Plant Resistance to Insects - American Chemical Society

17 Cytotoxic and Insecticidal Chemicals of Desert Plants

Downloaded by UNIV OF CALIFORNIA SAN DIEGO on April 12, 2016 | http://pubs.acs.org Publication Date: January 20, 1983 | doi: 10.1021/bk-1983-0208.ch017

ELOY RODRIGUEZ University of California, Phytochemical Laboratory, Department of Ecology and Biology, Irvine, CA 92717

A d i v e r s e group of n a t u r a l chemicals are produced by a r i d land p l a n t s . These n a t u r a l products, which are stored in g l a n d u l a r h a i r s (trichomes), i n c l u d e t e r p e n o i d s , alkaloids, phenolics and amines. Some of these compounds coat the l e a f and stem surfaces and prevent water l o s s through the cuticle and probably p r o t e c t the p l a n t from excessive damage by radiation. Another important e c o l o g i c a l r o l e of secondary metabolites is that of defense against phytophagous i n s e c t s and pathogens. Recent phytochemical i n v e s t i g a t i o n s in our l a b o r a t o r y i n d i c a t e t h a t chromenes, prenylated quinones and sesquiterpenes e s t e r i f i e d w i t h phenolic a c i d s , are e x c e l l e n t r e p e l l e n t s and in some cases are c y t o t o x i c and inhibit larval growth and development. The chemistry and r o l e of these c y t o t o x i n s and insecticides in desert p l a n t s of Baja California and Chihuahua is reviewed.

Deserts cover approximately one-seventh of the earth's land s u r f a c e , w i t h the North American deserts populated by a d i v e r s i t y of b i z a r r e plant l i f e forms ranging from c a c t i to creosote bushes to the boojum t r e e s of Baja C a l i f o r n i a , Mexico. An outstanding c h a r a c t e r i s t i c of a m a j o r i t y of p l a n t s that dominate the desert landscape i s t h e i r enormous photosynthetic c a p a c i t y to produce an array of secondary metabolites • Many of these n a t u r a l products are e s s e n t i a l t o the everyday s u r v i v a l o f p l a n t s exposed t o the harsh, hot and d r y environment of the d e s e r t . These n a t u r a l products, which i n c l u d e t e r p e n o i d s , a l k a l o i d s , p h e n o l i c s , amines and tannins are produced i n l a r g e q u a n t i t i e s by s p e c i a l i z e d glandular h a i r s c a l l e d trichomes and coat l e a f , stem and flower surfaces • This t h i n l a y e r of secondary chemicals are b e l i e v e d t o prevent water l o s s ( a n t i d e s s i c a n t s ) through the c u t i c l e and i n some cases prevent excessive c e l l damage by b l o c k i n g u l t r a v i o l e t 0097-6156/ 83/0208-0291 $ 0 6 . 0 0 / 0 © 1983 American Chemical Society

Hedin; Plant Resistance to Insects ACS Symposium Series; American Chemical Society: Washington, DC, 1983.


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r a d i a t i o n . More important, these b i o l o g i c a l l y a c t i v e c o n s t i t u e n t s a l s o r e p e l and i n some cases k i l l phytophagous i n s e c t s and plant pathogens. I t i s the desert a l l e l o c h e m i c a l s ( c o n s t i t u e n t s which have a d e l e t e r i o u s e f f e c t on herbivorous i n s e c t s and pathogens) which are of considerable i n t e r e s t to phytochemists concerned w i t h c o n t r o l l i n g i n s e c t pests of crop p l a n t s . With the current a g r i c u l t u r a l development of desert hydrocarbon crop plants,such as guayule (Parthenium argentatum) and j o j o b a (Simmondsia c h i n e n s i s ) , i t i s important that a l i n e of n a t u r a l i n s e c t i c i d e s and r e p e l l e n t s be developed against i n s e c t s e s p e c i a l l y adapted to p l a n t s c u l t i v a t e d i n marginal a r i d lands (1_) • In t h i s communication, we present our l a t e s t phytochemical f i n d i n g s on prenylated quinones and chromenes that are c y t o t o x i c and i n h i b i t l a r v a l growth and development. Many of these b i o a c t i v e chemicals are unique to desert p l a n t s and have probably been s e l e c t e d against desert i n v e r t e b r a t e s that feed on p l a n t s • Desert P l a n t s and Their Secondary M e t a b o l i t e s As p r e v i o u s l y noted, desert p l a n t s are no d i f f e r e n t from temperate p l a n t s i n producing a wide-range of secondary metabolites (2)« Dominant p l a n t species such as Larrea t r i d e n t a t a (Zygophyllaceae) may contain up to 15% of the dry weight i n l i g n a n s , f l a v o n o i d s , chromenes, t r i t e r p e n e s and v o l a t i l e terpenes ( 3 ) . Important desert f a m i l i e s i n c l u d e the Asteraceae, Fabaceae, Agavaceae, Burseraceae, Euphorbiaceae and Fonquieriaceae which synthesize d i v e r s e products such as sesquiterpene l a c t o n e s , methylated f l a v o n o i d s , p o l y a c e t y l e n e s , s t e r o i d s , saponins, a l k a l o i d s , cyanogenic g l y c o s i d e s , aromatic terpenes and amines ( r e f e r to Figure 1 and 2 f o r r e p r e s e n t a t i v e s t r u c t u r e s ) . These n a t u r a l products are not only used by n a t i v e peoples f o r medicines, food and n a t u r a l a n t i b i o t i c s , but many of these compounds are very e f f e c t i v e against a host of i n s e c t s and pathogens ( 4 ) . In our s t u d i e s we have concentrated on prenylated quinones and chromenes that are present i n desert species of the Asteraceae and Hydrophyllaceae. In the ensuing paragraphs we summarize the chemistry and b i o l o g i c a l e f f e c t s of a s e l e c t e d group of quinones and chromenes that are c y t o t o x i c and i n s e c t i c i d a l to milkweed bugs (Oncopeltus) and mealworm beetles (Tenebrio)• Prenylated Quinones Quinonoid compounds are q u i t e common throughout the plant kingdom, but only i n a few cases have they been reported i n glandular h a i r s (trichomes) of desert herbaceous p l a n t s . Many of these quinonoid compounds are extremely a c t i v e and are the major cause of a l l e r g i c r e a c t i o n s i n humans• For example, Primula obconica (Primulaceae), an ornamental p l a n t common to Europe, produces a quinone which i s stored i n small non-capitate trichomes which r e l e a s e t h e i r contents when touched. These


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Flourensia Acid Sesquiterpene Flourensia cernua

Figure 1.

Farinosin Sesquiterpene Lactone Encelia forinosa

Terpenoid constituents of desert plants.


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Nordihydroguairetic Acid Lignan

Phenylethylamines Cactaceae Figure 2.

Phenolic and alkaloid constituents of desert plants.



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secreted chemicals are very e f f e c t i v e a g a i n s t aphids that c r a w l on the l e a f . These chemicals, l i k e the s e c r e t i o n of Solanum tuberosum (Solanaceae), hardens on mouth parts and t a r s i of i n s e c t s and i n h i b i t s movement and f e e d i n g (5-6)• Recently we have i s o l a t e d a s e r i e s of p r e n y l a t e d quinones and quinonoid compounds from the v i s c i d c a p i t a t e - g l a n d u l a r trichomes of P h a c e l i a (Hydrophyllaceae) that are c y t o t o x i c , a l l e r g e n i c and i n s e c t i c i d a l . Most o f the species noted t o have the prenylated quinones are r e s t r i c t e d t o the Sonoran desert o f Baja C a l i f o r n i a , Mexico and the Mojave desert o f the Southwest (7-10). P h a c e l i a c r e n u l a t a , an annual which i s common along desert roadsides i n the southwestern United States and northern Mexico, i s r e s p o n s i b l e f o r a d e r m a t i t i s s i m i l a r t o that of poison oak, but i s i s a l s o been demonstrated t o i n h i b i t l a r v a l f o r m a t i o n . The e f f e c t s are s i m i l a r t o those noted f o r milkbugs (Oncopeltus) t r e a t e d w i t h the precocenes, compounds w e l l - n o t e d f o r t h e i r a n t i - j u v e n i l e a c t i v i t y ( 1 1 ) . The p r i n c i p a l c o n s t i t u e n t s are geranylhydroquinone ( I ) and i n l e s s e r amounts geranylbenzoquinone ( H ) ( 8 ) . Both compounds are new n a t u r a l products t o higher p l a n t s , but have been reported i n marine urochordates ( 1 2 ) . Compound ( I ) has been synthesized as a drug and found t o have cancer p r e v e n t i v e p r o p e r t i e s i n experimental animals ( 1 3 ) . Another s p e c i e s , V_. Ixodes from Baja C a l i f o r n i a , Mexico c o n t a i n s numerous quinones i n the trichomes (10)• The compounds have been i d e n t i f i e d as geranylhydroquine ( I ) , 3-geranyl-2,5-dihydroxyphenyl a c e t a t e ( I I I ) , geranylbenzoquinone ( I I ) , 2-geranyl-6-hydroxy-4-methoxyphenyl acetate ( I V ) , 2-geranyl-4-hydroxyphenyl a c e t a t e (V) and 6-hydroxy-2-methyl-2,4-methyl-3-pentenyl)-chromene ( V I ) . Compounds ( I ) through (IV) were assayed f o r t h e i r c y t o t o x i c and a l l e r g e n i c p o t e n t i a l on guinea p i g s , which are e f f e c t i v e i n d i c a t o r s of contact a l l e r g e n i c i t y i n humans ( 1 0 ) . The same compounds were a l s o tested on Tenebrio sp. (mealworm b e e t l e s ) , an experimental i n s e c t used t o t e s t the p o t e n t i a l of i n s e c t i c i d e s • Geranyl-benzoquinone proved t o be a very potent e l i c i t o r of a l l e r g i c s k i n r e a c t i o n s as w e l l as a potent i n s e c t i c i d e ( 1 0 ) • A t o p i c a l a p p l i c a t i o n of 100>*g of geranylbenzoquinone on pupae of Tenebrio caused severe a b n o r m a l i t i e s and death. Although the exact mechanism of t o x i c i t y f o r ( I I ) i s not known, i t s s i m i l a r i t y to the j u v e n i l e hormones suggests t h a t ( I I ) might be a powerful a l k y l a t o r of enzymes r e g u l a t i n g j u v e n i l e hormone s y n t h e s i s . Compound (VI) was not as potent as ( I I ) , but previous r e p o r t s of (VI) i n C o r d i a a l l i o d o r a (Boraginaceae) i n d i c a t e that (VI) i s a l s o an e f f e c t i v e i n s e c t i c i d e ( 1 4 ) . Two species of P h a c e l i a , P. minor and p a r r y i , widespread throughout the semi-arid mountains o f southern C a l i f o r n i a contained as the major c o n s t i t u e n t geranylgeranylhydroquinone ( V I I ) . A minor c o n s t i t u e n t , 2-(-l-oxofarnesyl)-hydroquinone ( V I I I ) was a l s o present and p r e v i o u s l y reported i n a brown a l g a (15) and Wigardia k u n t h i i o f the f a m i l y Hydrophyllaceae ( 1 6 ) .






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Geranylgeranylhydroquinone ( V I I ) was a p p l i e d ( l O O x g ) to f i f t h i n s t a r s of Oncopeltus (milkbugs) and found t o stunt growth and wing development. It i s apparent from our i n v e s t i g a t i o n s of prenylated quinones from desert annuals, that these compounds are not only potent s k i n s e n s i t i z e r s but a l s o p o t e n t i a l i n s e c t i c i d e s . The t o x i c i t y of the prenylated quinones i s i n part due to t h e i r l i p o p h i l i c i t y which permits the compounds t o penetrate the c u t i c l e and a l k y l a t e important metabolic enzymes. Another p o s s i b l e e x p l a n a t i o n f o r t h e i r a n t i j u v e n i l e a c t i o n i s that the prenylated quinones are transformed i n t o a quinone methide species which mimic the j u v e n i l e hormones (JH) and p o s s i b l y i n t e r f e r e w i t h the p r o d u c t i o n of JH o r d e a c t i v a t e the hormones• Chromenes i n the Asteraceae In a recent l i t e r a t u r e survey of chromenes and benzofurans i n f l o w e r i n g p l a n t s , we have documented that approximately 90% of the 200 compounds i s o l a t e d are present i n the sunflower f a m i l y (Asteraceae). These n a t u r a l l y o c c u r r i n g chemicals have r e c e n t l y received considerable a t t e n t i o n because of t h e i r potent c y t o t o x i c and i n s e c t i c i d a l a c t i v i t y . Chemotaxonomically, not a l l t r i b e s of the Asteraceae seem to produce chromenes or benzofurans, w i t h the major t r i b e s capable o f s y n t h e s i z i n g chromenes i d e n t i f i e d as the E u p a t o r i e a e , H e l i a n t h e a e , I n u l e a e , Senecioneae and the Astereae (17)• The chromenes and benzofurans are r a t h e r simple compounds b u i l t from acetate and isoprene m e t a b o l i t e s . H e t e r o c y c l i c r i n g formation gives r i s e to 2,2-dimethyl chromene or 2-isoprophenyl benzofurans. The m a j o r i t y of known chromenes and benzofurans e x h i b i t a methyl ketone moiety a t a p o s i t i o n para to the oxygen of the h e t e r o c y c l i c r i n g . C o n s t i t u e n t s e s t e r i f i e d w i t h phenolic a c i d s or l a c k i n g methyl ketones are r a r e . The chromenes are well-known f o r t h e i r c y t o t o x i c and a n t i j u v e n i l e a c t i v i t y i n i n s e c t s (18-19). The prococenes, simple chromenes f i r s t i s o l a t e d from Ageratum (Asteraceae), have been shown to act d i r e c t l y on the corpus a l l a t u m by d i r e c t c y t o t o x i c d e s t r u c t i o n o f the parenchymal c e l l s ( 2 0 ) . The precocenes, when a p p l i e d e x t e r n a l l y t o the second i n s t a r l a r v a e of the milkweed bug (Oncopeltus f a s c i a t u s ) cause the nymphs t o molt to normal t h i r d and f o u r t h i n s t a r l a r v a e , and then to precocious a d u l t s • Recent biochemical s t u d i e s have suggested that the precocenes undergo o x i d a t i v e a c t i v a t i o n w i t h the corpus alluatum and form r e a c t i v e epoxides that a l k y l a t e n u c l e o p h i l i c s u b s t r a t e s . The r e a c t i v e precocene intermediate i s suggested to be the quinone methide ( 2 0 ) , a s i m i l a r r e a c t i v e species that we have proposed for the prenylated quinones o f P h a c e l i a . Although considerable i n f o r m a t i o n has been gathered on c y t o t o x i c and a n t i j u v e n i l e a c t i o n of the precocenes, l i t t l e information i s a v a i l a b l e on the d i s t r i b u t i o n of chromenes and


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benzofurans i n desert p l a n t s and t h e i r p o s s i b l e r o l e as phototoxic agents and feeding d e t e r r e n t s . With t h i s i n mind, we have begun a d e t a i l e d phytochemical i n v e s t i g a t i o n of chromenes and benzofurans i n dominant desert shrubs of the Sonoran and Chihuahuan deserts that are c y t o t o x i c , phototoxic and insecticidal.


Chromenes and Benzofurans i n Desert Shrubs Using HPLC, we have surveyed i n d e t a i l taxa of E n c e l i a , F l o u r e n s i a , and Geraea. A l l of these genera were found to produce l a r g e q u a n t i t i e s of chromenes and benzofurans (21)• I n the genus E n c e l i a , chromenes can comprise up to 10% of the d r y weight m a t e r i a l . The compounds are more common i n l e a v e s , but have been detected i n the stem, f l o w e r i n g heads and i n some cases i n seeds • A d e t a i l e d q u a n t i t a t i v e study of the chromenes has been conducted on E n c e l i a f a r i n o s a ( b r i t t l e b u s h ) , a desert shrub common throughout Baja C a l i f o r n i a , Sonora and southern C a l i f o r n i a . The major chromene was i d e n t i f i e d as e n c e c a l i n ( I X ) , but a l s o present was the benzofuran euparin (X) which i s p r i m a r i l y produced i n the stems (22). A p p l i c a t i o n of e n c e c a l i n t o the f i r s t i n s t a r of l a r v a e of the milkweed bug proved t o be moderately i n s e c t i c i d a l . E n c e c a l i n , euparin, and 7-hydroxyencecalin (XI) were d i s s o l v e d i n methanol and were a p p l i e d a t concentrations 5 mg-lOOj^g. Each p e t r i d i s h contained 25-30 f i r s t i n s t a r l a r v a e of (). f a s c u l a t u s . Concentrations of 1.2 mg/petri d i s h (or higher) of e n c e c a l i n were l e t h a l to the l a r v a e w i t h i n a p e r i o d of three days. Lesser concentrations of e n c e c a l i n showed no e f f e c t s , w h i l e euparin and 7-hydroxyencecalin was not t o x i c (23)• E n c e c a l i n does not compare i n t o x i c i t y w i t h the precocenes, s i n c e 44ju-g of precocene I I have been reported t o induce precocious metamorphosis i n milkweed bug l a r v a e . The presence of a methylketone moiety i n e n c e c a l i n i n s t e a d of a methoxy s u b s t i t u e n t probably r e s u l t s i n a l o s s of a n t i j u v e n i l e a c t i v i t y noted f o r the precocenes. On the other hand, 7-hydroxyencecalin was l e s s a c t i v e than e n c e c a l i n and t h i s could be due to a more r a p i d d e t o x i f i c a t i o n of phenolic compounds e x h i b i t i n g f r e e hydroxyl groups r a t h e r than methoxyl groups (23). As a feeding d e t e r r e n t , e n c e c a l i n was more a c t i v e . F i f t h i n s t a r s of H e l i o t h i s zea (Lepidoptera) were exposed t o a r t i f i c i a l d i e t s c o n t a i n i n g v a r y i n g amounts of e n c e c a l i n . At concentrations of 0.35%, H. zea starved t o death (24). I t should be noted that e n c e c a l i n i s present i n higher amounts i n the l e a v e s , t h e r e f o r e suggesting that e n c e c a l i n and other l e s s c y t o t o x i c chromenes and benzofurans are feeding d e t e r r e n t s . I t should be added that most desert phytophagous i n s e c t s e i t h e r chew or suck p l a n t parts and therefore are l i k e l y t o be r e p e l l e d before they consume the chromenes. T o p i c a l a p p l i c a t i o n s are l e s s l i k e l y , but one could speculate that the a c c i d e n t a l r u p t u r i n g of glandular h a i r s could


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r e s u l t i n the d e p o s i t i o n of a c t i v e c y t o t o x i n s on an i n s e c t cuticle• A n a l y s i s of the stems of E n c e l i a ventorum from Baja C a l i f o r n i a showed the presence of a number of benzopyran and benzofuran d e r i v a t i v e s and two stereo isomers of a novel e u p a r i n - e n c e c a l i n ( X I I ) dimer (25). A closely related euparin-encecalin dimer ( X I I I ) , was p r e v i o u s l y i s o l a t e d from E. f a r i n o s a (26)* Although the dimer i s not photoactive, p r e l i m i n a r y s t u d i e s i n d i c a t e that i t i s a feeding deterrent to H e l i o t h i s zea. The benzofuran 6-methoxyeuparin (XIV) and the two chromenes e n c e c a l i n and 7-hydroxyencecalin from species of E n c e l i a (Asteraceae) from Baja C a l i f o r n i a have been shown to be phototoxic to s e v e r a l b a c t e r i a and yeast i n long wave UV l i g h t (23). Compound (XIV) was the most a c t i v i t y against Pseudomonas f l u o r e s c e n s , an organism that i s not a f f e c t e d by the potent p h o t o s e n s i t i z e r 8-methoxypsoralen ( 2 7 ) . The three compounds were a c t i v e against Saccharomyces c e r e v i s i a e and Candida a l b i c a n s . P r e l i m i n a r y experiments w i t h human erythrocytes w i t h t h i s new c l a s s of p h o t o s e n s i t i z e r s r u l e s out the membrane as a t a r g e t , since the chromenes seem to behave l i k e the p h o t o s e n s i t i z i n g furanocoumarins by i n t e r a c t i n g w i t h n u c l e i c acids or i n t r a c e l l u l a r molecules i n l i g h t • Further experimentation i s needed to c l e a r l y understand t h e i r mode of a c t i o n . Numerous chromenes and benzofurans have a l s o been i s o l a t e d from F l o u r e n s i a , a genus that i s dominant i n the desert of Chihuahua, Mexico. A benzofuran (XV) w i t h a cinnamic a c i d moiety from F^. dentata and i l i c i f o l i a has r e c e n t l y been shown to be extremely t o x i c to m i l k weed bugs and h i g h l y phototoxic (28). Approximately 30 chromenes and benzofurans have been i s o l a t e d from other desert sunflowers and we are c u r r e n t l y screening them f o r i n s e c t i c i d a l and phototoxic a c t i v i t y . Concluding Remarks Desert p l a n t s are remarkable phytochemical f a c t o r i e s • In t h i s chapter, we have covered only two c l a s s e s of compounds; chromenes and prenylated quinones that are a l l e r g e n i c , c y t o t o x i c and i n s e c t i c i d a l . Many other desert p l a n t s produce r e s i n s that are complex mixtures of s e s q u i t e r p e n o i d s , chromenes, f l a v o n o i d s and quinones. These mixtures might not be of i n t e r e s t to phytochemists, but to the p l a n t , secondary metabolites are e s s e n t i a l f o r s u r v i v a l and r e p r o d u c t i o n . L i k e the chromenes and quinones, many n a t u r a l c o n s t i t u e n t s of a r i d land plants play a dual r o l e . In some cases, the n a t u r a l products excreted on the l e a f or secreted by trichomes are f u n c t i o n i n g as a n t i d e s s i c a n t s (prevent water l o s s through the c u t i c l e ) , p r o t e c t i n g the l e a f from harmful r a d i a t i o n and, most important, keeping the plant healthy against phytophagous i n s e c t s and pathogens. The chromenes and benzofurans are chemicals that are antifeedants and e x h i b i t



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a n t i j u v e n i l e a c t i v i t y when a p p l i e d t o p i c a l l y . The chromenes are p r i m a r i l y r e s t r i c t e d t o members o f the Asteraceae and are more widespread i n desert sunflower species than p r e v i o u s l y thought. In combination w i t h sesquiterpene l a c t o n e s , the chromenes and benzofurans are another group of defensive compounds that desert i n v e r t e b r a t e s have to d e t o x i f y . Indeed, the success of many desert sunflower species i s i n part due t o t h e i r d i v e r s e secondary chemistry. P r e n y l a t e d quinones, on the other hand seem t o be r e s t r i c t e d to the Hydrophyllaceae and t r o p i c a l t r e e s . The quinones are extremely a c t i v e chemicals that e x h i b i t i n s e c t i c i d a l a c t i v i t y a t c o n c e n t r a t i o n s lower than many chromenes• The prenylated quinones of P h a c e l i a are a l s o potent c y t o t o x i n s and allergens• Acknowledgement s This research has been supported by NIH Grant A l 18398, NSF PCM-8209100 and the Focused Research Program a t UCI. I am g r e a t l y indebted to my research a s s o c i a t e s and colleagues c i t e d i n the r e f e r e n c e s , namely, Dr. G.H.N. Towers (UBC, Canada), Dr. Gary Reynolds (LSU), Dr. Peter Proksch (UCI), Charles Wisdom (UCI), Manuel A r e g u l l i n (UCI) and Margareta Proksch (UCI). Literature Cited 1.

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