Phytoalexins and Their Potential Role in Control of Insect Pests

Chapter 13

Phytoalexins and Their Potential Role in Control of Insect Pests

Downloaded by UNIV OF GUELPH LIBRARY on March 13, 2013 | http://pubs.acs.org Publication Date: January 9, 1991 | doi: 10.1021/bk-1991-0449.ch013

Jack D. Paxton Department of Plant Pathology, University of Illinois, 1102 S. Goodwin, Urbana, IL 61801

Plant phytoalexins [natural plant a n t i b i o t i c s ] [1] have the p o t e n t i a l of becoming a new c l a s s of u s e f u l compounds i n the c o n t r o l of insect p e s t s . Some phytoalexins have been demonstrated as d e t e r r e n t s to i n s e c t f e e d i n g . C o n s i d e r a b l e p r o g r e s s has been made to c h a r a c t e r i z e them c h e m i c a l l y and t o extend the study of t h e i r function in plant disease resistance, but e x p l o r a t i o n of t h e i r r o l e i n the c o n t r o l of i n s e c t pests i s just beginning.

Plant

Defenses

Against

Stresses

Plants have developed many responses a n d ways o f defending themselves against attacks by pathogens and i n s e c t s . Some o f t h e s e d e f e n s e s a r e p r e f o r m e d s u c h a s t h e plant cuticle, which provides a barrier against desiccation a n d which possibly even creates an i n h o s p i t a b l e environment f o rvarious pathogens. Another preformed defense against s t r e s s i s l i g n i f i c a t i o n o f c e l l walls. This creates a physical barrier t o mechanical p e n e t r a t i o n b y f u n g i o r i n s e c t mouthparts, however, t h e m o s t common p r e f o r m e d d e f e n s e t h a t h a s b e e n s t u d i e d t o date i s t h e accumulation o f chemical deterrents (allomones) [ 2 ] . In preformed defenses t h e p l a n t i n v e s t s considerable energy a n dother metabolic resources i na generalized d e f e n s e a g a i n s t some s t r e s s e s t h a t may n e v e r m a t e r i a l i z e . 0097-6156/91Λ)449-0198$06.00Λ) © 1991 American Chemical Society In Naturally Occurring Pest Bioregulators; Hedin, P.; ACS Symposium Series; American Chemical Society: Washington, DC, 1991.


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199

T h e s e d e f e n s e s h a v e t h e a d v a n t a g e o f b e i n g i n p l a c e when the insect arrives at the plant thereby preventing a p p r e c i a b l e damage t o t h e p l a n t . A p o s s i b l e disadvantage i s t h a t a c o n s i d e r a b l e amount o f t h e p l a n t ' s resources a r e d e v o t e d t o a d e f e n s e t h a t may n o t b e n e c e s s a r y and which might u l t i m a t e l y reduce i t ' s a b i l i t y t o reproduce and compete f o r an e c o l o g i c a l n i c h e and r e s o u r c e s . Between preformed ( c o n s t i t u t i v e ) and inducible defenses exists a wide range o f compounds t h a t a r e e s s e n t i a l l y p r e f o r m e d , b u t s t o r e d i n an i n a c t i v e f o r m u n t i l damage o c c u r s t o t h e c e l l . An e x a m p l e o f t h i s i s juglone, a 5-hydroxy naphthoquinone t h a t i s accumulated as i t s 4 - g l u c o s i d e i n m e m b e r s o f t h e J u g l a n d a c e a e [2.] . Upon i n j u r y of the c e l l , b-glucosidases i n the cell release the aglucone hydrojuglone, which i s then r a p i d l y oxidized t o juglone by a i r and p l a n t cell oxidases. Juglone, f o r example, i s a potent a n t i f e e d a n t t o Scolytus m u l t i s t r i a t u s [£_] . H y d r o j u g l o n e i s r e l a t i v e l y non-toxic c o m p a r e d t o j u g l o n e [£]. A n o t h e r compound b o r d e r i n g between preformed and i n d u c e d d e f e n s e s i s g o s s y p o l . T h i s compound a c c u m u l a t e s within epidermal g l a n d s on t h e s u r f a c e o f c o t t o n p l a n t s a n d i s v e r y t o x i c t o some i n s e c t s [£.] . G o s s y p o l , and a series of structurally r e l a t e d c o m p o u n d s o n t h e same biosynthetic pathway, accumulate to substantially i n c r e a s e d l e v e l s i n p l a n t s t h a t have been c h a l l e n g e d by potential pathogens. For this reason they have been considered phytoalexins by some plant pathologists. Phytoalexins are inducible antibiotics and w i l l be discussed later. I n d u c i b l e d e f e n s e s have t h e advantage o f d i v e r t i n g p l a n t m e t a b o l i c r e s o u r c e s t o d e f e n s e o n l y when a n i n s e c t o r p a t h o g e n a t t a c k a c t u a l l y o c c u r s . W h i l e some t i s s u e may be damaged a n d l o s t , a r e s p o n s e t o t h e i n s e c t o r p a t h o g e n can prevent significant damage t o t h e p l a n t , without d i v e r t i n g t h e same a m o u n t o f r e s o u r c e s t h a t w o u l d be r e q u i r e d f o r p r e f o r m e d d e f e n s e s . F u r t h e r m o r e , some o f t h e p r e f o r m e d compounds t h a t seem t o p l a y a s i g n i f i c a n t r o l e i n d e f e n s e a g a i n s t f e e d i n g o f some i n s e c t s , a c t u a l l y a r e used as 'keys' t o f e e d i n g o n t h e same p l a n t b y other i n s e c t s t h a t a t t a c k t h a t p a r t i c u l a r p l a n t [2] . Plant

Defenses Against

Insects

Plants have evolved a number of different defenses a g a i n s t i n s e c t s . One p r o m i n e n t d e f e n s e i s h a i r s o r o t h e r s t r u c t u r e s which cover t h e surface o f t h e p l a n t and deter insect feeding. Another i s accumulation of allomones (compounds t h a t s e r v e t o d e t e r f e e d i n g o r o v i p o s i t i o n o r are otherwise toxic to the insect), especially i n c r i t i c a l p l a n t p a r t s such as t h e r e p r o d u c t i v e s t r u c t u r e s .

In Naturally Occurring Pest Bioregulators; Hedin, P.; ACS Symposium Series; American Chemical Society: Washington, DC, 1991.

200

NATURALLY OCCURRING PEST BIOREGULATORS

Immature seeds a n d t h e i r seed c o a t s a r e o f t e n a good source o f such compounds. As an example, w a l n u t trees c o n t a i n t h e r i c h e s t source o f hydrojuglone glucoside i n young growing p a r t s and i n t h e p e r i c a r p s u r r o u n d i n g t h e s e e d [2.] ·


Preformed

Compounds

A w i d e r a n g e o f c o m p o u n d s a r e now k n o w n t o a c c u m u l a t e i n plants and serve as allomones t o some insects and kairomones (feeding attractants o r excitants) t o other i n s e c t s [2J . A n e x a m p l e o f s u c h a c o m p o u n d i s g l a u c o l i d e A, a g e r m a c r a n o l i d e type sesquiterpene lactone found i n Vernonia spp. G l a u c o l i d e A h a s a n t i f e e d a n t a c t i o n a g a i n s t some L e p i d o p t e r a . But other Lepidoptera, such as t h e cabbage looper [Trîchoplusia ni] and t h e yellow woollybear [Spilosoma virginica] actually prefer Vernonia spp. w i t h t h i s compound [ 2 ] .

I n d u c i b l e Compounds

W h i l e i n d u c i b l e compounds t h a t d e t e r i n s e c t f e e d i n g have not been w i d e l y s t u d i e d , some i n t e r e s t i n g e x a m p l e s o f these compounds a r e known. A proteinase inhibitor i n d u c i n g f a c t o r ( P I I F ) , d i s c o v e r e d b y Ryan i n wounded tomatoes, has been extensively studied i n insect resistance [£_] . P I I F a c t i v i t y has been i s o l a t e d from t o m a t o l e a v e s a s a s i n g l e , b r o a d S e p h a d e x G-50 p e a k w i t h a Mr r a n g e o f 5,000-10,000 a n d i s p r i m a r i l y c a r b o h y d r a t e . PIIF can e l i c i t the accumulation o f two proteinase i n h i b i t o r s i n wounded tomato l e a v e s a n d t h e s e inhibitors i n t e r f e r e with p r o t e i n d i g e s t i o n by i n s e c t s . I n h i b i t o r I has a m o l e c u l a r r a t i o o f 41,000 a n d i s a p e n t a m e r . E a c h subunit has an a c t i v e s i t e , specific f o r inhibiting chymotrypsin, w i t h a K i o f a b o u t 10~^M. I n h i b i t o r I I i s a dimer with a molecular ratio o f 23,000 a n d s t r o n g l y i n h i b i t s both t r y p s i n and chymotrypsin with K i values o f a b o u t 10"~ a n d 10"" M r e s p e c t i v e l y [jl] . F u r t h e r m o r e , p l a n t and fungal c e l l w a l l fragments a c t i v a t e expression o f p r o t e i n a s e i n h i b i t o r genes f o rp l a n t defense j u s t like they a c t i v a t e phytoalexin accumulation . C a r r o l l a n d Hoffman [ H J presented evidence that a feeding stimulant f o r Acalymma vittata i s rapidly m o b i l i z e d i n t o d a m a g e d C u c u r j b i t a moschata l e a v e s . These same l e a v e s r a p i d l y accumulate a feeding inhibitor of Epilachna tredecimnotata. This plant response i s circumvented b y Epilachna tredecimnotata by trenching around t h e leaf area t o be eaten, prior t o feeding. 8

7


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Unfortunately the active compounds have not been chemically characterized. A n o t h e r g r o u p o f i n d u c i b l e compounds t h a t probably have an important role i n plant insect resistance i s phytoalexins.


Phytoalexins

Phytoalexins a r e low molecular weight, a n t i m i c r o b i a l compounds t h a t a r e b o t h s y n t h e s i z e d b y a n d a c c u m u l a t e d i n plants after exposure t o microorganisms [1_] . S e v e r a l l i n e s o f e v i d e n c e s u g g e s t t h a t t h e s e compounds have an important r o l e i n p l a n t disease and pest r e s i s t a n c e [12J. Phytoalexins f r o m many d i f f e r e n t p l a n t s h a v e b e e n chemically characterized. The phytoalexins include isoflavanoid-derived pterocarpan compounds c h a r a c t e r i s t i c of the Leguminosae, sesquiterpenoid compounds c h a r a c t e r i s t i c o f t h e S o l a n a c e a e , p h e n a n t h r e n e compounds characteristic of the Orchidaceae and acetylenic compounds c h a r a c t e r i s t i c o f t h e C o m p o s i t a e . G l y c e o l l i n , a p h y t o a l e x i n o f soybeans, accumulates as a s e r i e s of isomers first identified by Lyne e t al. [lu]; t h e t h r e e m o s t common i s o m e r s a r e s h o w n i n F i g u r e 1. P l a n t s f r e q u e n t l y p r o d u c e a s e r i e s o f a c t i v e isomers of related phytoalexins, and soybeans a r e a u s e f u l e x a m p l e [JLA] . Phytoalexins

as Insect

Feeding

Deterrents

In t h e f i r s t work t o i m p l i c a t e p h y t o a l e x i n s i n f e e d i n g deterrent a c t i v i t y o f p l a n t s , R u s s e l l et a l . [ l u ] found t h a t 3 R - ( - ) - v e s t i t o l a n d s a t i v a n f r o m Lotus pendunculatus leaf e x t r a c t s were major deterrents f o r Costelytra zealandica larvae. Furthermore pastures c o n t a i n i n g as l i t t l e a s 2 0 % Lotus pendunculatus were r e l a t i v e l y f r e e o f t h i s insect pest. V e s t i t o l h a d a n ED50 w i t h Costelytra zealandica larvae o f about 8.5 μg/g o f medium a n d f e e d i n g was completely i n h i b i t e d a t 100 μg/g o f m e d i u m . Vestitol however could not account f o r a l lof the feeding deterrency o f t h e Lotus e x t r a c t s , and s a t i v a n was i m p l i c a t e d i n t h i s a d d i t i o n a l a c t i v i t y . The d u a l f u n c t i o n of v e s t i t o l as a p h y t o a l e x i n and i n s e c t f e e d i n g d e t e r r e n t i s o f e c o l o g i c a l i n t e r e s t . I t must s t i l l be d e t e r m i n e d whether v e s t i t o l i s induced by i n s e c t f e e d i n g or i s present i n uninfected f i e l d plants. S u b s e q u e n t r e s e a r c h f o u n d t h a t Costelytra zealandica a n d Heteronychus arator l a r v a e a r e s e n s i t i v e t o seven phytoalexins including pisatin, maackiain and medicarpin Γ161 . R e l a t e d compounds n a r i n g e n i n , apigenin, morin,




202

F i g u r e 1.

Major soybean

phytoalexins.


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coumestrol, formononetin, b i o c h a n i n A and g e n i s t e i n d i d not s i g n i f i c a n t l y affect feeding a c t i v i t y . Phaseollin, v e s t i t o l , p h a s e o l l i n i s o f l a v a n , and 2 -methoxyphaseollinisoflavan were t h e most a c t i v e , showing significant f e e d i n g r e d u c t i o n a t l ( ^ g / m l o r l e s s . Heteronychus arator s e e m s m o r e s e n s i t i v e t h a n Costelytra zealandica t o these c o m p o u n d s , e x c e p t f o r p i s a t i n . P h y t o a l e x i n s may t h e r e f o r e s e r v e t w o d i f f e r e n t a n d p e r h a p s indépendant r o l e s i n t h e plant. Research by Hart e t a l . [11] on t h e e f f e c t of s o y b e a n p h y t o a l e x i n s on M e x i c a n bean b e e t l e Epilachna v a r i v e s t i s a n d t h e s o y b e a n l o o p e r Pseudoplusia includens showed t h a t t i s s u e s i n w h i c h t h e s e isomers had been elicited [by e x p o s u r e to ultraviolet irradiation] s t r o n g l y d e t e r r e d t h e Mexican bean b e e t l e but not t h e soybean looper. At the induced, physiological c o n c e n t r a t i o n o f 1% o f d r y w e i g h t , g l y c e o l l i n h a d some e f f e c t on s u r v i v a l o f 1 - d a y - o l d s o y b e a n l o o p e r l a r v a e b u t not on s u b s e q u e n t s u r v i v a l and d e v e l o p m e n t . S i n c e this i n s e c t r e a d i l y f e e d s o n s o y b e a n s , a s i t s name i m p l i e s , t h i s a b i l i t y t o t o l e r a t e g l y c e o l l i n i s not s u r p r i s i n g . In a d d i t i o n , t e s t i n g s i n g l e compounds i n an a r t i f i c i a l diet ignores the possible synergistic effects of the multitude o f p h e n o l i c compounds i n g e s t e d f r o m t h e p l a n t during n o r m a l h e r b i v o r y . A d d i t i o n a l l y a compound d i s t r i b u t e d i n a diet rather uniformly may not approximate the l o c a l i z e d , and sometimes h i g h e r c o n c e n t r a t i o n s i n p l a n t s . On t h e o t h e r h a n d t h e o l i g o p h a g o u s Mexican bean beetle clearly was deterred from feeding on t h e p h y t o a l e x i n - r i c h t i s s u e . Since t h i s insect i s not e a s i l y reared on a r t i f i c i a l diets, the direct toxicity of glyceollin t o t h e Mexican bean b e e t l e could n o t be determined i n these experiments. This i s a common experimental p r o b l e m when d e t e r m i n i n g the effect of a g i v e n compound i n v i v o . Some o f t h e s e problems have been addressed by Fischer, D.C.; Kogan, M.; Paxton, J.D., (Environ . E n t o m o l . s u b m i t t e d ) . They p u r i f i e d g l y c e o l l i n , a p p l i e d i t to common b e a n (Phaseolus vulgaris) leaves at rates of 0.22, 1.1, 2.2, 11.0 o r 22.0 μg/mg d r y w e i g h t o f l e a f tissue. These t i s s u e s were then subjected to feeding preference tests i n p e t r i plates with the southern corn rootworm {Diabrotica undecimpunctata howardi), the M e x i c a n b e a n b e e t l e (Epilachna v a r i v e s t i s ) and t h e bean leaf beetle (Cerotoma trifurcata) . Glyceollin treated l e a v e s were consumed l e s s by t h e s o u t h e r n corn rootworm and t h e M e x i c a n bean b e e t l e , even a t l e v e l s below t h a t f o u n d i n e l i c i t e d p l a n t s . On t h e o t h e r h a n d t h e b e a n l e a f b e e t l e f e d f r e e l y , e v e n a t v e r y h i g h [22μg/mg] d o s e s o f g l y c e o l l i n . T h i s s u g g e s t s t h a t p h y t o a l e x i n s may r e p r e s e n t a convergence o f defenses a g a i n s t both microorganisms and insect herbivores. 1


203


204



Elicitation

of Phytoalexins

by

Stresses

Many e n v i r o n m e n t a l f a c t o r s s u c h a s h e a t , d r o u g h t , a n d f r o s t may a f f e c t h e r b i v o r e / p l a n t i n t e r a c t i o n s b y increasing or decreasing the level of resistance ofthe plant t o the herbivore [ϋ] . This suggests that t h e plant i s a c t i v e l y responding t o t h e f e e d i n g by t h e h e r b i v o r e a n d t h a t p h y t o a l e x i n s m i g h t t h e r e f o r e b e i n v o l v e d [20.] · This also suggests that s e l e c t i v e e l i c i t a t i o n o f p h y t o a l e x i n s i n p l a n t s might be a d e s i r a b l e s t r a t e g y f o r p r o t e c t i n g p l a n t s a g a i n s t i n s e c t s [21]. A number o f d i f f e r e n t s t r e s s e s c a n e l i c i t i n d u c i b l e compounds i m p o r t a n t i n i n s e c t i n t e r a c t i o n s w i t h p l a n t s . Some o f t h e s e c o m p o u n d s a p p e a r t o a t t r a c t i n s e c t s t o a p l a n t ' i n d i s t r e s s ' , such as t h e southern pine b e e t l e , Dendroctonus f r o n t a l i s , t o Pinus s p p . O t h e r compounds a p p e a r t o p r e v e n t a t t a c k [22]. O z o n e d e c r e a s e s s o y b e a n r e s i s t a n c e t o i n s e c t herbivory and o v e r r i d e s induced r e s i s t a n c e [ L i n , H.C.; K o g a n , M.; E n d r e s s , A.G., E n v i r o n . E n t o . 1990, i n p r e s s . ] . T h i s m i g h t be due t o a d i v e r s i o n o f p h e n o l i c s i n t o c o u m e s t r o l i n s t e a d o f more t o x i c compounds s u c h a s g l y c e o l l i n . Pathogens E l i c i t

Phytoalexins

The m o s t s t u d i e d a s p e c t o f p h y t o a l e x i n e l i c i t a t i o n i s t h a t generated by fungal pathogens o f p l a n t s . Karban e t al.[22] f o u n d i n d u c e d r e s i s t a n c e a n d i n t e r s p e c i f i c c o m p e t i t i o n between s p i d e r mites and a v a s c u l a r w i l t f u n g u s . M c l n t y r e e t a l . [2A] d e m o n s t r a t e d t h a t 7 d a y s a f t e r t o b a c c o p l a n t s were i n f e c t e d w i t h t o b a c c o m o s a i c virus, reproduction o f t h e green peach aphid, Myzus persicae, was s i g n i f i c a n t l y r e d u c e d o n t h e s e i n f e c t e d p l a n t s . Inoculation o f plants with tobacco mosaic v i r u s i n d u c e d r e s i s t a n c e t o s e v e r a l pathogens, however t h e m e c h a n i s m f o r i n d u c e d r e s i s t a n c e was n o t c h a r a c t e r i z e d . This suggests that a d i f f e r e n t type o f p r o t e c t i o n o f p l a n t s a g a i n s t i n s e c t a t t a c k i s p o s s i b l e . Few c a s e s e x i s t where such p r o t e c t i v e i n t e r a c t i o n s between pathogens a n d i n s e c t s on p l a n t s have been s t u d i e d . I b e l i e v e s u c h i n t e r a c t i o n s a r e common a n d d e s e r v e m o r e a t t e n t i o n t h a n received t o date. Insect

Feeding E l i c i t s

Plant

Responses

D e c r e a s e d f e e d i n g on soybean c a n be i n d u c e d b y p r e v i o u s i n s e c t h e r b i v o r y as w e l l as by mechanical i n j u r y .L i n Γ251 found mechanical i n j u r y and p r i o r herbivory induced r e s i s t a n c e i n s o y b e a n c v W i l l i a m s 82 t o t h e s o y b e a n



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Phytoalexins and Control of Insert

205

l o o p e r a n d t h e M e x i c a n b e a n b e e t l e . The l e v e l o f induced r e s i s t a n c e d e p e n d e d on t h e number o f i n j u r e d h o s t c e l l s i n c o n t a c t w i t h h e a l t h y c e l l s , and n o t on t h e amount o f l e a f a r e a l o s t . The r e s i s t a n c e i n d u c e d b y t h e s o y b e a n looper r e s u l t e d from a combination of mechanical i n j u r y a n d c o m p o u n d s i n t h e l a r v a l r e g u r g i t a n t . No c o m m u n i c a t i o n o f t h e i n d u c t i o n s i g n a l s between p l a n t s , and no s u b s e q u e n t p r o t e c t i o n , was f o u n d . I n d u c e d r e s i s t a n c e h a d a s i g n i f i c a n t r e t a r d a n t e f f e c t on d e v e l o p m e n t a n d g r o w t h o f b o t h i n s e c t s , b u t i t h a d no s i g n i f i c a n t e f f e c t o n t o t a l f o o d consumed by e i t h e r i n s e c t . L i n [25.] s e p a r a t e d , b y h i g h p r e s s u r e liquid chromatography, from soybean l e a f e x t r a c t s , twelve peaks r e p r e s e n t i n g an unknown number o f compounds. F e e d i n g by the Mexican bean b e e t l e i n c r e a s e d the areas of t h r e e p e a k s and f e e d i n g by t h e soybean l o o p e r i n c r e a s e d t h e a r e a s o f two p e a k s . These compounds were s i g n i f i c a n t l y c o r r e l a t e d w i t h a n t i f e e d i n g a c t i v i t y of the l e a f samples. K a r b a n [2£] found that cotton r e s i s t a n c e to beet a r m y w o r m s , Spodoptera exigua, c o u l d be i n d u c e d by p r i o r e x p o s u r e t o s p i d e r m i t e s , Tetranychus turkestani. In t h e s e c a s e s t h e compounds r e s p o n s i b l e f o r r e s i s t a n c e were not identified.

Use

of Phytoalexins

and

Their

Elicitors

B a s e d on t h e p r e v i o u s e x a m p l e s , t h e e l i c i t a t i o n o f p h y t o a l e x i n s and o t h e r i n d u c i b l e compounds i n p l a n t s by v a r i o u s e l i c i t o r s m i g h t be a s u c c e s s f u l t a c t i c f o r c o n t r o l l i n g i n s e c t p e s t s on i m p o r t a n t c r o p s . T h i s e l i c i t a t i o n w o u l d n e e d t o o c c u r o n l y when t h e i n s e c t f e e d s , t o p r e v e n t u n n e c e s s a r y damage t o t h e p l a n t b y a c c u m u l a t i o n o f compounds t o x i c t o p l a n t c e l l s as w e l l . B a s e d on p r e s e n t l y known c a r b o h y d r a t e e l i c i t o r s , i t seems p l a u s i b l e t h a t p l a n t s u r f a c e s c o u l d be t r e a t e d i n s u c h a way t h a t t h e e l i c i t o r i s c a r r i e d i n t o t h e p l a n t u p o n i n s e c t f e e d i n g [21]. These carbohydrate elicitors should b e s t a b l e a n d s h o u l d p o s e no e n v i r o n m e n t a l threat since t h e y a r e most l i k e l y n o n - t o x i c t h e m s e l v e s . I s u g g e s t t h a t p h y t o a l e x i n s p l a y an i m p o r t a n t role i n i n s e c t r e s i s t a n c e by p l a n t s . T h i s r o l e o f p h y t o a l e x i n s a n d p h y t o a l e x i n e l i c i t a t i o n now s h o u l d b e s t u d i e d f u r t h e r and t e s t e d under f i e l d c o n d i t i o n s .

Acknowledgments C e r t a i n aspects of the were s u p p o r t e d i n p a r t

research presented i n t h i s chapter by t h e I l l i n o i s A g r i c u l t u r a l


206


Experiment Station, U.S.D.A. Competitive

The American Soybean Grants Program.

Association,

and

Literature Cited 1. 2.


3. 4. 5. 6.

7.

8. 9.

10. 11. 12. 13. 14. 15. 16. 17. 18.

Paxton, J.D. Phytopath. Zeit. 1981, 101, 106-109. Norris, D.M., In Chemistry of Plant Protection; Haug, G.; Hoffmann, H. Eds.; Springer-Verlag: Berlin, 1986; pp 99-146. Daglish, C. Biochem. J. 1950, 47, 452-462. Gilbert, B.L.; Norris, D.M. Insect Physiol. 1968, 14, 1063-1068. Paxton, J.D.; Wilson, E.E. Phytopathology 1965, 55, 21-26. Stipanovic, R.D.; Bell, Α.A.; Lukefahr, M.J. In Host Plant Resistance to Pests; Hedin, P.Α., Ed.; ACS Symposium Series No.62; American Chemical Society: Washington, DC, 1977; Chapter 14. Mabry, T.J.; Gill, J.E.; Burnett, W.C.; Jones, S.B. In Host Plant Resistance to Pests; Hedin, P.Α., Ed.; ACS Symposium Series No.62; American Chemical Society: Washington, DC, 1977; Chapter 12. Ryan, C . A . Trends Biochem. Sci. 1978, 3, 148-150. Nelson, C.E.; Walker-Simmons, M.; Makus, D.; Zuroske, G.; Graham, J.; Ryan, C.A. In Plant Resistance to Insects; Hedin, P.Α., Ed.; ACS Symposium Series No.208; American Chemical Society: Washington, DC, 1983; Chapter 6. Ryan, C.A.; Bishop, P.D.; Graham, J.S.; Droadway, R.M.; Duffey, S.S. J. Chem. Ecol. 1986, 3, 10251036. Carroll, C.R.; Hoffman, C.A. Science 1980, 209, 414416. Hedin, P.Α., Ed. Host Plant Resistance to Pests: ACS Symposium Series No.62; American Chemical Society: Washington, DC, 1977; pp 286. Lyne, R.L.; Mulheirn, L.J.; Leworthy, D.P. JCS Chem.Comm. 1976, 1976, 497-498. Ingham, J.L.; Keen, N.T.; Mulheirn, L.J.; Lyne, R.L. Phytochem. 1981, 20, 795-8. Russell, G.B.; Sutherland, O.W.R.; Hutchins, R.F.N.; Christmas, P.E. J.Chem.Ecol. 1978, 4, 571-579. Sutherland, O.W.R.; Russell, G.B.; Biggs, D.R.; Lane, G.A. Biochem. Syst. Ecol. 1980, 8, 73-75. Hart, S.V.; Kogan, M.; Paxton, J. J. Chem. Ecol. 1983, 9, 657-72. Fukami, H.; Nakajima, M. In Naturally Occurring Insecticides; Jacobsen, M.; Crosby, D.G., Eds.; Marcel Dekker, New York, 1971; pp 71-97.


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RECEIVED May

16,

1990


Phytoalexins and Their Potential Role in Control of Insect Pests

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