide i n the a c t i o n of these h e r b i c i d e s . I t has been shown with i s o l a t e d c h l o r o p l a s t s that the production of super oxide, as measured by the conversion of hydroxylamine to n i t r i t e , was promoted by paraquat and r e s t r a i n e d by superoxide dismutase (21) (Figure 7). The generation of superoxide was l i m i t e d i f an e l e c t r o n transport i n h i b i t o r such as monuron was present (Table I I I ) . Although the c h i o r o p l a s t contains superoxide dismutase enzymes, i t i s assumed that the r a p i d generation of 0 ~ overtaxes the c a p a b i l i t i e s of the enzymes. Further experiments with whole leaves and the superoxide scavenger copper p e n i c i l l a m i n e (31) showed that the presence of t h i s compound not only m i t i g a t e d the a c t i o n of the h e r b i c i d e i n promoting c h l o r o p h y l l decay (32) (Figure 8), but a l s o l i m i t e d l i p i d p e r o x i d a t i o n as shown by the diminished r e l e a s e of ethane (33) (Figure 9). The f e a s i b i l i t y of the superoxide r a d i c a l being the i n i t i a l t o x i c species i n v i v o was p r e d i c t e d by F a r r i n g t o n et a l . , (34) using pulse r a d i o l y s i s s t u d i e s . I t was p o s t u l a t e d that the concentra t i o n of superoxide w i t h i n the p l a n t c e l l could remain constant at 1 μΜ up to 10 ym or more from the c h i o r o p l a s t t h y l a k o i d membrane. 2

Although i t was thought i n i t i a l l y that superoxide i t s e l f could i n t e r a c t with membrane l i p i d s to i n i t i a t e l i p i d per o x i d a t i o n , more recent evidence has expressed doubt on the p o t e n t i a l r e a c t i v i t y of t h i s molecule to induce t h i s process (35). Much d i s c u s s i o n has centered on the p o s s i b l e involvement of Fenton and Haber-Weiss type r e a c t i o n s o c c u r r i n g i n v i v o and generating more t o x i c species such as hydroxyl f r e e r a d i c a l s and s i n g l e t oxygen. At present i t i s not p o s s i b l e to a f f i r m that such systems operate (36, 37). However, i t might be p o s s i b l e f o r the reduced paraquat r a d i c a l to i n t e r a c t with superoxide to generate hydrogen peroxide, a w e l l known product of reduced paraquat r e o x i d a t i o n (38). 2H PQ*

+

+ 0

2

PQ

2 +

+ 0

2

+

H 0 2

2



4.

DODGE

69


Figure 6. The effect of monuron (ΙΟ M) on the chlorophyll level of paraquattreated (10~ M) cotyledons under light of 5.25 Wm' . Key: paraquat, O; and para quat plus monuron, |3

4

2




Illumination Time

(mins)

Figure 7. Nitrite formation from hydroxylamine. Reaction mixture contained in 3 mL: 50 mM phosphate buffer pH 7.8; 1 μτηοΐ of NH OH; chloroplasts with 75 ng of chlorophyll and where indicated 6.6 Μ paraquat; 50 units SOD. Illuminated at 275 Wm' at 22°C. Key: control, •; plus paraquat, A; plus SOD, •; and plus paraquat and SOD, Δ (22). 2

μ

2



4.

DODGE

71


TABLE I I I The e f f e c t of monuron (lCT^M) n the a b i l i t y of paraquat to promote the formation of n i t r i t e from hydroxylamine i n i s o l a t e d chloroplasts. F o r f u r t h e r d e t a i l s see legend to Figure 7, from Youngman et_ a l . (32) Q

Treatment

Water (nmoles n i t r i t e / m g

Monuron chlorophyll/hr)

Control

100

17

Paraquat

195

28



72


24

48

Illumination Time (h)

Figure 8. The chlorophyll content of paraquat-treatedflaxcotyledons incubated in the presence or absence of copper-penicillamine (PA-Cu) under light of 5.25 Wm' . The final concentration of paraquat was 10 M and the PA-Cu represented 50 units of superoxide dismutase. Key: control, paraquat plus PA-Cu, A ; and paraquat, Φ (32). 2

s

Illumination Time (h)

Figure 9. Ethane generation byflaxcotyledons incubated inflasksunder light of 5.25 Wm' . Thefinalconcentration of paraquat was 10' M and the copper-peni cillamine (PA-Cu) represented 50 units of superoxide dismutase. Key: control, ·; paraquat, A / and paraquat plus PA-Cu, |f33J. 2

6


4.

DODGE


73

Further i n t e r a c t i o n of reduced paraquat w i t h hydrogen peroxide could y i e l d the more r e a c t i v e hydroxyl f r e e r a d i c a l (39) which could i n i t i a t e l i p i d p e r o x i d a t i o n i n membrane f a t t y a c i d s .

+

PQ* + H 0


2

2

^PQ

2

+

+ 0H~ +

OH"

E l e c t r o n microscope s t u d i e s of paraquat-treated leaves showed that a f t e r a few hours, membranes had been d i s r u p t e d and c e l l u l a r compartmentalization was destroyed. Experiments demonstrating the r e l e a s e of potassium from t r e a t e d t i s s u e as an i n d i c a t i o n of plasmalemma and tonoplast d i s r u p t i o n (25) (Figure 10) corresponded i n time with the v i s i b l e demonstration of c e l l u l a r d i s o r g a n i z a t i o n (40). I f the i n i t i a l a c t i o n of the h e r b i c i d e s i s to i n d i r e c t l y promote l i p i d p e r o x i d a t i o n of membrane unsaturated f a t t y a c i d s and lead to c e l l u l a r d i s o r g a n i z a t i o n , then subsequent d e t e r i o r a t i v e changes w i l l occur because of the r e l e a s e of vacuolar contents. Not only w i l l there be a r a p i d change i n the osmotic p r o p e r t i e s of the c e l l , but the r e l e a s e of vacuolar h y d r o l y t i c enzymes w i l l cause f u r t h e r damage. In a d d i t i o n , type 1 and type 2 s e n s i t i z e d r e a c t i o n s may a l s o i n c r e a s e and c o l l e c t i v e l y these changes w i l l l e a d to r a p i d p l a n t death. Although paraquat i s used as a broad spectrum t o t a l - k i l l h e r b i c i d e , t o l e r a n c e has been found i n c e r t a i n l i n e s of Lolium perenne (41) and the weed Conyza (42) (Figure 11) . In both i n s t a n c e s , t o l e r a n t l i n e s showed a l a c k of e f f e c t on carbon d i o x i d e f i x a t i o n , i n d i c a t i n g reduced p e n e t r a t i o n of h e r b i c i d e (42, 43) (Figure 12). T o l e r a n t l i n e s of Lolium perenne were nevertheless shown to possess greater superoxide dismutase a c t i v i t y as w e l l as greater c a t a l a s e and peroxidase a c t i v i t i e s (44). T o l e r a n t Conyza biotypes showed approximately t h r e e - f o l d increases i n superoxide dismutase a c t i v i t y (42). Conclusion The p h y t o t o x i c a c t i o n of both e l e c t r o n transport i n h i b i t o r and e l e c t r o n d e v i a t o r h e r b i c i d e s i s promoted by l i g h t and i s l a r g e l y a response to the overtaxing of p r o t e c t i v e systems. In both i n s t a n c e s , type 1 r e a c t i o n s , i m p l i c a t i n g the d i r e c t a c t i o n of e x c i t e d t r i p l e t c h l o r o p h y l l , may be i n v o l v e d . However, of greater p o t e n t i a l importance i s the i n t e r a c t i o n of a c t i v e oxygen s p e c i e s . With e l e c t r o n t r a n s p o r t i n h i b i t o r s , s i n g l e t oxygen i s produced as an i n c i d e n t a l response to unquenched t r i p l e t c h l o r o p h y l l . With e l e c t r o n d e v i a t o r h e r b i c i d e s , the generation of superoxide i s a d i r e c t consequence of the d i v e r s i o n of e l e c t r o n flow (Figure 13). Once membrane d i s r u p t i o n i s




3

6

9

Hours Paraquat Treatment

Figure 10. Membrane permeability measured as potassium leakage from slices of paraquat-treated (10~ M)flaxcotyledons (25). 4

v

2.0

5 LL CD

—?4h ^ ^ B i o t y p e il

1.5

B

"48h

Ε

S

1.01

c Ο ϋ

] | 0.5

α ο ο .C ο

24 Biotype l

10 Light

Intensity

40

30

20 (W

m" ) 2

Figure 11. The chlorophyll content of leaf sections of two biotypes of Conyza treated for 24 or 48 h with paraquat at 10~ M , at various light intensities (41). 5


75



4. DODGE

Figure 13. Summary scheme of the primary effects caused by A, photosynthetic inhibitor herbicides and B, photosynthetic deviator herbicides. 0 is triplet or ground state oxygen; PQ represents paraquat. 3

2



76

i n i t i a t e d by l i p i d p e r o x i d a t i o n , and death f o l l o w s .

rapid c e l l u l a r

disorganization


Literature Cited 1. Franck, J. "Photosynthesis in Plants"; The Iowa State College Press: Iowa, 1949; p 293. 2. Krinsky, N.I. Pure and Appl. Chem. 1979, 51, 649. 3. Wolff, Ch.; Witt, H.T. Z. Naturforsch. 1969, 246, 1031. 4. Foote, C.S.; Denny, R.W. J. Am. Chem. Soc. 1968, 90, 6233. 5·. Hughes, C.T.; Gaunt, J.K.; Laidman, D.L. Biochem. J . 1971, 124, 9p. 6. Steiger, H.M.; Beck, E.; Beck, R. Plant Physiol. 1977, 60, 903. 7. Marsho, T.V.; Behrens, P.W.; Radmer, R.J. Plant Physiol. 1979, 64, 656. 8. Elstner, E.F.; Stoffer, C.; Heupel, A. Z. Naturforsch. 1975, 30C, 53. 9. Asada, K.; Urano, M.; Takahashi, M. Eur. J. Biochem. 1973, 36, 257. 10. Foyer, C.H.; Hall, D.O. FEBS Lett. 1979, 101, 324. 11. Halliwell, B.; Foyer, C.H.; Charles, S.A. Proc. 5th Int. Congr. Photosynth.: Halkidiki, Greece, 1981; in press. 12. Heber, V.; Krause, G.H. TIBS 1980, 5, 32. 13. Chollet, R. TIBS, 1977, 2, 155. 14. Renger, G. Biochim. Biophys. Acta 1976, 440, 287. 15. Pallett, K.E.; Dodge, A.D. Z. Naturforsch. 1979, 34C, 1058. 16. Minshall, W.H. Weeds, 1957, 5, 29. 17. Oorschot, J.L.P. Van; Leeuwen, P.H. Van. Weed Res. 1974, 14, 81. 18. Pallett, K.E.; Dodge, A.D. J. Exp. Bot. 1980, 31, 1051. 19. Rawls, H.R.; Santen, P.J. Van. J . Am. Oil. Chem. Soc. 1970, 47, 121. 20. Riely, C.A.; Cohen, G.; Liebermann, M. Science 1974, 183, 208. 21. Elstner, E.F.; Konze, J.R. Nature 1976, 263, 351. 22. Youngman, R.J.; Pallett, K.E.; Dodge, A.D. "Chemical and biochemical aspects of superoxide and superoxide dismutase". Elsevier/North Holland: New York, 1980; p 402. 23. Percival, M.; Dodge, A.D. (in preparation). 24. Percival, M.; Dodge, A.D. Proc. 5th Int. Congr. Photosynth.: Halkidiki, Greece, 1981; in press. 25. Harris, N.; Dodge, A.D. Planta 1972, 104, 210. 26. Zweig, G.; Shavit, Ν.; Avron, M. Biochim. Biophys. Acta 1965, 109, 332. 27. Dodge, A.D. Endeavour 1971, 30, 130. 28. Mees, G.C. Ann. Appl. Biol. 1960, 48, 601. 29. Merkle, M.G.; Leinweber, C.L.; Bovey, R.W. Plant Physiol. 1965, 40, 832.



4.

DODGE


77

30. Rensen, J.J.S. van. Physiol. Plant 1975, 33, 42. 31. Lengfelder, E.; Elstner, E.F. Hoppe-Seylers Z. Physiol. Chem. 1978, 359, 751. 32. Youngman, R.J.; Dodge, A.D. Z. Naturforsch. 1979, 34C, 1032. 33. Youngman, R.J.; Dodge, A.D.; Lengfelder, E.; Elstner, E.F. Experientia. 1979, 35, 1295. 34. Farrington, J.A.; Ebert, M.; Land, E.J.; Fletcher, K. Biochim. Biophys. Acta 1973, 314, 372. 35. Bors, W.; Saran, M.; Lengfelder, E.; Spöttl, R.; Michel, C. Curr. Top. Radiat. Res. 1974, 9, 247. 36. Halliwell, B. FEBS Lett. 1976, 72, 8. 37. Koppenol, W.H.; Butler, J.; Leeuwen, J.W. van. Photochem. Photobiol. 1978, 28, 655. 38. Davenport, H.E. Proc. R. Soc. B. 1963, 157, 332. 39. Farrington, J.A. Proc. Brit. Crop. Prot. Conf. 1976, 225. 40. Harris, N.; Dodge, A.D. Planta 1972, 104, 201. 41. Harvey, B.M.R.; Muldoon, J.; Harper, D.B. PI. Cell Environ. 1978, 1, 203. 42. Youngman, R.J.; Dodge, A.D. Proc. 5th Int. Congr. Photosynth.: Halkidiki, Greece, 1981; in press. 43. Harvey, B.M.R.; Fraser, T.W. Pl. Cell. Environ. 1980, 3, · 44. Harper, D.B.; Harvey, B.M.R. P l . Cell. Environ. 1978, 1, 211. RECEIVED September 2, 1981. 1 0 7


Biochemical Responses Induced by Herbicides - American Chemical

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