Biologically Active Natural Products - American Chemical Society

Chapter 16

Terpenoids as Models for New Agrochemicals Stella D. Elakovich

Downloaded by UNIV OF MICHIGAN ANN ARBOR on February 18, 2015 | http://pubs.acs.org Publication Date: November 28, 1988 | doi: 10.1021/bk-1988-0380.ch016

Department of Chemistry, University of Southern Mississippi, Hattiesburg, MS 39406-5043

This chapter examines the evidence that some terpenoids serve as plant growth regulators (allelochemicals) as well as anti-herbivore agents. The plant origin and bioassay method of terpenoid allelopathic agents is explored. The role these same compounds play in plant-insect communication due to volatiles, and their involvement as insect pheromones is discussed. The agrochemical possibilities are far-reaching. Terpenes and terpenoids are ubiquitous in the higher plant kingdom. Although the role of these compounds is s t i l l being debated, considerable evidence is accumulating that they have functions both as allelopathic agents and as anti-herbivore agents. As such, they possess the potential of being incorporated via genetic engineering methods into selected crop plants in order to both provide a defensive allelochemical edge over other plants, and also to minimize crop damage by insects. Many secondary compounds implicated in allelopathic interactions have also been reported to be involved in other protective or defensive roles for the plant (1). It is likely that many secondary compounds have more than one role in nature. This chapter will explore the role of terpenoids first as allelopathic agents--potential models for new herbicides-and then as important agents in plant-insect interactions. Allelopathic Agents In his classical paper titled "The Influence of One Plant on Another--Allelopathy", Hans Molisch in 1937 coined the term allelopathy to refer to biochemical interactions among all types of plants including microorganisms (2.). Rice, in the second edition of his comprehensive monograph Allelopathy supports this early definition which includes both inhibitory and stimulatory interactions (3). Not surprisingly, the most commonly identified allelopathic compounds produced by higher plants are simple phenols 0097-6156/88/0380-0250$06.00/0 © 1988 American Chemical Society

In Biologically Active Natural Products; Cutler, H.; ACS Symposium Series; American Chemical Society: Washington, DC, 1988.

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and c i n n a m i c a c i d d e r i v a t i v e s ( 3 ) . A s l o n g ago a s 1 9 0 8 , Schreiner and Reed (4) r e p o r t e d t h a t v a n i l l i n , v a n i l l i c a c i d , and h y d r o q u i n o n e a r e commonly p r o d u c e d p l a n t c o n s t i t u e n t s i n h i b i t o r y t o s e e d l i n g growth. T h i s f o c u s i n g on p l a n t p h e n o l i c c o n s t i t u e n t s as a l l e l o c h e m i c a l s l i k e l y o c c u r r e d f o r two m a i n r e a s o n s : t h e e a s e o f i s o l a t i o n and i d e n t i f i c a t i o n o f p h e n o l i c compounds, and t h e i r h i g h water s o l u b i l i t y . R e c e n t l y F i s c h e r and Q u i j a n o (5) h a v e p r o p o s e d t h a t c o m p o u n d s o f l o w w a t e r s o l u b i l i t y may a c t a s a l l e l o c h e m i c a l s v i a m i c e l l e f o r m a t i o n , a n d t h e y s u g g e s t a réévaluation o f w a t e r i n s o l u b l e p l a n t c o n s t i t u e n t s as p o t e n t i a l a l l e l o p a t h i c a g e n t s . B o t h mono- a n d s e s q u i t e r p e n o i d s f r e q u e n t l y o c c u r i n t h e s t e a m v o l a t i l e e s s e n t i a l o i l s of higher plants. M o n o t e r p e n o i d s a r e 10c a r b o n c o m p o u n d s b i o g e n e t i c a l l y d e r i v e d f r o m two i s o p r e n e u n i t s (6.) . S e v e r a l h u n d r e d a r e known. T h e i r f u n c t i o n as g e r m i n a t i o n and p l a n t g r o w t h r e g u l a t o r s was r e v i e w e d b y E v e n a r i ( 7 ) i n 1949 a n d r e c e n t l y by F i s c h e r ( 8 ) . Sesquiterpenoids, 1 5 - c a r b o n compounds d e r i v e d f r o m t h r e e i s o p r e n e u n i t s ( 6 ) , d i s p l a y w i d e s t r u c t u r a l v a r i e t y and a d r a m a t i c i n c r e a s e i n t h e number o f known c o m p o u n d s - - s e v e r a l t h o u s a n d a r e known. The h i g h d e g r e e o f r e s e a r c h a c t i v i t y i n t h i s a r e a i s e x e m p l i f i e d by t h r e e r e v i e w s p u b l i s h e d i n the p a s t f i v e y e a r s . S t e v e n s (9) r e v i e w e d the b i o l o g i c a l l y a c t i v e s e s q u i t e r p e n e lactones, F i s c h e r (8) r e v i e w e d the g e r m i n a t i o n and p l a n t g r o w t h r e g u l a t o r y f u n c t i o n s o f b o t h mono- a n d s e s q u i t e r p e n o i d s , a n d E l a k o v i c h (10) reviewed sesquiterpenes a c t i n g as p h y t o a l e x i n s and p l a n t g r o w t h regulators. Since these are a l l q u i t e recent reviews, t h i s paper w i l l o n l y g i v e a c u r s o r y r e v i e w o f w o r k m e n t i o n e d i n them. Reports t h r o u g h l a t e 1987 o f mono- a n d s e s q u i t e r p e n o i d s a l l e g e d t o b e a l l e l o p a t h i c agents not i n c l u d e d i n these three recent reviews w i l l b e r e v i e w e d h e r e i n more d e t a i l . Monoterpenes. M o n o t e r p e n e s w e r e i m p l i c a t e d i n a l l e l o p a t h y o v e r 60 y e a r s ago w h e n S i g m u n d ( 1 1 ) s c r e e n e d e s s e n t i a l o i l s a n d p u r e monoterpenes and o b s e r v e d i n h i b i t i o n o f s e e d g e r m i n a t i o n and p l a n t g r o w t h i n wheat, r a p e and v e t c h . I n h i s 1986 r e v i e w , F i s c h e r g i v e s t h e s t r u c t u r e s o f 14 m o n o t e r p e n e s t h a t h a v e b e e n i m p l i c a t e d i n allelopathy (8). T e n o f t h e m , a- a n d β-pinene, c a m p h e n e , c a m p h o r , 1 , 8 - c i n e o l e , p u l e g o n e , b o r n e o l , l i m o n e n e , α-phellandrene a n d pc y m e n e a r e common c o n s t i t u e n t s o f p l a n t e s s e n t i a l o i l s a n d h a v e f r e q u e n t l y b e e n i m p l i c a t e d i n a l l e l o p a t h y . M u l l e r and M u l l e r (12) f o u n d c a m p h e n e , c a m p h o r , c i n e o l e , d i p e n t e n e , a- a n d β-pinene among t h e v o l a t i l e i n h i b i t o r s p r o d u c e d b y Salvia s p e c i e s . Of these, camphor and c i n e o l e were t h e most t o x i c t o r o o t g r o w t h o f t e s t seedlings (13). A s p l u n d (14) i n v e s t i g a t e d t h e i n h i b i t o r y n a t u r e o f c a m p h o r , p u l e g o n e , b o r n e o l , c i n e o l e , l i m o n e n e , α-phellandrene, pc y m e n e , a- a n d β-pinene t o w a r d r a d i s h s e e d g e r m i n a t i o n a n d f o u n d t h a t a l t h o u g h compounds w i t h a k e t o n e g r o u p , camphor and p u l e g o n e , w e r e more i n h i b i t o r y t h a n t h e o t h e r s , a l l were i n h i b i t o r y . Rather s u r p r i s i n g l y , a l l s t i m u l a t e d g e r m i n a t i o n a t low concentrations. The " b a r e z o n e s " , a r e a s f r e e o f h e r b a c e o u s v e g e t a t i o n , s u r r o u n d i n g n a t u r a l i z e d s t a n d s o f Eucalyptus camaldulensis are due t o t h e h i g h l y t o x i c c i n e o l e and l e s s t o x i c p i n e n e and a - p h e l l a n d r a n e f o u n d among t h e t e r p e n e s p r o d u c e d b y Ε. camaldulensis (15.) . This o r d e r o f t o x i c i t y i s r e i n f o r c e d by d a t a f r o m Weaver and K i s h (16) who m e a s u r e d t h e e f f e c t s o f e i g h t t e r p e n e s o n c u c u m b e r a n d f o u n d e v e n the s m a l l e s t amounts t e s t e d o f c i n e o l e , d i p e n t e n e , c i t r o n e l l o l ,



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menthol and t e r p i n e o l e s s e n t i a l l y e l i m i n a t e d both root and hypocotyl growth. H a l l i g a n (17) examined t h e r e l a t i v e a c t i v i t i e s o f t e r p e n o i d s f r o m Artemisia californica, w h i c h l i k e Eucalyptus, i s c h a r a c t e r i z e d b y bare zones under and a d j a c e n t t o t h e t h i c k e t s i t forms. O f t h e f i v e t e r p e n o i d s f o u n d i n m a j o r a m o u n t s , camphor was most t o x i c , f o l l o w e d b y c i n e o l e . S o u r o r a n g e , Citrus aurantium L., a l s o i n h i b i t s growth o f h e r b a c e o u s v e g e t a t i o n v i a a n a l l e l o p a t h i c m e c h a n i s m ( 1 8 - 1 9 ) . Among the v o l a t i l e i n h i b i t o r s i d e n t i f i e d a r e four terpenoids: a - a n d βpinene, (i)-limonene, and c i t r o n e l l a l . A l l o f t h e s e compounds r e d u c e d t h e h y p o c o t y l g r o w t h o f Amaranthus retroflexus; a l l except the lower c o n c e n t r a t i o n t e s t e d o f (+)-limonene a l s o reduced r a d i c a l l e n g t h o f A. retroflexus, and a l l except (-)-limonene i n h i b i t e d t h e g e r m i n a t i o n o f A. retroflexus seeds. Inhibitory effects increased with increased inhibitor concentrations. α-Pinene w a s t h e m o s t a c t i v e o f these i n h i b i t o r s ; t h i s i s the f i r s t report i m p l i c a t i n g citronellal i n allelopathy. The h e x a n e e x t r a c t o f s e e d s f r o m Eryngium paniculatum was f o u n d t o i n h i b i t g e r m i n a t i o n o f v e l v e t l e a f (Abutilon theophrasti M e d i c ) , a s e r i o u s weed i n c o r n a n d s o y b e a n f i e l d s ( 2 0 ) . F r a c t i o n a t i o n s m o n i t o r e d b y b i o a s s a y gave t h e t e r p e n e a l d e h y d e - e s t e r (-)-2,2,2-trimethyl-3-formyl-2,5-cyclohexadienyl angelate (1) as t h e o n l y a c t i v e component. S t r u c t u r e - a c t i v i t y studies o f (1) and nine analogs suggest that a c t i v i t y i sdiminished by removing the formyl group from t h e r i n g , t h e c y c l i c double bonds a r e r e q u i r e d , and t h e o r i e n t a t i o n o f t h e a c y l double bond i sn o ti m p o r t a n t .

H e i s e y a n d D e l w i c h e (21) o b s e r v e d a h i g h l y t o x i c monoterpene a l c o h o l a s a m a j o r i n h i b i t o r p r e s e n t i n Trichostema lanceolatum Benth. ( v i n e g a r weed). T h i s a l c o h o l , t e r p i n e n - 4 - o l , was l e s s i n h i b i t o r y t h a n c a m p h o r , b u t a l m o s t t w i c e a s i n h i b i t o r y a s 1,8c i n e o l e as measured b y g e r m i n a t i o n and r a d i c a l growth i n h i b i t i o n o f Hordeum vulgare ( s e l e c t e d because o f i t s g e n e t i c homogeneity) and Bromus mollis ( s e l e c t e d b e c a u s e i t i s common t o t h e C a l i f o r n i a grassland). I n o u r i n v e s t i g a t i o n s o f a l l e l o p a t h i c p l a n t s , we h a v e e x a m i n e d t h e c r e e p i n g p e r e n n i a l h e r b Lippia nodiflora, w h i c h i s known f o r i t s rampant growth ( 2 2 ) , and h a d e a r l i e r been r e p o r t e d t o be a g e r m i n a t i o n i n h i b i t o r ( 7 ) . We f o u n d t h e e s s e n t i a l o i l i n h i b i t o r y t o l e t t u c e s e e d l i n g s , p r o b a b l y due i n p a r t t o t h e p r e s e n c e o f t h e t e r p e n e s / ? - p i n e n e a n d p - c y m e n e a n d t h e s e s q u i t e r p e n e α-caryophyllene i d e n t i f i e d i n t h e complex e s s e n t i a l o i l . I n v e s t i g a t i o n (23) o f t h e e s s e n t i a l o i l o f a s e c o n d Lippia s p e c i e s , Lippia adoensis, revealed a simple mixture completely dominated by t h e terpene a l c o h o l , l i n a l o o l (81% o f the t o t a l e s s e n t i a l o i l ) . The a l l e l o p a t h i c m o n o t e r p e n e s 1 , 8 - c i n e o l e a n d a - a n d β-pinene w e r e a l s o i d e n t i f i e d . Lettuce s e e d l i n g b i o a s s a y o f both the e s s e n t i a l o i land o f pure l i n a l o o l showed s i m i l a r a c t i v i t y . B o t h appear t o enhance r a d i c a l growth a t l o w c o n c e n t r a t i o n s , a l t h o u g h t h e enhancement i s n o t


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statistically significant. A t 400 ppm l i n a l o o l c a u s e s a 4 2 % r e d u c t i o n a n d L. adoensis l e a f e x t r a c t a 45% r e d u c t i o n i n l e t t u c e radical length. Mechanisms o f A l l e l o p a t h i c I n h i b i t i o n by Mono-Terpenoids. There i s a d e a r t h o f i n f o r m a t i o n a v a i l a b l e on t h e s p e c i f i c e f f e c t s t h a t a l l e l o c h e m i c a l s produce. M u l l e r and M u l l e r (12) f o u n d camphor and c i n e o l e t o be t h e m o s t t o x i c among t h e v o l a t i l e i n h i b i t o r s p r o d u c e d b y Salvia species. I n d e e d , c i n e o l e was u s e d a s t h e s t r u c t u r a l b a s i s f o r the s y n t h e t i c h e r b i c i d e c i n m e t h y l i n (24). A s p l u n d (14) f o u n d t e r p e n o i d s c o n t a i n i n g a k e t o n e g r o u p , camphor and p u l e g o n e t o be t h e m o s t i n h i b i t o r y among n i n e t e r p e r o i d s e x a m i n e d . B o t h H e i s e y and D e l w i c h e (21) and E l a k o v i c h and O g u n t i m e i n (23) f o u n d m o n o t e r p e n e a l c o h o l s t o be t h e m a j o r v o l a t i l e i n h i b i t o r s p r o d u c e d by Trichostema lanceolatum a n d Lippia adoensis, respectively. C e r t a i n l y these r e s u l t s s u g g e s t t h a t o x y g e n a t e d t e r p e n e s a r e more h i g h l y i n h i b i t o r y than terpene hydrocarbons. E i n h e l l i g (25) s u g g e s t s t h a t i t i s a r a r e e x c e p t i o n when a s i n g l e s u b s t a n c e i s r e s p o n s i b l e f o r allelopathy. He h a s s h o w n (26.) t h a t b o t h a d d i t i v e a n d s y n e r g i s t i c i n h i b i t i o n may o c c u r , b u t t h e m e c h a n i s m s o f t h i s i n h i b i t i o n h a v e n o t been determined. M u l l e r (27.) h a s r e v i e w e d t h e p o s s i b l e m e c h a n i s m s i n v o l v e d i n a l l e l o c h e m i c a l i n h i b i t i o n of herbs. When Cucumis sativus (cucumber) s e e d l i n g s a r e e x p o s e d t o Salvia leucophylla vapors, elongation of t h e h y p o c o t y l s i s s e v e r e l y c u r t a i l e d and g r o w t h i s r e d u c e d t o 25% o f t h e c o n t r o l , i n d i c a t i n g b o t h stem and r o o t c e l l s a r e a f f e c t e d by the v o l a t i l e terpenoids. Those c e l l s w h i c h f i r s t d e v e l o p i n a g e r m i n a t i n g s e e d a r e more s u s c e p t i b l e t o t h e s e v o l a t i l e terpenoids t h a n a r e the c e l l s o f an o l d e r p l a n t and c e l l e l o n g a t i o n , cell d i v i s i o n , and t i s s u e m a t u r a t i o n a r e a l l i n f l u e n c e d ( 2 8 ) . Somewhat i n c o n t r a s t i s t h e w o r k o f W e a v e r a n d K l a r i c h ( 2 9 ) who f o u n d t h a t volatile s u b s t a n c e s , a s s u m e d t o be m o n o t e r p e n e s , f r o m Artemisia tridentata N u t t . s u p p r e s s e d s e e d l i n g g r o w t h and the r e s p i r a t i o n r a t e of j u v e n i l e p l a n t m a t e r i a l , but e l e v a t e d the r e s p i r a t i o n r a t e of mature leaves. T h e y s h o w e d i n l a b o r a t o r y t e s t s t h a t some t e r p e n e s r a i s e d and o t h e r s l o w e r e d the r e s p i r a t i o n i n wheat (Triticum aestivum L.). V o l a t i l e s o f S. leucophylla essentially halted m i t o s i s o f Allium cepa r o o t t i p s w i t h i n 72 h r s o f e x p o s u r e ( 3 0 ) . When l o w e r c o n c e n t r a t i o n s o f t h e t e r p e n o i d s w e r e u s e d f o r treatments, t h e e f f e c t on chromosomes c o u l d be s e e n t o be s i m i l a r t o t h a t c a u s e d by c o l c h i c i n e t r e a t m e n t . The l o n g e r t h e A. cepa b u l b s a r e e x p o s e d t o t e r p e n o i d s , o r t h e more c o n c e n t r a t e d t h e terpenoids t o w h i c h the c e l l s are exposed, the g r e a t e r are the chromosomal abnormalities. Increased c u t i n deposits i n root epidermal c e l l s , and i n c r e a s e d l i p i d a c c u m u l a t i o n i n r o o t c o r t i c a l c e l l s a l s o o c c u r w i t h i n c r e a s e d e x p o s u r e t o Salvia t e r p e n o i d s (31.) . T h e s e i n c r e a s e d c u t i n s a n d l i p i d s may e n h a n c e t h e t e r p e n o i d i n h i b i t o r y e f f e c t s b y making access of the a l l e l o c h e m i c a l s i n t o the c e l l s e a s i e r . E i n h e l l i g ( 2 5 ) s u g g e s t s t h a t l o s s o f membrane i n t e g r e t y b y a b s o r p t i o n o f l i p i d s o l u b l e t e r p e n e s i n t o t h e membranes i s a l i k e l y starting point for their destructive action. M u l l e r (27) s u g g e s t s t h a t e v e n i f s u s c e p t i b l e p l a n t s do s u r v i v e , t h e y w o u l d b e w e a k e r a n d t h u s more l i k e l y t o succumb t o e n v i r o n m e n t a l s t r e s s e s s u c h as drought. I t i s thus p o s s i b l e to m i t i g a t e or i n t e n s i f y a l l e l o p a t h i c e f f e c t s by e n v i r o n m e n t a l f a c t o r s .



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Sesquiterpene Hydrocarbons and T h e i r D e r i v a t i v e s . Recent reviews (8,10) o f s e s q u i t e r p e n e hydrocarbons and t h e i r d e r i v a t i v e s t h a t have b e e n i m p l i c a t e d i n a l l e l o p a t h y g i v e s t r u c t u r e s f o r 20 c o m p o u n d s . I n c l u d e d a r e b e r g a m o t e n e , b i s a b o l e n e , a - b u l n e s e n e , δ-cadinene, calamenene, β - c a r y o p h y l l e n e , α-copaene, a - g u a y e n e , β-patchoulin, and / 3 - s e l i n e n e , a l l h y d r o c a r b o n s f r e q u e n t l y f o u n d i n p l a n t e s s e n t i a l oils. Three sesquiterpene aldehydes, (-)-isobicyclogermacrenal, ( - ) - l e p i d o z e n a l , and ( + ) - v i t r e n a l a r e i n c l u d e d along w i t h the ketone zerumbone. The s e s q u i t e r p e n e a l c o h o l , f a r n e s o l , i t s a c e t a t e , t h e r e l a t e d c o m p o u n d m e t h y l f a r n e s a t e , a n d t h e c a d i n e n e d e r i v a t i v e , epikhusinol acetate are a l l phytotoxic. Two i n h i b i t o r y c o m p o u n d s h a v i n g m u l t i - f u n c t i o n a l i t y i n c l u d e t h e ent-2,3-secoa l l o a r o m a d e n d r a n e p l a g i o c h i l i n A a n d phomenone. Structure-activity s t u d i e s o f the l a t t e r suggest the epoxide f u n c t i o n i s necessary f o r growth i n h i b i t i o n , and a c e t y l a t i o n i s c l o s e l y connected w i t h t h e t o x i c p r o p e r t i e s (32.) . P a u l et al. ( 3 3 ) r e c e n t l y e l u c i d a t e d t h e s t r u c t u r e o f f i v e new b i o a c t i v e s e s q u i t e r p e n o i d s f r o m t h e g r e e n a l g a e , Caulerpa ashmeadii. F o u r o f t h e s e compounds, ( 2 ) , ( 3 ) , ( 4 ) , and ( 5 ) ,

showed a n t i m i c r o b i a l a c t i v i t y t o w a r d a t l e a s t one m a r i n e b a c t e r i u m and a l l were a l s o t o x i c t o w a r d t h e d a m s e l f i s h , Pomacentrus coeruleus. The a l d e h y d e a n d e n o l a c e t a t e f u n c t i o n a l g r o u p s p r e s e n t i n t h e s e compounds c a n p o t e n t i a l l y r e a c t w i t h p r o t e i n s i n a number o f ways t o a l t e r o r i n a c t i v a t e p r o t e i n o r enzyme f u n c t i o n , s u p p o r t i n g the hypothesis that these metabolites a r e used i n chemical defense. Seed g e r m i n a t i o n b i o a s s a y o f t h e e t h y l a c e t a t e e x t r a c t o f d r i e d , g r o u n d Ambrosia peruviana W i l l d . , w i l d t a n s y , showed i n h i b i t o r y a c t i v i t y (34). Five sesquiterpenes, four lactones of the pseudoguaianolide type and a d i o l were c h a r a c t e r i z e d from t h i s extract. T h e d i o l s t r u c t u r e was d e t e r m i n e d b y s p e c t r a l e v i d e n c e t o be (6), (+)-alloaromadendrane-4/3,10a-diol. This i s the f i r s t OH

(6) r e p o r t e d s e s q u i t e r p e n e d i o l f r o m Ambrosia s p e c i e s . I t i s antipodal t o a c o m p o u n d i s o l a t e d f r o m t h e m a r i n e s o f t c o r a l , Sinularia mayi and thus i l l u s t r a t e s t h e f r e q u e n t l y o b s e r v e d a n t i p o d a l r e l a t i o n s h i p between s e s q u i t e r p e n e s d e r i v e d from marine and t e r r e s t r i a l organisms. B i o a s s a y o f i s o l a t e d (6) s h o w e d i t t o c a u s e r e d u c t i o n o f c r e s s r o o t s and shoots a t the three c o n c e n t r a t i o n s t e s t e d , b u t o n l y


16.

ELAKOVICII



t h e h i g h e s t c o n c e n t r a t i o n i n h i b i t e d l e t t u c e s e e d l i n g r o o t s and shoots. A t t h e two l o w e r c o n c e n t r a t i o n s t e s t e d , l e t t u c e r o o t s shoots were s i g n i f i c a n t l y s t i m u l a t e d .

255

and

Sesquiterpene Lactones. Of a l l o f t h e t e r p e n o i d compounds, t h e sesquiterpene l a c t o n e s possess the g r e a t e s t v a r i e t y o f b i o l o g i c a l activities. M o r e t h a n 1000 o f t h e s e c o m p o u n d s h a v e b e e n i s o l a t e d , c h i e f l y from the p l a n t f a m i l y Asteraceae (Compositae), but a l s o from the U m b e l l i f e r e a e and M a g n o l i a c e a e ( 8 ) . I n 1976 R o d r i g u e z , et al. (35) r e v i e w e d the b i o l o g i c a l a c t i v i t i e s and mechanism o f a c t i o n o f t h e s e compounds. I n a 1979 r e v i e w , F i s c h e r e t al. (36.) l i s t 950 s e s q u i t e r p e n e l a c t o n e s w h i c h h a d b e e n c h a r a c t e r i z e d b y 1977. They a l s o d i s c u s s the b i o g e n e t i c r e l a t i o n s h i p s of sesquiterpene l a c t o n e s . The a c t i v i t i e s t h e s e c o m p o u n d s p o s s e s s i n c l u d e a n t i n e o p l a s t i c agents, i n s e c t feeding d e t e r r e n t s , p l a n t growth r e g u l a t o r s , a n t i m i c r o b i a l agents, s c h i s t o s o m i c i d a l agents, v e r t e b r a t e poisons a n d c o n t a c t d e r m a t i t i s i n humans ( 8 , 1 0 ) . Several structure-activity s t u d i e s have l e d to the c o n c l u s i o n t h a t p l a n t growth r e g u l a t i o n r e q u i r e s the p r e s e n c e o f an e x o c y c l i c a,/3-unsaturated lactone moiety (7) w h i c h c a n combine w i t h s u l f h y d r y l g r o u p s i n k e y enzymes t h a t control cell division (8,9,35).

I n h i s 1984 r e v i e w , S t e v e n s ( 9 ) g i v e s s t r u c t u r e s o f 8 s e s q u i t e r p e n e l a c t o n e s which have a l l e l o p a t h i c a c t i v i t y . Fischer ( 8 ) , i n h i s 1986 r e v i e w , g i v e s s t r u c t u r e s o f 38 a d d i t i o n a l a l l e l o p a t h i c sesquiterpene lactones. A r e c e n t r e p o r t by G o l d s b y and B u r k e (34) g i v e s s t r u c t u r e s f o r f o u r s e s q u i t e r p e n e l a c t o n e s o f the pseudoguaianolide type i s o l a t e d from the e t h y l a c e t a t e e x t r a c t of Ambrosia peruviana. Three o f t h e s e , ( 8 ) , ( 9 ) , and ( 1 0 ) , a r e s t r u c t u r e s n o t r e p o r t e d by S t e v e n s (9) o r F i s c h e r ( 8 ) . Of t h e s e , a m b r o s i n (8) and p s i l o s t a c h y i n Β (10) were most a c t i v e i n p r e v e n t i n g g e r m i n a t i o n and r o o t and s h o o t g r o w t h i n l e t t u c e and c r e s s seedlings. D a m s i n (9) e x h i b i t e d b o t h s t i m u l a t o r y and i n h i b i t o r y e f f e c t s on s e e d l i n g g r o w t h , d e p e n d i n g on t h e c o n c e n t r a t i o n . I t was a l s o a c t i v e a g a i n s t t h e f u n g a l o r g a n i s m Cladosporium herbarium.

A g l a n c e a t any c u r r e n t i s s u e o f a p h y t o c h e m i c a l j o u r n a l r e v e a l s a n e v e r i n c r e a s i n g n u m b e r o f new s e s q u i t e r p e n e l a c t o n e s t r u c t u r e s i s o l a t e d from higher p l a n t s . No d o u b t many o f t h e s e , w h e n s u b j e c t e d t o g r o w t h i n h i b i t i o n a s s a y s , w i l l a l s o p r o v e t o be a l l e l o p a t h i c . Diterpenoids. Liverwarts c o n t a i n o i l bodies which are high i n terpenoid content. B e y e r et al. ( 3 7 ) i s o l a t e d s i x new diterpenoids



256


f r o m t h e l i v e r w a r t Anas trophyHum minutum ( S c h r e b . ) S c h u s t . I n a d d i t i o n , t h e k n o w n s e s q u i t e r p e n e h y d r o c a r b o n s , a n a s t r e p t e n e , βb a r b a t e n e , a n d b i c y c l o g e r m a c r e n e were i s o l a t e d a n d i d e n t i f i e d . The s i x new d i t e r p e n o i d s , ( 1 1 ) , ( 1 2 ) , ( 1 3 ) , ( 1 4 ) , ( 1 5 ) , a n d ( 1 6 ) r e p r e s e n t a new d i t e r p e n o i d t y p e w h i c h t h e a u t h o r s t e r m e d sphenolobane. The s p h e n o l o b a n e s k e l e t o n p r o b a b l y a r i s e s b y t h e c y c l i z a t i o n o f g e r a n y l g e r a n y l pyrophosphate ( 3 7 ) . The m a j o r c o m p o u n d , 3α,4a-epoxy-5a-acetoxy-18-hydroxysphenoloba-13E,16E-diene, (11), showed l o w growth i n h i b i t o r y a c t i v i t y a g a i n s t r i c e s e e d l i n g s , Oryza sativa. The i n h i b i t o r y n a t u r e o f c o m p o u n d s ( 1 2 ) - ( 1 6 ) w a s n o t tested.

CP

CP

OR

(11)

OCOCHj

R=COCH

3

(13)

Allelochemicals

(15) (16)

(12) R = Η

R = C0CH, R = H

Involved i n Plant-Insect Interactions

A l l e l o c h e m i c a l s c a nbe used t o minimize c o m p e t i t i o n and i n v a s i o n o f weeds i n c r o p f i e l d s e s p e c i a l l y b y u s e o f c r o p r o t a t i o n schemes. I s o l a t i o n and i d e n t i f i c a t i o n o f s p e c i f i c a l l e l o c h e m i c a l s has lagged b e h i n d t h e i d e n t i f i c a t i o n o f a l l e l o p a t h i c p l a n t s , l a r g e l y due t o t h e t e d i o u s , time-consuming n a t u r e o f i s o l a t i n g l a r g e enough samples o f p u r e compounds f o r a d e t a i l e d s t r u c t u r e s t u d y . Some o f t h e i s o l a t e d a l l e l o c h e m i c a l s h a v e shown p o t e n t i a l f o r o t h e r u s e s , s p e c i f i c a l l y a s n a t u r a l p e s t i c i d e s a n d g r o w t h r e g u l a t o r s (38)· C e r t a i n l y t h e s e c o m p o u n d s h a v e t h e p o t e n t i a l o f s e r v i n g a s m o d e l s f o r u s e f u l new agrochemicals. A s L o d h i et al. s t a t e ( 1 ) , " I t i s c l e a r t h a t t h e i n v o l v e m e n t o f b i o c h e m i c a l s i n a n a g r o e c o s y s t e m i s a phenomenon t h a t cannot be ignored, because these p h y t o t o x i n s p l a y a multipurpose role." Duke, i n a n o t h e r c h a p t e r i n t h i s book, e x p l o r e s t h e p o t e n t i a l o f t e r p e n o i d s d e r i v e d f r o m t h e g e n u s Artemisia as pesticides. P o w e l l and Spencer, i n a separate chapter, e x p l o r e t h e p h y t o c h e m i c a l i n h i b i t o r s o f Arbutilon theophrasti (velvetleaf) g e r m i n a t i o n a s m o d e l s f o r new h e r b i c i d e s . The f i r s t p a r t o f t h i s chapter has explored t h er o l e o f terpenoids as a l l e l o p a t h i c agents; the remainder o f t h e c h a p t e r w i l l examine t h e e v i d e n c e t h a t these same t e r p e n o i d s a r e i m p o r t a n t a g e n t s i n p l a n t - i n s e c t i n t e r a c t i o n s . Because o f space c o n s t r a i n t s , t h e coverage w i l l be r e p r e s e n t a t i v e , not exhaustive. O l f a c t o r y responses toward p l a n t v o l a t i l e s . The g r e a t i m p o r t a n c e o f terpenoids as agents o f p l a n t - i n s e c t communication probably r e s u l t s from t h e i r v o l a t i l i t y combined w i t h t h e i r g r e a t s t r u c t u r a l d i v e r s i t y w h i c h a l l o w s s p e c i f i c i t y ( 3 9 ) . The o l f a c t o r y r e s p o n s e s toward monoterpene hydrocarbons, monoterpene a l c o h o l s , and s e s q u i t e r p e n e h y d r o c a r b o n s i s o l a t e d f r o m p i n e p h o l e m o f Hylobius abietis, a weevil


16.

ELAKOVICH


257


w h i c h i s one o f t h e m o s t d e s t r u c t i v e p e s t s o f N o r d i c f o r e s t p l a n t a t i o n s , w e r e m e a s u r e d b y S e l a n d e r et al. (40). The t o t a l s t e a m d i s t i l l a t e was e i t h e r a t t r a c t i v e o r n e u t r a l t o t h e w e e v i l s . A f r a c t i o n o f m o n o t e r p e n e h y d r o c a r b o n s was s l i g h t l y r e p e l l e n t e v e n t h o u g h two o f t h e t h r e e m a j o r c o m p o n e n t s (α-pinene a n d 3 - c a r e n e ) were c l e a r l y a t t r a c t i v e . The t h i r d m a j o r c o m p o n e n t , l i m o n e n e , was n e u t r a l , which suggests t h a t the minor monoterpene hydrocarbons i n h i b i t the a t t r a c t a n t e f f e c t s o f the major components. Those f r a c t i o n s c o n t a i n i n g oxygenated t e r p e n e s were a t t r a c t i v e t o t h e w e e v i l s a s was a s e s q u i t e r p e n e h y d r o c a r b o n c o n t a i n i n g fraction. The o n l y p u r e c o m p o n e n t t e s t e d , t h e t e r p e n e a l c o h o l 4t e r p i n e o l was a l s o a t t r a c t i v e . I n g e n e r a l , f e m a l e s were more a t t r a c t e d by the t e r p e n e s t h a n were males, but c o n c e n t r a t i o n plays an i m p o r t a n t r o l e . S i m i l a r o l f a c t o r y responses have been observed i n Hylobius pales H e r b s t . w h i c h w e r e a t t r a c t e d t o t h e m o n o t e r p e n o i d s a n e t h o l e , α-phellandrene, d - a - p i n e n e , β-pinene, e u g e n o l , t e r p i n e o l , camphene, a l l o o c i m e n e , and 3 - c a r e n e ( 4 1 ) . The o x y g e n a t e d t e r p e n e s and s e s q u i t e r p e n e h y d r o c a r b o n s c l e a r l y p l a y an i m p o r t a n t r o l e i n olfactory orientation. B l u s t and H o p k i n s (42) e x a m i n e d t h e r o l e o f o l f a c t i o n i n t h e a d a p t i o n o f t h e s p e c i a l i s t g r a s s h o p p e r , Hypochlora alba Dodge w h i c h f e e d s a l m o s t e x c l u s i v e l y o n Artemisia ludoviciana, Louisiana sagewort. G e r e r a l i s t grasshoppers feed v e r y l i t t l e upon t h i s p l a n t which i s r i c h i n monoterpenes. Some 33 t o 50% o f t h e s e m o n o t e r p e n e s a r e one c o m p o n e n t , 1 , 8 - c i n e o l e . The p l a n t e x t r a c t c o n t a i n i n g a m i x t u r e o f m o n o t e r p e n e s e l i c i t e d g r e a t e r o l f a c t o r y r e s p o n s e t h a n any o f the 5 major monoterpene components t e s t e d i n d i v i d u a l l y . Of t h e i n d i v i d u a l m o n o t e r p e n e s t e s t e d , camphene, c i n e o l e , camphor, b o r n e o l a n d g e r a n i o l , b o r n e o l was t h e m o s t s t i m u l a t o r y . The s o y b e a n (Glycine max) g e n o t y p e PI 227687 i s r e s i s t a n t t o i n s e c t s , p a r t i c u l a r l y t o c a b b a g e l o o p e r (Trichoplusia ni). T. ni t h r i v e s on o t h e r s o y b e a n c o m m e r c i a l v a r i e t i e s s u c h as D a v i s , but f e e d s l e s s , grows more s l o w l y , and shows p o o r e r s u r v i v a l on r e s i s t a n t PI 227687 p l a n t s ( 4 3 ) . Steam d i s t i l l a t e s f r o m s u s c e p t i b l e D a v i s c u l t i v a r s a t t r a c t e d T. ni f e m a l e a d u l t s , w h e r e a s s t e a m d i s t i l l a t e s f r o m r e s i s t a n t P I 227687 c u l t i v a r s r e p e l l e d them and were a l s o more t o x i c t o f i r s t - i n s t a r l a r v a e . Since the p r i m a r y s e l e c t i o n o f h o s t p l a n t i s made b y t h e a d u l t Γ. ni m o t h i n conjunction with s e l e c t i o n of o v i p o s i t i o n a l s i t e s , v o l a t i l e plant c h e m i c a l s ( a l l e l o c h e m i c a l s ) a r e a s s u m e d t o be i m p o r t a n t , and r e p e l l e n t compounds a r e t h e d o m i n a n t v o l a t i l e c h e m i c a l m e s s e n g e r s . L i m i t e d c h e m i c a l d i f f e r e n c e s i n soybean p l a n t s can thus a l t e r t h e i r a c c e p t a b i l i t i e s t o Γ. ni ( 4 3 ) . Plant v o l a t i l e s a l s o c o n t r i b u t e to r i c e r e s i s t a n c e t o t h e l e a f h o p p e r Nephotettix virescens (44). When v o l a t i l e s from a r e s i s t a n t r i c e c u l t i v a r were a p p l i e d to a s u s c e p t i b l e c u l t i v a r , l e a f h o p p e r f e e d i n g was disrupted. The m o n o t e r p e n e m y r c e n e ( 1 7 ) , a l t h o u g h n o t y e t i m p l i c a t e d i n a l l e l o p a t h y , i s a common p l a n t c o n s t i t u e n t a n d i s p r e s e n t i n t h e o l e o r e s i n o f p i n e t r e e s (Pinus s p p . ) . B e e t l e s o f t h e g e n u s Ips a t t a c k and c o l o n i z e p i n e t r e e s . They a g g r e g a t e i n r e s p o n s e t o the t e r p e n e a l c o h o l s i p s i d i e n o l (18) and i p s e n o l ( 1 9 ) , and myrcene (17) c a n s e r v e as t h e p r e c u r s o r o f t h e s e pheromones ( 4 5 ) . The stimulus f o r t h e b i o s y n t h e s e s o f ( 1 8 ) a n d ( 1 9 ) i n t h e Ips g e n u s i s a s s o c i a t e d w i t h f e e d i n g , s u g g e s t i n g t h a t a g g r e g r a t i n g p h e r o m o n e s o f Ips beetles are waste products from terpene metabolism. Bark b e e t l e s of the


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g e n u s Dendroctonus m e t a b o l i z e α-pinene, a m o n o t e r p e n e w h i c h i s u b i q u i t o u s i n t h e o l e o r e s i n o f Pinus s p p . , t o t h e p h e r o m o n e s transv e r b e n o l ( 2 0 ) a n d v e r b e n o n e ( 2 1 ) among o t h e r m i n o r p r o d u c t s ( 4 6 ) . The same o r s i m i l a r s y s t e m s o f t e r p e n e m e t a b o l i s m a r e l i k e l y i n d i f f e r e n t s p e c i e s w i t h i n Dendroctonus and i n c l o s e l y r e l a t e d genera.

Insect mixed-function oxidases. M i x e d - f u n c t i o n o x i d a s e s (MFO, also k n o w n a s m i c r o s o m a l c y t o c h r o m e Ρ-450 m o n o o x y g e n a s e ) a r e a g r o u p o f w i d e l y d i s t r i b u t e d enzymes b e s t known f o r t h e i r a b i l i t y t o d e g r a d e d r u g s , p e s t i c i d e s , and o t h e r compounds. Their primary function i s t o c o n v e r t l i p o p h i l i c compounds i n t o more p o l a r , more r e a d i l y excreted hydrophilic metabolites. B r a t t s t e n et al. (47) h a v e shown t h a t MFO's o f t h e s o u t h e r n armyworm, Spodoptera eridania, are i n d u c e d by s e c o n d a r y p l a n t s u b s t a n c e s added t o i t s f o o d , and the i n d u c t i o n i s r a p i d enough t o p r o v i d e t h i s p o l y p h a g o u s i n s e c t w i t h p r o t e c t i o n a g a i n s t these p o t e n t i a l l y o f f e n s i v e d i e t a r y f a c t o r s . E i g h t t e r p e n o i d s w e r e e v a l u a t e d f o r t h i e r MFO a c t i v i t y i n d u c i n g ability. The m o s t p o t e n t i n d u c e r s w e r e t h e m o n o t e r p e n e h y d r o c a r b o n s (+)-α-pinene a n d m y r c e n e . E v e n a b r i e f e x p o s u r e t o a s m a l l amount o f t h e s e c o m p o u n d s a p p e a r s t o s u f f i c e t o t r i g g e r a n i n c r e a s e i n MFO activity. A l t h o u g h i n s e c t MFO enzyme s y s t e m s l i k e l y e v o l v e d f o r endogenous f u n c t i o n s , t h e i r o p e r a t i o n a g a i n s t hazardous secondary p l a n t s u b s t a n c e s , s u c h a s t h e u b i q u i t o u s t e r p e n o i d s , may b e t h e i r major d e t o x i f i c a t i o n f u n c t i o n . I n v e s t i g a t i o n s w i t h Peridroma saucia H u b n e r , t h e v a r i e g a t e d cutworm, suggest t h a t p l a n t s p e c i e s d i f f e r i n the degree t o w h i c h t h e y s t i m u l a t e t h e MFO s y s t e m , a n d t h u s a n i n s e c t ' s a b i l i t y t o d e t o x i f y i n s e c t i c i d e s may d e p e n d o n t h e t e r p e n o i d s ( a n d o t h e r compounds) p r o d u c e d by i t s h o s t p l a n t ( 4 8 ) . Further studies i n w h i c h f a l l a r m y w o r m s , Spodoptera frugiperda, a generalist insect, w e r e f e d d i e t s c o n t a i n i n g 0.2% o f 13 m o n o t e r p e n o i d s , 3 s e s q u i t e r p e n e s , 2 d i t e r p e n e s , 5 t r i t e r p e n e s , and the t e t r a t e r p e n e c a r o t e n e , showed t h e microsomes o f t h e s e i n s e c t s o x i d i z e d m o n o t e r p e n e s more f a v o r a b l y t h a n o t h e r t e r p e n o i d s , i n d i c a t i n g a p r e f e r e n c e f o r the monoterpenes (49). Conclusions From t h i s b r i e f r e v i e w i t i s c l e a r t h a t t e r p e n o i d s p l a y an i n c r e a s i n g l y important part i n p l a n t - p l a n t i n t e r a c t i o n s . As o u r k n o w l e d g e o f a l l e l o p a t h i c c o m p o u n d s a n d t h e i r modes o f a c t i o n i n c r e a s e , we w i l l b e b e t t e r a b l e t o a p p l y t h i s k n o w l e d g e t o s o l u t i o n s to problems i n a g r i c u l t u r e . Many o f t h e same t e r p e n o i d s w h i c h show a l l e l o p a t h i c a c t i v i t y a l s o p o s s e s s a c t i v i t y as i n s e c t pheromones. Research i n t h i s area of i n s e c t - p l a n t i n t e r a c t i o n s may y i e l d i n f o r m a t i o n o f much v a l u e i n t h e d e v e l o p m e n t o f s o p h i s t i c a t e d methods o f i n s e c t c o n t r o l as w e l l as i n t h e b a s i c r e l a t i o n s b e t w e e n i n s e c t s and p l a n t s ( 4 8 ) . Such s t u d i e s w i l l r e q u i r e e x t e n s i v e


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cooperation among chemists, biologists, and agricultural scientists, but will be rewarded by the development of new and better herbicides and plant growth hormones based on structures of allelochemicals, by useful crop rotation schemes, and by the development of genetically engineered cultivars which not only repel traditional insect pests, but also retard growth of unwanted plants. The agrochemical possibilities are far-reaching!


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9. 10.

11.

12. 13. 14. 15. 16. 17.

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12, 1988


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