Plant Resistance to Insects - American Chemical Society

5 Function and Chemistry of Plant Trichomes and Glands in Insect Resistance Protective Chemicals in Plant Epidermal Glands and Appendages ROBERT D. STIPANOVIC

Downloaded by COLUMBIA UNIV on April 7, 2013 | http://pubs.acs.org Publication Date: January 20, 1983 | doi: 10.1021/bk-1983-0208.ch005

U.S. Department of Agriculture, Agricultural Research Service, National Cotton Pathology Research Laboratory, P.O. Drawer JF, College Station, T X 77841

Plants have developed various mechanisms of defense against phytophagus insects. Two defensive morphological features are trichomes and glands. Trichomes may be h a i r - l i k e or glandular. Plant hairs act as physical barriers keeping smaller insects away from the leaf surface. Glandular trichomes and plant glands may exude a sticky substance that entraps and immobilizes small insects, or they may contain toxic constitutents which spill into the surrounding tissue when the gland is ruptured, making it unpalatable or t o x i c . These toxins are generally weak and do not kill the insect d i r e c t l y , rather they retard insect growth and delay pupation. As a result, the insects are more vulnerable to disease, predation, and the environment. The balance which has evolved between plants and insects could be seriously disrupted if secondary plant toxin analogs are synthesized and used as insecticides. Insects developing resistance to the analogs might develop resistance to the natural toxin. P l a n t s have served as a food source f o r f i s h , i n s e c t s , and mammals s i n c e e a r l y b i o t i c times. I n response p l a n t s have developed i n t r i c a t e p h y s i c a l as w e l l as chemical p r o t e c t i v e mechanisms. The two defensive s t r u c t u r e s that are the primary subject of t h i s chapter are trichomes and glands. Trichomes are epidermal appendages o f d i v e r s e form and s t r u c t u r e , such as p r o t e c t i v e and g l a n d u l a r h a i r s and s c a l e s or p e l t a t e h a i r . H a i r s , whether they are u n i c e l l u l a r , m u l t i c e l l u l a r , o r p e l t a t e , may be g l a n d u l a r . Glandular trichomes e l a b o r a t e v a r i o u s substances, such as v o l a t i l e o i l s , r e s i n s , mucilages, and gums. Rupture of the c u t i c l e a l l o w s the g l a n d u l a r contents t o escape. Other types of glands are a l s o found on the s u r f a c e o f the p l a n t . These i n c l u d e : 1) the g l a n d u l a r epidermis c o v e r i n g the l e a f t e e t h as found i n Primus; 2) nectary glands which produce a This chapter not subject to U . S . copyright. Published 1983 American Chemical Society. In Plant Resistance to Insects; Hedin, P.; ACS Symposium Series; American Chemical Society: Washington, DC, 1983.


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sugary s e c r e t i o n a s s o c i a t e d w i t h flowers and other p l a n t p a r t s ; 3) glandular e x c r e t o r y s t r u c t u r e s which discharge a v a r i e t y of o i l s and r e s i n s ; 4) o i l glands which c o n t a i n v a r i o u s terpenoid oils. The u t i l i t y of secondary plant chemicals as defensive agents against pest a t t a c k has only r e c e n t l y been widely accepted. However, t h i s view i s s t i l l not u n i v e r s a l l y accepted as i l l u s t r a t e d by Luckner's (1) recent comment: "....secondary metabolism i s c h a r a c t e r i z e d by a high degree of order, i . e . by the p r e c i s e r e g u l a t i o n of enzyme l e v e l and a c t i v i t y i n metabolic pathways, the compartmentation and channeling of enzymes, p r e c u r s o r s , i n t e r m e d i a t e s , and products as w e l l as the i n t e g r a t i o n of secondary metabolism i n the programs of c e l l s p e c i a l i z a t i o n of the producer organism. However, c h a r a c t e r i s t i c s of secondary metabolism are a l s o the b i z a r r e chemical s t r u c t u r e s of the formed products, the r e s t r i c t e d occurrence of the d i f f e r e n t secondary compounds w i t h i n groups of l i v i n g beings and t h e i r usefulness which u s u a l l y i s s m a l l or absent, i . e . , p r o p e r t i e s which g i v e secondary metabolism i t s e r r a t i c features." However, I b e l i e v e t h i s and other chapters w i l l more than adequately show that secondary p l a n t chemicals were and s t i l l are important weapons i n the p l a n t s a r s e n a l of defense. The f o l l o w i n g pages review the f u n c t i o n and chemistry of trichomes and glands. The concluding s e c t i o n s address the i n s e c t ' s response to the p l a n t ' s defensive chemicals, and end w i t h an appeal to the chemical p e s t i c i d e i n d u s t r y . E x t r a f l o r a l Nectaries I t i s g e n e r a l l y conceded that f l o r a l n e c t a r i e s evolved as an a t t r a c t a n t to p o l l i n a t i n g i n s e c t s . The f u n c t i o n of e x t r a f l o r a l n e c t a r i e s i s not so obvious. Some suggest that the s e c r e t i o n of sugars i s a s s o c i a t e d w i t h a s h i f t from a " s i n k " t o a "source" of carbohydrates during development (2^, 3) • Others propose that sugars are excreted i n c i d e n t a l to the e x c r e t i o n of water and s a l t s (4, _5, 6 ) . However, B. L. Bentley c o n v i n c i n g l y argues i n her review that e x t r a f l o r a l n e c t a r i e s are a t t r a c t a n t s f o r ants which act as "pugnacious body guards" i n defense of the p l a n t (7_). She bases t h i s contention on f o u r observations. 1) E x t r a f l o r a l n e c t a r i e s f o l l o w no recognizable d i u r n a l p a t t e r n and produce nectar throughout the day and n i g h t . 2) A c t i v e n e c t a r i e s are found on younger p o r t i o n s of the p l a n t and are o f t e n a s s o c i a t e d with developing reproductive organs. The n e c t a r i e s are f u l l y developed before the reproductive organ, and s e c r e t i o n ceases soon a f t e r the organ matures. 3) Secretory a c t i v i t y i s u s u a l l y greatest at the height of the growing season and may continue throughout the year i n moist t r o p i c a l r e g i o n s . 4)

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


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Attack by sucking i n s e c t s o f t e n increases the r a t e o f s e c r e t i o n i n a p o s i t i v e l y c o r r e l a t e d manner w i t h increased i n f e s t a t i o n l e v e l s . Bentley argues that n e c t a r i e s f r e q u e n t l y remain a carbohydrate source u n t i l m a t u r i t y , w h i l e developing buds, f l o w e r s , and f r u i t never become a carbohydrate source; sucking i n s e c t s reduce the carbohydrate source pressure o f an organ and yet nectar s e c r e t i o n s increase w i t h i n c r e a s i n g i n f e s t a t i o n s . Thus, the source/sink hypothesis does not seem to apply. In Catalpa, E l i a s and Newcombe report that glandular trichomes on leaves are not only very s i m i l a r t o n e c t a r i e s but are t h e i r precursors ( 8 ) . These authors propose these m u l t i p l e n e c t a r i e s i n the lower l e a f surface v e i n a x i e s act as a t t r a c t a n t s f o r b e n e f i c i a l i n s e c t s t o c o n t r o l o r minimize the e f f e c t s of herbivorous i n s e c t s . Predatory ants are g e n e r a l l y considered t o be b e n e f i c i a l i n s e c t s . T h e i r presence on p l a n t s c o n t a i n i n g e x t r a f l o r a l n e c t a r i e s i s a widely observed phenomena. However, these mercenaries are h i r e d a t a c o s t . For example, C u r t i s and L e r s t e n report that one o f the most d e v a s t a t i n g i n s e c t s observed to be feeding on cottonwood (Populus d e l t o i d e s ) was an Aphis species herded by an u n i d e n t i f i e d species o f l a r g e black ant ( 9 ) . Thus, t h i s "body guard" may "pugnaciously" defend the p l a n t from some pests only to usher i n a plant pest o f i t s choosing. Trichomes as a Form of P h y s i c a l Resistance In medieval times, c i t i e s commonly erected w a l l s as a p r o t e c t i v e b a r r i e r t o i n v a s i o n . P l a n t s have evolved s i m i l a r p r o t e c t i v e mechanisms. Thorns and n e t t l e s which r e p e l most herbivores are two examples o f p r o t e c t i v e b a r r i e r s . To ward o f f i n s e c t a t t a c k , p l a n t s have evolved non-glandular trichomes which act i n a s i m i l a r f a s h i o n . Thus, i n some p l a n t s , the d e n s i t y , l e n g t h , o r branching o f trichomes have been n e g a t i v e l y c o r r e l a t e d w i t h i n s e c t s u r v i v a l (10). The degree of l e a f pubescence g r e a t l y a f f e c t s the behavior of c e r e a l l e a f b e e t l e g r a v i d females, Oulema melanopus (11). Densely pubsecent wheat had only o n e - t h i r d as many eggs as the glabrous c o n t r o l . On pubescent leaves i t was o f t e n found that eggs were l a i d i n areas where a d u l t s had d i s r u p t e d the trichome cover by feeding. F i e l d cage t e s t s showed that the v i a b i l i t y o f eggs decreased w i t h i n c r e a s i n g pubescence. Eggs l a i d o r mechanically placed on pubescent wheats were more s u s c e p t i b l e t o d e s i c c a t i o n . L a r v a l s u r v i v a l and weight g a i n were a l s o minimized on densely pubescent leaves (12). This was e s p e c i a l l y true i n f i r s t - i n s t a r l a r v a e , w h i l e t h i r d - i n s t a r and f o u r t h - i n s t a r l a r v a e were l i t t l e a f f e c t e d by pubescence. However, long o r dense trichomes d i d not c o r r e l a t e i n a greenhouse t e s t w i t h r e s i s t a n c e of wheat t o greenbug, Schizaphis graminum (13). A h a i r y c o t t o n v a r i e t y that had the most trichomes, the longest trichomes, and the most branched trichomes was the most r e s i s t a n t t o s p i d e r mites and leafhoppers (14). I n a no-choice




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cage t e s t w i t h three cotton i s o l i n e s , Lygus herperus o v i p o s i t i o n response was h i g h e s t , but growth r a t e slowest on densely pubescent c o t t o n as compared t o normal and smooth cottons ( 1 5 ) • Nymphal s u r v i v a l was e s s e n t i a l l y equal on a l l l i n e s , but the e f f e c t o f predators was not a f a c t o r i n these cage t e s t s . However, pubescence i s not always an advantage t o p l a n t s , as i l l u s t r a t e d by the g r e a t e r r e s i s t a n c e of smooth l e a f c o t t o n t o fleahoppers ( 1 6 ) • Hooked trichomes on the French bean, Phaseolus v u l g a r i s have been reported t o capture a d i v e r s e group of i n s e c t species i n c l u d i n g the potato leafhopper, Empoasca fabae ( 1 7 ) , and the aphids, Myzus p e r s i c a e ( 1 8 ) , Aphis fabae ( 1 9 ) , and Aphis c r a c c i v o r a (20). A recent study has shown t h a t the major f a c t o r a f f e c t i n g potato leafhopper damage on the French bean was the d e n s i t y of hooked trichomes ( 2 1 ) . Leafhopper nymphs were impaled by the trichomes, l e a d i n g t o wounding and eventual death. This same p o s i t i v e c o r r e l a t i o n between capture m o r t a l i t y and trichome d e n s i t y a l s o has been reported f o r a d u l t leafhoppers on f i e l d bean c u l t i v a r s , J?, v u l g a r i s and P. lunatus ( 2 2 ) . Hooked trichomes growing a t angles l e s s than 3 0 ° are r e p o r t e d l y i n e f f e c t i v e i n c a p t u r i n g leafhoppers. The i n h e r i t a n c e o f pubescence type ( 2 3 ) and the morphology of pubescence i n soybean, G l y c i n e max, have been s t u d i e d , and densely pubescent p l a n t s were found t o be the most vigorous ( 2 4 ) . Growth d i f f e r e n c e s were a s s o c i a t e d w i t h IS. fabae i n f e s t a t i o n s . Glabrous soybeans supported a higher p o p u l a t i o n o f IS. fabae and had a higher i n c i d e n c e of o v i p o s i t i o n than pubescent v a r i e t i e s ( 2 5 , 2 6 ) . This same o b s e r v a t i o n has been made on other pubescent host p l a n t s ( 1 7 ) . The d i f f e r e n c e s i n populations of E. fabae were r e l a t e d t o o r i e n t a t i o n , l e n g t h , and the erectness of the l e a f trichomes ( 2 7 , 2 8 ) . When populations of E. fabae, which i s 1.0 - 4 . 0 mm i n l e n g t h , were compared t o t h a t of a s p r i n g t a i l , Deuterosmiathurus yumanensis, which i s 0 . 2 - 0 . 4 mm i n l e n g t h , on near i s o g e n i c l i n e s o f soybean, i t was found that both species had the highest populations on the glabrous genotype. On a deciduous v a r i e t y , w i t h only misshapen and s e v e r e l y appressed trichomes, the p o p u l a t i o n o f the s m a l l phytophagus species was depressed, w h i l e t h a t o f the l a r g e r species was not a f f e c t e d . Populations of E>. fabae decreased w i t h i n c r e a s i n g trichome l e n g t h ( 0 . 9 - 1 . 6 mm) r e g a r d l e s s o f trichome d e n s i t y , whereas the s p r i n g t a i l s p o p u l a t i o n decreased w i t h i n c r e a s i n g trichome d e n s i t y . The populations o f t h r i p s , S e r i c o t h r i p s v a r i a b i l i s , and bandedwing w h i t e f l y , T r i a l e u r o d e s a b u t i l o n e a , showed no c o n s i s t e n t response t o trichome v a r i a t i o n s ( 2 9 ) . f

Trichomes and Glands as a Form o f Chemical Resistance In a d d i t i o n t o p h y s i c a l forms o f r e s i s t a n c e , p l a n t s a l s o r e l y on chemicals t o immobilize, r e p e l and poison phytophagus i n s e c t s . These chemicals may be l o c a t e d i n v a r i o u s types of o i l



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or secretory glands or i n g l a n d u l a r trichomes. Glandular h a i r s or trichomes are widely d i s t r i b u t e d i n v a s c u l a r p l a n t s . A c a r e f u l h i s t o c h e m i c a l study showed that 39 o f 43 p l a n t species from 26 d i f f e r e n t p l a n t s f a m i l i e s had stem h a i r s (30). Some o f these p l a n t s , such as tomato, had s e v e r a l morphologically d i s t i n c t h a i r s . P l a n t h a i r s are a l s o chemically d i s t i n c t as evidenced by t h e i r r e a c t i o n w i t h v a r i o u s h i s t o c h e m i c a l reagents. Reviews on the i n t r a c e l l u l a r compartmentation o f f l a v o n o i d s and other secondary metabolites have been published (31, 32). A review on the chemical c o n s t i t u e n t s o f these glands i s complicated by a number o f f a c t o r s . The d i v e r s i t y and the complexity o f chemicals produced i n a gland o r trichome a r e two such f a c t o r s . However, one of the most formidable o b s t a c l e s t o a review .on g l a n d u l a r c o n s t i t u e n t s i s the d e t a i l s reported on the e x t r a c t i o n procedure. I t i s common f o r i n v e s t i g a t o r s t o simply d i v i d e the p l a n t i n t o i t s obvious components, e.g. r o o t s , f o l i a r p a r t s , flowers and buds, stems, bark, e t c . When examining l e a v e s , f o r example, there i s o f t e n no attempt t o d i f f e r e n t i a t e between v a r i o u s morphological e n t i t i e s . The l e a f i s ground o r e x t r a c t e d whole. A l l evidence i n d i c a t i n g the occurrence of a p a r t i c u l a r chemical i n a trichome o r gland i s o b l i t e r a t e d . In the study o f r e s i s t a n c e mechanisms, i t i s recognized t h a t the l o c a t i o n of a p a r t i c u l a r t o x i c chemical may be as important as the presence o r absence o f t h a t chemical. For example, a h i g h c o n c e n t r a t i o n of a t o x i c chemical i n a p l a n t part that the i n s e c t does not e a t o r eats only i n the l a t e r stages o f l a r v a l growth, w i l l probably have minimal a f f e c t on the r e s i s t a n c e of that p l a n t to i t s host. Conversely, a low c o n c e n t r a t i o n o f a t o x i c chemical i n a s p e c i f i c s i t e a t which the i n s e c t feeds i n an e a r l y l a r v a l stage may s i g n i f i c a n t l y a f f e c t the p l a n t ' s r e s i s t a n c e . In h o s t - p l a n t r e s i s t a n c e s t u d i e s , i t i s t h e r e f o r e imperative f o r i n v e s t i g a t o r s t o r e p o r t not o n l y what chemicals are present, but a l s o t o r e p o r t as a c c u r a t e l y as p o s s i b l e the p r i n c i p a l s i t e ( s ) a t which the chemical i s concentrated. This i n f o r m a t i o n i s g e n e r a l l y not reported, t h e r e f o r e t h i s review w i l l undoubtedly omit reported chemicals that a r e l o c a t e d i n glands and g l a n d u l a r trichomes and improperly i n d i c a t e g l a n d u l a r components that are a c t u a l l y l o c a t e d elsewhere i n the p l a n t . However, i n f o r m a t i o n on the l o c a t i o n o f chemicals w i l l be given wherever p o s s i b l e . This s e c t i o n w i l l review the major types o f chemicals that are present i n glands and g l a n d u l a r trichomes. Immobilizing Chemicals. Some p l a n t s produce a s t i c k y , gummy exudate from g l a n d u l a r trichomes. These exudates e f f e c t i v e l y immobilize s m a l l i n s e c t s . A number of p l a n t s o f the Solanum and N i c o t i a n a genera are p a r t i c u l a r l y adept a t producing s t i c k y l e a f exudates. I n some w i l d potato s p e c i e s , an exudate i s discharged from g l a n d u l a r h a i r s when aphids mechanically rupture the c e l l w a l l s (33). The c l e a r , water s o l u b l e exudate i s s t a b l e i n the absence o f 0 , 9



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but r a p i d l y darkens and forms a p r e c i p i t a t e on the aphids limbs when exposed t o a i r . E v e n t u a l l y the aphid becomes immobilized and d i e s . I n v e s t i g a t o r s found s e v e r a l m o r p h o l o g i c a l l y d i f f e r e n t types of glands; however, only one was an apparent source of the exudate. Once t h i s gland was ruptured, the m a t e r i a l was not r e p l a c e d . The c l e a r m a t e r i a l gave a p o s i t i v e t e s t w i t h the F o l i n - D e n i s phenol reagent. The formation of the dark p r e c i p i t a t e was i n h i b i t e d by the copper c h e l a t i n g agent, sodium d i e t h y l d i t h i o c a r b a m a t e . Polyphenol oxidase enzymes may be i n v o l v e d i n t h i s r e a c t i o n s i n c e copper i s e s s e n t i a l f o r t h e i r r e a c t i v i t y . In other research on Empoasca fabae, the percentage m o r t a l i t y of nymphs, females, and males confined to the glanded species, polyadenium, was 78, 64, and 94 r e s p e c t i v e l y , compared to l e s s than 20% on 2 nonglandular species (34). Trichome exudates were found on the mouthparts of IS. fabae i n 75, 67, and 29% of dead nymphs, females, and males, r e s p e c t i v e l y . Scanning e l e c t r o n microscopy showed that the t i p of the labium was t o t a l l y occluded by the trichome exudate. The s u r v i v i n g leafhoppers had no observable exudate on t h e i r bodies. The viscous exudate, which r a p i d l y darkens and hardens, could be d i s s o l v e d i n 95% e t h a n o l . Aphids, attempting to feed on the tomato, Solanum p e n n e l l i i , are entangled i n a s t i c k y l e a f exudate and soon d i e (35). This exudate could be removed by washing w i t h cotton s a t u r a t e d w i t h 95% e t h a n o l , but the washed leaves r a p i d l y s e c r e t e d a new exudate that a l s o was f a t a l . Trichomes were a d e t e r r e n t to o v i p o s i t i o n by the tobacco w h i t e f l y , Bemisia t a b a c i , on both tomato and tobacco leaves (36). The s t i c k y exudate may p a r t i a l l y account f o r t h i s s i n c e w h i t e f l i e s were found glued to the g l a n d u l a r hairs. Glandular h a i r s a l s o have been i m p l i c a t e d i n the r e s i s t a n c e of c e r t a i n annual Medicago species to the a l f a l f a w e e v i l , Hypera p o s t i c a (37). The annual s p e c i e s , M. d i s c i f o r m i s , and M. s c u t e l l a t a , possess e r e c t g l a n d u l a r h a i r s , and the exudate from these glands acts as a glue to immobilize l a r v a e . The p e r e n n i a l s p e c i e s , M. s a t i v a , which i s s u s c e p t i b l e to the a l f a l f a w e e v i l , possesses only procumbert glands. The exudate from these glands does not prevent l a r v a l movement (38). Stylosanthes hamata and S^. scabra, which are h i g h l y productive and n u t r i t i o u s species of t r o p i c a l pasture legumes, are covered w i t h g l a n d u l a r trichomes. The trichomes secrete a viscous s e c r e t i o n that immediately immobilize l a r v a e of the c a t t l e t i c k , Boophilus microplus (39). T i c k s have a n a t u r a l tendency to climb p l a n t s , and wait f o r a host animal. The s e c r e t i o n has no r e p e l l a n t p r o p e r t i e s , so that t i c k s do not attempt to seek a l t e r n a t i v e p l a n t s . In a d d i t i o n to i m m o b i l i z i n g the l a r v a e , the p l a n t s produce an u n i d e n t i f i e d v o l a t i l e compound(s) that poison the larvae, w i t h i n 24 hours. As w i t h many p l a n t defensive systems, g l a n d u l a r trichomes may a l s o be d e t r i m e n t a l to the p l a n t . I t has been proposed that



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the tobacco i n t r o d u c t i o n 1112 ( T . I . 1112) may be r e s i s t a n t t o some i n s e c t s because i t s l e a v e s , although h a i r y , l a c k g l a n d u l a r trichomes (40). The glandular trichomes that cover the a e r i a l p o r t i o n s of most tobacco p l a n t s are a conspicuous source of odors, as w e l l as a source of the s t i c k y exudate. I t has been proposed that the trichome exudate serves as an a t t r a c t a n t o r o v i p o s i t i o n stimulant f o r tobacco budworm moths and as an a r r e s t a n t f o r a l a t e green peach aphids. The absence of g l a n d u l a r trichomes on the leaves of T.I. 1112 may account f o r i t s p a r t i a l r e s i s t a n c e t o these i n s e c t s . However, T.I. 1112 has glandular trichomes on the calyces which may e x p l a i n the readiness of tobacco budworm moths t o o v i p o s i t i o n on i t s flowers and flower buds. The absence of g l a n d u l a r trichomes a l s o increased Trichogramma p a r a s i t i s m on H e l i o t h i s eggs on T.I. 1112. H e l i o t h i s egg m o r t a l i t y from t h i s p a r a s i t e on other tobacco i s n e g l i g i b l e because the t i n y p a r a s i t i c wasp becomes stuck i n the exudate (41). Toxic and Repellent

Allelochemics

L e v i n has proposed t o c l a s s i f y t o x i c p l a n t chemicals i n v o l v e d i n r e s i s t a n c e i n t o two broad c a t e g o r i e s , those that confer s p e c i f i c r e s i s t a n c e and those that confer general r e s i s t a n c e (42). Compounds e x h i b i t i n g s p e c i f i c r e s i s t a n c e a r e c h a r a c t e r i z e d as extremely t o x i c t o a small group of s p e c i a l i z e d pathogens or h e r b i v o r e s . Each compound i s present only i n a few s p e c i e s , and i s o f t e n t i s s u e s p e c i f i c . They tend t o reach t h e i r highest concentration i n young leaves and f r u i t s and decrease as they mature. Examples would be s i n i g r i n , tomatine, s o l a n i n e , and gossypol. Compounds c l a s s i f i e d as showing general r e s i s t a n c e d e t e r , r e p e l , o r are weakly t o x i c t o most microorganisms and/or h e r b i v o r e s . These compounds are present i n s e v e r a l plant species and sometimes i n f a m i l i e s of d i f f e r e n t orders. They are g e n e r a l l y not t i s s u e s p e c i f i c , and t h e i r concentration increases as the t i s s u e matures. Examples i n c l u d e chlorogenic a c i d , q u e r c e t i n , and tannins. Although a t o x i c p l a n t chemical may not f i t e i t h e r category p e r f e c t l y , those chemicals discussed below that are t i s s u e s p e c i f i c would g e n e r a l l y be considered t o show s p e c i f i c r e s i s t a n c e . I t i s i n t e r e s t i n g t o note that those phytochemicals t h a t are e s p e c i a l l y t o x i c t o one group of i n s e c t s are q u i t e o f t e n e s s e n t i a l d i e t a r y i n g r e d i e n t s or feeding s t i m u l a n t s t o other i n s e c t s that feed p r i m a r i l y on that p l a n t . The phytochemicals that are discussed below may be d i v i d e d i n t o three c l a s s i c a l c a t e g o r i e s : a l k a l o i d s , f l a v o n o i d s , and terpenes. S t r a i g h t chain carbon compounds, such as hydrocarbons, waxes, f a t t y a c i d and a l c o h o l s a l s o occur i n glands. The a l k a l o i d s tend t o react as feeding deterents and as poisons (43). They are probably the major c l a s s found i n any l i s t s of p l a n t t o x i n s (44, 45). Flavonoids are w e l l known a n t i b a c t e r i a l ,



76


a n t i m i c r o b i a l and a n t i v i r a l agents (46-49). Flavonoids a l s o i n h i b i t the growth of H e l i o t h i s zea l a r v a e (50). They may a l s o act as e i t h e r feeding d e t e r r e n t s o r s t i m u l a n t s f o r d i f f e r e n t i n s e c t s (22, 43, 51.* 52, 53). I t was found that v i c i n a l h y d r o x y l a t i o n was necessary, but not s u f f i c i e n t f o r growth i n h i b i t i o n (50). Flavanones, f l a v o n e s , and f l a v o n o i d g l y c o s i d e s i n h i b i t Na-independent passive t r a n s p o r t of sugars by i n t e s t i n a l e p i t h e l i a l c e l l s (54). The i n h i b i t o r y a c t i o n i s i n f l u e n c e d by the extent and p o s i t i o n of h y d r o x y l a t i o n of the f l a v o n o i d nucleus, the degree of p l a n a r i t y of the molecules, the presence of a carbonyl group, and g l y c o s y l a t i o n . The occurrance of f l a v o n o i d aglycones throughout the p l a n t kingdom has been c a r e f u l l y cataloged (55). Terpenoids are a d i v e r s e group of compounds showing a wide spectrum of b i o l o g i c a l a c t i v i t i e s . Among the most b i o l o g i c a l l y a c t i v e terpenoids are the sesquiterpene l a c t o n e s . Their b i o l o g i c a l a c t i v i t y has been reviewed (56, 57, 58). Sesquiterpene lactones show c y t o t o x i c i t y , mammalian t o x i c i t y , a l l e r g i c contact d e r m a t i t i s , a l l e l o p a t h y , a n t i b i o t i c a c t i v i t y t o b a c t e r i a and f u n g i , s c h i s t o s o m i c i d a l a c t i v i t y , a n t i f e e d a n t a c t i v i t y toward mammals and i n s e c t s , i n s e c t l a r v a l growth i n h i b i t i o n , and deter i n s e c t o v i p o s i t i o n . T h e i r a c t i v i t y can be explained i n many cases by Michael a d d i t i o n r e a c t i o n s between a n u c l e o p h i l e and the e x o c y c l i c a , 6 - u n s a t u r a t e d y-lactone f u n c t i o n . Other types of terpenoids a r e a n t i f e e d a n t s t o the A f r i c a n armyworm (59), and the obscure root w e e v i l (60). General terpenoid a n t i f e e d a n t s from east A f r i c a n t r o p i c a l p l a n t s have been reviewed (61, 62). Terpenes may a c t as feeding s t i m u l a n t s or i n h i b i t o r s depending on c o n c e n t r a t i o n (63)• Terpenoids a l s o e x h i b i t i n s e c t growth r e g u l a t i o n (64), antiecdysone a c t i v i t y (65), and are a c t i v e against a wide range of b a c t e r i a and f u n g i (66-71). A l k a l o i d s and Phenols from Tobacco, Tomato, and Potato. Tobacco, tomato, and potato p l a n t s c o n t a i n a number of t o x i c a l k a l o i d s . Probably the most widely s t u d i e d i s n i c o t i n e . The i n s e c t i c i d a l p r o p e r t i e s of t h i s and other tobacco a l k a l o i d s have been reviewed (72). A study of N i c o t i a n a showed that a l k a l o i d s are secreted by trichomes i n the seven species t e s t e d (73). N i c o t i n e was the major a l k a l o i d i d e n t i f i e d i n the trichome s e c r e t i o n (74). Anabasine and n o r n i c o t i n e were a l s o i d e n t i f i e d i n two species ( 7 5 ) . Other ether s o l u a b l e c o n s t i t u t e n t s have a l s o been i d e n t i f i e d (76). Aphids were k i l l e d by contact w i t h these s e c r e t i o n s . Trichome s e c r e t i o n s from N i c o t i a n a a l s o were t o x i c t o the tobacco hornworm and the two spotted spider mite (77, 78). In a p h y s i o l o g i c a l study of i n s e c t ' s response t o n i c o t i n e , i t was found that the p e n e t r a t i o n r a t e of n i c o t i n e i n t o the i s o l a t e d nerve cord was pH dependent (79)• At the pH of i n s e c t haemolymph the p e n e t r a t i o n of n i c o t i n e i n t o the nerve cord was higher on a u n i t weight b a s i s i n the n i c o t i n e - s u s c e p t i b l e



5.

STIPANOVIC

Plant Trichomes

and

Glands

77

silkworm (Bombyx mori) than i n the n i c o t i n e - r e s i s t a n t hornworm, Manduca s e x t a . This was i n t e r p r e t e d as i n d i c a t i n g a l e s s e f f i c i e n t ion-impermeable b a r r i e r of the silkworm nervous system. The e f f e c t s of the Solanum a l k a l o i d s on the Colorado potato b e e t l e , L e p t i n o t a r s a decemlineata, have been c a r e f u l l y s t u d i e d . Solanine, chaconine, l e p t i n e I , l e p t i n i n e I , l e p t i n i n e I I , demissine, and tomatine were a l l found t o be feeding d e t e r r e n t s (74, 80). N i c o t i n e , even i n q u i t e s m a l l c o n c e n t r a t i o n s , was very t o x i c (74). The Colorado potato b e e t l e was found t o feed more on young tomato p l a n t s which had a low c o n c e n t r a t i o n of tomatine than on mature o r f l o w e r i n g p l a n t s that had a higher c o n c e n t r a t i o n of tomatine (81). Feeding was a l s o i n h i b i t e d (20-80%) when tomatine was i n f i l t r a t e d i n t o tomato l e a f d i s k s a t concentrations between 65 and 165 mg/100 g f r e s h weight. N o r n i c o t i n e , s o l a n i n e , and tomatine were a l l t o x i c t o nymphs o f the two-striped grasshopper, Melanoplus b i v i t t a t u s , which i s a general feeder (82). Trichome s e c r e t i o n s of tomato are a l s o t o x i c t o the green peach aphid (83). An extensive l i s t of p l a n t a l k a l o i d s and other phytochemicals that act as i n s e c t feeding d e t e r r e n t s and r e p e l l e n t s as w e l l as feeding s t i m u l a n t s and a t t r a c t a n t s has been published (45). I n the case o f the tobacco hornworm, M. s e x t a , n o r v a l a t i n e and nonpolar or weakly p o l a r f r a c t i o n s o f tomato leaves s t i m u l a t e f e e d i n g , w h i l e feeding d e t e r r e n t s were present i n water e x t r a c t s of tomato leaves (84). Tomato trichome exudates are t o p i c a l l y t o x i c t o the s p i d e r mite, Tetranychus u r t i c a e (85). The f l a v o n a l g l y c o s i d e , r u t i n , has been i s o l a t e d from the t e t r a c e l l u l a r g l a n d u l a r trichomes of the tomato p l a n t , Lycopersicon esculentum (86). This and other trichome exudates reduce l a r v a l growth o f H e l i o t h i s zea. A morphologically d i f f e r e n t type of g l a n d u l a r trichome on the w i l d tomato, L. hirsutum, contains 2-tridecanone, which i s t o x i c t o 11. zea and M. sexta when a p p l i e d t o p i c a l l y (87)• T o t a l g l y c o a l k a l o i d s i n f o l i a g e o f w i l d potatoes 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 r e s i s t a n c e t o the potato leafhopper (88). Flavonoids and Terpenoids i n Bud Exudate. The occurrence of f l a v o n o i d aglycones i n buds has been reviewed by Wollenweber and D i e t z (55). They note that the f l a v o n o i d aglycones w i t h a low number of hydroxyl groups and/or a high number of methoxyl groups, because of t h e i r l i p o p h i l i c nature, do not accumulate i n the c e l l sap. Thus, these types of compounds are found i n p l a n t s w i t h g l a n d u l a r trichomes, e x c r e t i o n c e l l s , o r c a v i t i e s . A v a r i e t y of p l a n t f a m i l i e s produce bud exudates c o n t a i n i n g widely v a r y i n g f l a v o n o i d s . I t was p r e v i o u s l y mentioned that f l a v o n o i d s have a wide range of b i o l o g i c a l a c t i v i t i e s . However, the b i o l o g i c a l a c t i v i t y o f only a small f r a c t i o n o f the f l a v o n o i d s has been i n v e s t i g a t e d against an Qven smaller f r a c t i o n of p l a n t p e s t s . For t h i s reason, s p e c i f i c compounds w i l l not be l i s t e d , but i t i s c l e a r that many, i f not most, of the f l a v o n o i d s confer some p r o t e c t i o n on t h e i r parent p l a n t s .



78

Table I . F l a v o n o i d Aglycones i n Bud Exudates

CO

cu o

o a

o

CO CD

c o

CO CD

O a o >

a o a cd


cd

Family Salicaeae Betulaceae

a

4 6 9 2 1

b

Populus > Alnus > > B e t u l a > > >8> Ostrya Elaegia* Acanthospermum ^ Aes cuius Prunus ' Rhamnus ' Decry a c

d

a

e

c

f

h

c

#

Rubiaceae Asteraceae Hippo cas t umaceae Rosaceae Rhamnaceae Didieraceae

f R e f . (55) R e f . (110) -*Ref. ( I l l ) R e f . (112) *Ref. (113) R e f . (114) *Ref. (115) b

d

f

a

k

12 14 20 12 1 11 9 4 1

m

m

11

5 1 2

o u

•H O 1

CJ

CO Q)

a

o

tH

cd CJ

o

CJ iH

cd

^3 U 2 1

1

1

n

R e f . (91) ^ e f . (94) ^Ref. (116) *Ref. ( 9 2 j •"•Ref. (117) "Ref. (118) R e f . (119) n

The f l a v o n o i d aglycones r e p o r t e d i n buds of A l n u s , B e t u l a , Ostrya, E l a e g i a , Acanthospermum, Aescuius, Primus, Rhamnus, and Decrya are l i s t e d i n Table 1. The b i o s y n t h e s i s of f l a v o n o i d s i n s u b c e l l u l a r glands has been i n v e s t i g a t e d i n Populus n i g r a ( 8 9 ) , and the f l a v o n o i d s i n the l i p o p h i l i c c o a t i n g i n Populus buds have been thoroughly analyzed ( 9 0 ) . I n a d d i t i o n t o t h i s wide v a r i e t y of f l a v o n o i d s , mixtures of terpenoids have a l s o been reported i n bud exudates. I n B e t u l a n i g r a the bud exudate i s reported t o be mainly u n i d e n t i f i e d terpenoids (91). U n i d e n t i f i e d terpenoids a r e found i n bud exudates from Aescuius sp. ( 9 2 ) , Alnus sp., B e t u l a sp., and Ostrya sp. ( 9 3 ) . Some s p e c i f i c terpenoids have been i d e n t i f i e d . The t r i t e r p e n e s i s o f o u q u i e r o l , dammarenediol-11, and (20S)-dammar-24-ene-3 , 20, 2 6 - t r i o l have been i s o l a t e d from the bud exudate of E l a e g i a u t i l i s ( 9 4 ) , and 6-amyrenone i s reported to be a major c o n s t i t u e n t of the bud exudate from a l d e r trees



5.

STIPANOVIC

Plant Trichomes

and

Glands

79

(95). Several raelampolide type sesquiterpene lactones have been i s o l a t e d from the Tanzanian plant Acanthospermum glabratum (96, 97); however, t h e i r occurence i n the bud exudate i s u n c e r t a i n . Although the c o n s t i t u e n t s o f bud exudates are u s u a l l y a s c r i b e d t o f l a v o n o i d s and terpenes, other c o n s t i t u e n t s may a l s o be present. The flower buds of Alnus pendula produce a viscous m a t e r i a l which i n c l u d e s a wide v a r i e t y of compounds i n c l u d i n g a c i d s (cinnamic, 3 - p h e n y l p r o p i o n i c , and b e n z o i c ) , an e s t e r ( 3 phenylethyl cinnamate), ketones ( t r a n s , t r a n s - 1 , 7 - d i p h e n y l - l , 3 heptadiene-5-one and benzylacetone), an a l c o h o l ( 3 - p h e n y l e t h y l a l c o h o l ) , an aldehyde (cinnamaldehyde), s t i l b e n e s ( p i n o s y l v i n and p i n o s y l v i n raonomethyl e t h e r ) , and phenols (eugenol and c h a v i c o l ) , as w e l l as p a r a f f i n s , f l a v o n o i d s (pinocembrin, p i n o s t r o b i n , a l p i n e t i n , and g a l a n g i n ) , and t r i t e r p e n e s (6 -amyrenone and taraxerone) (98). In A. s i e b o l d i a n a two ketones were a l s o i s o l a t e d (yashabushiketol and d i h y d r o y a s h a b u s h i t o l ) . Farinose Exudates o f the Polypodiaceae and Primulaceae. Members of the Polypodiaceae produce a yellow o r white powdery deposit on the lower surface of t h e i r fronds. These deposits are u s u a l l y r e f e r r e d t o as f a r i n o s e exudates. F a r i n a from species of Pityrogramma, C h e i l a n t h e s , Adiantum, and Notholaena have been c a r e f u l l y s t u d i e d . The f a r i n o s e c o a t i n g of these p l a n t s i s formed by the t e r m i n a l c e l l o f s m a l l h a i r s u s u a l l y found on the lower surface of the f r o n d . Wollenweber (99) has reviewed the morphology and chemistry of these ferns which are prodigious producers o f f a r i n a , r e p r e s e n t i n g 0.9%-5.0% of the dry weight of the fronds. Wollenweber r e p o r t s that f l a v o n o i d s are the major c o n s t i t u e n t s o f the f a r i n a . Chalcones (100-106) dihydrochalcones (102, 103, 107, 108, 109), f l a v o n o l s (102, 106, 108, 120-128), flavones TT02,

108, 121, 123, 125, 128, 12977 flavanonesTT30), and the

c h a l c o n e - l i k e compound, ceroptene (124, 131), have been reported i n the f a r i n a from f e r n s . The f l a v o n o i d p a t t e r n i n the f a r i n a of 220 samples from 14 species of the goldenback and s i l v e r b a c k f e r n s has been reviewed (132). Flavanones w i t h methyl s u b s t i t u e n t s (133) and f l a v o n o l s e s t e r i f i e d a t the 8 p o s i t i o n w i t h b u t y r i c and a c e t i c a c i d (134) have a l s o been i d e n t i f i e d i n f a r i n a . The t r i t e r p e n e s d i p l o p t e r o l , fernene, adiantone, isoadiantone (135, 136), and 6 3 , 22-dihydroxyhopane (136) and v a r i o u s p h y t o s t e r o l s (137-140) have been i s o l a t e d from f e r n . However, the morphological source of these compounds i s not c l e a r . This i s a l s o t r u e f o r the sesquiterpenes (141, 142, 143), the l a c t o n e , calomenanolactone (144), the ecdysone analogues (145, 146), and p-hydroxystyryl-3-D-glucoside (147). However, the novel d i h y d r o s t i l b e n e , 5-hydroxy-3,4 -dimethoxy-6-carbbxylic a c i d b i b e n z y l , i s a f a r i n o s e c o n s t i t u t e n t of Notholaena dealbata and N_. l i m i t a n e a (148)• Glycosides of f l a v o n o l s have a l s o been i s o l a t e d from f a r i n a (121). A group o f hydrocarbons, t e r p e n o i d s , and f a t t y acids have been detected i n the glandular l i p i d s of f


80


D r y o p t e r i s a s s i m i l i s f e r n s by gas chromatography (149). The dihydrochalcone, 2 ^ ' - d i h y d r o x y - 4,4'-dimethoxydihydrochalcone, from Pityrogramma calomelanos has shown marked a n t i f u n g a l p r o p e r t i e s (150)Tbther f l a v o n o i d s from Pityrogramma are reported to be a l l e l o p a t h i c agents. 2 ,6 -Dihydroxy-4 -methoxydihydrochalcone i n h i b i t e d spore germination and gametophyte development by calmelanos at a l l concentrations t e s t e d , but 2,6-dihydroxy4 -methoxychalcone i n h i b i t e d germination at 5 X 10 M and s t i m u l a t e d germination at 5 X 10 M. I z a l p i n i n showed s i m i l a r e f f e c t s , i n h i b i t i n g germination at 5 X 10 M and s t i m u l a t i n g germination at 5 X 10 M. These f l a v o n o i d s appear to act as germination i n h i b i t o r s around the parent p l a n t (151) . Many primroses (Primula) a l s o produce a f a r i n o s e exudate on t h e i r stems and l e a v e s . Eighteen species have been i n v e s t i g a t e d (152) . The major components were found to be f l a v o n e , 5-hydroxy-and 5,8-dihydroxyflavone and the three 2'-hydroxy derivatives. f

f

f

f


f

Sesquiterpene Lactones and Other Glandular Trichome Components from Veronia, Parthenium, H e l i a n t h u s , and Artemesia. Sesquiterpene lactones are major c o n s t i t u e n t s of Veronia, Parthenium, Helianthus and Artemesia. As i n d i c a t e d p r e v i o u s l y , the sesquiterpene lactones as a group are a c t i v e i n a wide range of b i o l o g i c a l systems. Mabry, et a l . found that the sesquiterpene l a c t o n e , g l a u c o l i d e A, found i n the glandular trichomes of some species of Veronia, p r o t e c t s these p l a n t s against some i n s e c t s (153). Leaf d i e t s were prepared w i t h and without g l a u c o l i d e A f o r s i x i n s e c t l a r v a e : 1) the y e l l o w woolybear, D i a c r i s i a v i r g i n i c a ; 2) cabbage looper, T r i c h o p l u s i a n i ; 3) y e l l o w s t r i p e d armyworm, Spodoptera o r n i t h o g a l l i ; 4) saddleback c a t e r p i l l a r , S i b i n e s t i m u l e a ; 5) f a l l armyworm, Spodoptera f r u g i p e r d a ; 6) southern armyworm, S^. e r i d a n i a (57). In a f r e e choice s i t u a t i o n , a l l i n s e c t s p r e f e r r e d the d i e t without the l a c t o n e , and the Veronia species that d i d not c o n t a i n g l a u c o l i d e A. Larvae of 3,5, and 6 were s i g n i f i c a n t l y smaller when fed d i e t s c o n t a i n i n g g l a u c o l i d e A compared w i t h a c o n t r o l d i e t , w h i l e l a r v a e of 1 and 2 were unaffected. Furthermore, the days to pupation increased f o r a l l l a r v a e except 1. Other work has shown that p l a n t s c o n t a i n i n g g l a u c o l i d e A deterred o v i p o s t i o n i n some i n s e c t s (154). Other sesquiterpene lactones have been i s o l a t e d from Veronia species (155, 156, 157) as w e l l as t r i t e r p e n e s (158, 159), long chain alkanes (159), and an i r i d o i d g l u c o s i d e (160). The morphological o r i g i n of these l a t t e r compounds i s u n c e r t a i n . Parthenin i s a major component found i n the trichomes of Parthenium hysterophorus, making up about 8% of the dry weight of the p l a n t (161). I t causes d e r m a t i t i s i n humans and c a t t l e (162, 163) and acts as an a l l e l o c h e m i c (164). Parthenin acted as an a n t i f e e d a n t and was t o x i c o r a l l y at 0.01% t o Dysdereus k o e n i g i ,



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Plant Trichomes

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81

Aedes a e g y p t i , T r i b o l i u m castaneum, P e r i p l a n e t a americana, and Phthormea o p e r c u l e l l a (165)• Two other sesquiterpene l a c t o n e s , c o r o n o p i l i n and t e t r a n e u r i n - A (166), and 34 flavones (19 g l y c o s i d e s and 15 aglycones) have been i s o l a t e d from Parthenium species (167). Sesquiterpene lactones may o f f e r some i n s e c t r e s i s t a n c e i n sunflower. Glandular trichomes o c c u r r i n g on the l e a v e s , p h y l l a n d r i e s , and anthers of Helianthus m a x i m i l i a n i c o n t a i n a sesquiterpene l a c t o n e , maximilin-C. The f i r s t i n s t a r l a r v a e o f the sunflower moth, Homeosoma e l e c t e l l u m , s u f f e r e d a high m o r t a l i t y r a t e when f e d on a wheat germ d i e t c o n t a i n i n g concentrations of 1.0 and 10.0% o f maximilin-C (168, 169). A number of other sequiterpene lactones have a l s o been i s o l a t e d from Helianthus species (170-175). The d i t e r p e n o i d a c i d s , trachyloban-19-oic a c i d and (-)-kaur-16-en-19-oic a c i d , have a l s o been i m p l i c a t e d i n r e s i s t a n c e t o the sunflower moth (176)• However, as w i t h maximilin-C, r e l a t i v e l y l a r g e dosages (0.5-1.0%) were r e q u i r e d t o reduce growth on s y n t h e t i c d i e t s by one-half, as compared t o a c o n t r o l . Other d i t e r p e n o i d s (177, 178, 179), t r i t e r p e n o i d s (180, 181, 182), two a c e t y l i n i c compounds (172, 183), a flavone (175), and v o l a t i l e c o n s t i t u e n t s (184) have a l s o been reported from Helianthus s p e c i e s . A p r e l i m i n a r y report i n d i c a t e s that b r i t t l e brush contains a g l a n d u l a r trichome sesquiterpene that i s a feeding d e t e r r e n t to moth l a r v a e (185). The sesquiterpene l a c t o n e s i n Artemesia species have been reviewed (186). H i s t o c h e m i c a l t e s t s have shown t h a t A. nova has, i n a d d i t i o n t o nonglandular trichomes, g l a n d u l a r trichomes c o v e r i n g 21-35% o f i t s l e a f surface (187). These glands hold a c l e a r f l u i d which contains some of the monoterpenes and a l l of the sesquiterpene lactones present i n the leaves. Components of Glandular Trichomes i n Populus, Prunus, Newcastelia, and S a l v i a . I n Populus d e l t o i d e s , the marginal t e e t h of the f i r s t leaves t o emerge are covered w i t h non-glandular trichomes. I n successive leaves, the t e e t h have glands that s e c r e t e a r e s i n as the lamina u n r o l l s . E x t r a f l o r a l n e c t a r i e s occur proximal t o each g l a n d u l a r t i p . F i e l d observations and a l a b o r a t o r y feeding experiment i n d i c a t e that the r e s i n a c t s as an i n s e c t r e p e l l a n t ( 9 ) . I n V. d e l t o i d e s , i n s e c t f e e d i n g was g r e a t e r on newly expanded leaves i n which the r e s i n had d r i e d than on buds covered w i t h f r e s h l i q u i d r e s i n (188). Larvae o f the cottonwood l e a f b e e t l e , when given leaves of d e l t o i d e s i n which only the margin was r e s i n o u s , f e d normally, pupated, and emerged as normal a d u l t s . Larvae given resin-covered leaves d i d not eat them. The few l a r v a e that pupated f a i l e d t o complete t h e i r l i f e c y c l e . Crude e x t r a c t s o f poplar (Populus) t r e e leaves e x h i b i t e d a n t i b a c t e r i a l and a n t i f u n g a l a c t i v i t y (189); r e s p o n s i b l e agents have not been identified. The l e a f t e e t h i n Prunus are covered by g l a n d u l a r trichomes.



82


A coumarin g l u c o s i d e , tomenin, has been i s o l a t e d from Prunus tomentosa, but i t s morphological o r i g i n i s not i n d i c a t e d (190). F i v e d i f f e r e n t types of terpenoid s e c r e t i n g trichomes have been described i n the Western A u s t r a l i a n shrub Newcastelia v i s c i d a (191)• A r e s i n i s r e l e a s e d beneath the c u t i c l e of the g l a n d u l a r h a i r , which expands and e v e n t u a l l y breaks, r e l e a s i n g the r e s i n . Once terpenoid production has ceased, the gland i s c l o s e d o f f by l e a f c u t i n i z a t i o n of the w a l l s . As the gland matures, a drop of r e s i n forms and runs down onto the a d a x i a l l e a f s u r f a c e . A f t e r r u p t u r e , the glands apparently become f u n c t i o n l e s s but new glands are formed during l e a f expansion, and r e s i n i s continuously produced u n t i l the l e a f i s f u l l y expanded. Terpenes i d e n t i f i e d i n N. v i s c i d a i n c l u d e the t r i t e r p e n o i c a c i d s , o l e a n o l i c and b e t u l i c a c i d s (192), and the t r i c y c l i c d i t e r p e n e , isoprimara-9(11),15-diene-3,19-diol (193). A quick d i p of the a e r i a l p a r t s i n ether has been used t o e x t r a c t the g l a n d u l a r trichome contents of S a l v i a g l u t i n o s a (194). The main component was the t r i t e r p e n o l , a-amyrin. Small amounts of flavones and f l a v o n o l s were a l s o i s o l a t e d . Leaf Exudates from Didymocarpus, L a r r e a , Hymenaea, and B e y e r i a . Didymocarpus p e d i c e l l a t a i s a s m a l l herbaceous p l a n t found i n the western Himalayas. I t produces a r e d d i s h , dusty l e a f exudate from which 7-hydroxy-5,6,8-trimethoxyflavone (195), two chalcones, p e d i c i n , and p e d i c e l l i n , and flavanone, and i s o p e d i c i n , (196) have been i s o l a t e d . Two other chalcones, pashonone and m e t h y l p e d i c i n , have been i s o l a t e d from the leaves of I), p e d i c e l l a t a , and the l a t t e r i s reported to be one of the major components (197). Leaf components are reported to be t o x i c to f i s h (198, 199). D i t e r p e n o i d a c i d s have been i s o l a t e d from the leaves of D. oblonga (200, 201). L a r r e a t r i d e n t a t a and L. d i v a r i c a t a are a r i d and semiarid p l a n t s found i n North and South America. L a r r e a produces a l e a f r e s i n that accounts f o r 10-15% of the dry weight of the leaves. The r e s i n i s composed of about h a l f n o r d i h y d r o q u a i a r e t i c a c i d , which i s one of the most powerful a n t i o x i d a n t s known (202). The other h a l f i s p r i m a r i l y composed of f l a v o n o i d s (202, 203). V o l a t i l e c o n s t i t u e n t s of L a r r e a have been reported (204) and t h e i r a n t i h e r b i v o r e chemistry reviewed (205). The t r o p i c a l legume, Hymenaea c o u r b a r i l , produces a l e a f r e s i n t h a t was t e s t e d as a defense a g a i n s t the g e n e r a l i s t h e r b i v o r e , beet armyworm (Spodoptera exigua) (206). Larvae showed a dose-response i n the decrease of pupal weight and delay i n pupation. In a p a l a t a b i l i t y t e s t , S^. exigua s t r o n g l y p r e f e r r e d untreated to t r e a t e d bean l e a f d i s k s . The primary components i n l e a f r e s i n were found to be the sesquiterpene hydrocarbons, c a r y o p h y l l e n e , a - and $-selinene, and 3-copaene (207). The leaves of Beyeria b r e v i f o l i a , from western A u s t r a l i a , have a hard r e s i n c o a t i n g . D i t e r p e n o l s and d i t e r p e n o i c a c i d s


5.

Plant Trichomes

STIPANOVIC

and

83

Glands


have been i d e n t i f i e d i n t h i s r e s i n (208). Other d i t e r p e n o i d s have been i s o l a t e d from IS. c a l y c i n a (209, 210). Cotton Pigment Glands. P l a n t s belonging t o the genera Gossypium ( c o t t o n ) , C i e n f u e g o s i a , Thespesia, and Kokia c o n t a i n subepidermal pigment glands from which the phenol, gossypol, has been i s o l a t e d (211). S t r u c t u r e e l u c i d a t i o n s t u d i e s , chemical r e a c t i v i t y (212, 213, 214), and b i o s y n t h e s i s (215) o f gossypol have been reviewed. Because gossypol i s present i n raw cottonseed meal, i t s t o x i c i t y , e s p e c i a l l y t o monogastric animals, has been c a r e f u l l y s t u d i e d . The t o x i c o l o g y , p h y s i o l o g i c a l e f f e c t s and metabolism have r e c e n t l y been reviewed (216, 217). The Chinese r e p o r t s that gossypol may a c t as an a n t i f e r t i l i t y agent i n men (218) have renewed i n t e r e s t i n t h i s and r e l a t e d compounds. Gossypol has been i s o l a t e d i n an o p t i c a l l y a c t i v e form from Thespesia populnea ([a ] i +445°* 10°, CHClo) (219) and i n a (+) and (±) form from cottonseed (219, 220, 221). Glands i n the f o l i a r p a r t s of £. hirsutum produce, i n a d d i t i o n t o gossypol, the t e r p e n o i d s , j>-hemigossypolone (222), h e l i o c i d e s H^, (223), H (224), H (225), and H (223). I n a d d i t i o n t o these compounds, barbadense a l s o produces the methyl e t h e r d e r i v a t i v e s , jp- hemigossypolone methyl ether and the h e l i o c i d e s B p B (226), B , and B^ (227). G. r a i m o n d i i produces raimondal (228). The S c h i f f base, g o s s y r u b i l o n e , has been detected i n the glands o f £. hirsutum (226). Anthocyanins (229, 230) and flavone (230) have been reported i n glands (229) and c y a n i d i n - 3 - g l u c o s i d e has been i s o l a t e d from £. barbadense glands (231). Hemigossypol, hemigossypol-6-methyl e t h e r , 6-deoxyhemigossypol (232), gossypol-6-methyl and 6,6 -dimethyl ether (233), desoxyhemigossypol and desoxyhemigossypol-6-methyl ether (234) have been i s o l a t e d from glands i n r o o t s , stems, or seed. Several o f these compounds have e x h i b i t e d a n t i b i o t i c a c t i v i t y . Z a k i , e t a l . found that hemigossypol and desoxyhemigossypol were more a c t i v e than gossypol a g a i n s t the fungus, V e r t i c i l l i u m d a h l i a e , (235). Hemigossypolone was a l s o a c t i v e against V. d a h l i a e (236). Terpenoids were found t o be exuded i n t o the r h i z o s p h e r e by c o t t o n r o o t s (237) and may be r e s p o n s i b l e f o r r e s i s t a n c e t o root r o t (238). Gossypol has been shown t o have a n t i b a c t e r i a l (239), a n t i v i r a l (240, 241, 242) and antitumor (243) a c t i v i t i e s . Apogossypol, which has a lower mammalian t o x i c i t y , r e t a i n s t h i s a n t i v i r a l a c t i v i t y (244). The chemical c o n s t i t u e n t s i n the cotton p l a n t have been e x t e n s i v e l y s t u d i e d . V o l a t i l e o r steam d i s t i l l a b l e compounds present i n cotton buds (245-253) and leaves (254, 255, 256) have been e x t e n s i v e l y cataloged. A number of the surface l i p i d s have been i d e n t i f i e d (257). Two anthocyanins, cyanidin-3-3-glucoside (231, 258) and p e l a r g o n i d i n (259), and the f l a v o n o l s and f l a v o n o l g l y c o s i d e s , q u e r c e t i n , kaempferol, i s o q u e r c i t r i n , q u e r c e t i n - 7 9

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84


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g l y c o s i d e , and q u e r c e t i n - 3 - g l y c o s i d e (260) have a l s o been i s o l a t e d . I s o q u e r c i t r i n , q u e r c i t r i n , and q u e r c e t i n are t o x i c and i n h i b i t growth of the bollworm, H. zea, tobacco budworm, H. v i r e s c e n s , and the pink bollworm, Pectinophora g o s s y p i e l l a , i n l a b o r a t o r y t e s t s on a r t i f i c i a l d i e t s (261). These compounds were found to be more t o x i c to the tobacco budworm than to the bollworm. Some of these compounds, such as cyanidin-3-3g l u c o s i d e and the terpene e s s e n t i a l o i l s , are undoubtedly i n , but not n e c e s s a r i l y confined t o , the pigment glands. Others may be l o c a t e d i n g l a n d u l a r trichomes. V a r i a t i o n s i n the c o n c e n t r a t i o n of gossypol and other c o n s t i t u e n t s , such as tannins and f l a v o n o i d s , have been measured w i t h respect to such v a r i a b l e s as c u l t i v a r (244, 262, 263), p l a n t age (264), and plant part (265). In each study, i n s e c t growth was n e g a t i v e l y c o r r e l a t e d w i t h gossypol or terpenoid aldehyde content. Hanny, et a l . found cabbage looper ( T r i c h o p l u s i a n i ) damage c o r r e l a t i o n s of -0.46, -0.60, and -0.31 f o r flowerbud, t e r m i n a l l e a f , and l e a f t e r p e n o i d s , r e s p e c t i v e l y (262). Yellow c o t t o n anthers were found to have a higher gossypol content than cream-colored anthers. This i s b e l i e v e d to be r e s p o n s i b l e f o r suppressing H e l i o t h i s v i r e s c e n s l a r v a e growth (265). Cook was among the f i r s t to propose that the pigment glands of cotton might act as a r e p e l l a n t to the bollwoim (266). Lukefahr and Houghtaling found that c u l t i v a r s of c o t t o n w i t h a flowerbud gossypol content of 1.7% s i g n i f i c a n t l y reduced the populations of tobacco budworm i n l a r g e , r e p l i c a t e d f i e l d t e s t s (267). I t a l s o was found that t h i s experimental Upland c o t t o n was u t i l i z e d l e s s e f f i c i e n t l y by the bollworm than a standard l i n e c o n t a i n i n g 0.5% gossypol (268). Food consumption by the tobacco budworm l a r v a e decreased w i t h i n c r e a s i n g gossypol content. Seaman, et a l . observed a s t r o n g c o r r e l a t i v e c o e f f i c i e n t between a p l a n t ' s r e s i s t a n c e l e v e l and the c o n c e n t r a t i o n of gossypol and the h e l i o c i d e s (269). This same study r e p o r t s that i n l i n e s d i f f e r i n g g r e a t l y i n r e s i s t a n c e , hemigossypolone and the four h e l i o c i d e s occur i n roughly the same p r o p o r t i o n i n buds, w i t h gossypol and the h e l i o c i d e s each comprising about 44% of the terpenoids. This i s i n c o n t r a s t t o a subsequent study which reported gossypol as the primary terpenoid (270) i n buds. These d i f f e r e n c e s may be accounted f o r by the age of the t i s s u e examined. Seaman a l s o reported that the c o n c e n t r a t i o n of each terpenoid aldehyde i n r e s i s t a n t i n d i v i d u a l p l a n t s i s approximately twice the amount found i n s u s c e p t i b l e p l a n t s (269). The t o x i c i t y of the cotton terpenoid aldehydes to d i f f e r e n t l a r v a e has been reported by s e v e r a l groups (227, 259, 270-275). These r e s u l t s are summarized i n Table 2. Although there i s v a r i a t i o n i n the t e s t r e s u l t s among the d i f f e r e n t l a b o r a t o r i e s , i t i s obvious that gossypol and probably the other terpenoid aldehydes have a wide range of t o x i c i t y to many moth l a r v a e . Waiss, et a l . report that the f i r s t i n s t a r l a r v a e of


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86


H e l i o t h i s zea g e n e r a l l y avoided consuming the pigment glands (276) i n d i c a t i n g t h a t gossypol may act as a feeding d e t e r r e n t . Gossypol apparently acts as a f e e d i n g d e t e r r e n t to Spodoptera l i t t o r a l i s , Egyptian c o t t o n leafworm. When polystyrene l a m e l l a e were painted on one s i d e w i t h sucrose and on the other s i d e w i t h gossypol, the 1% gossypol l a m e l l a e s t r o n g l y suppressed feeding over that of a c o n t r o l (277). The feeding r a t e was n e g a t i v e l y c o r r e l a t e d w i t h the gossypol c o n c e n t r a t i o n . Larvae f e d about h a l f as much on lamellae painted w i t h a l e a f e x t r a c t of a h i g h gossypol c o t t o n as oh l a m e l l a e painted w i t h an e x t r a c t of a glandless cotton. Larvae (90-110 and 170-190 mg) of £. l i t t o r a l i s , r a i s e d on cotton p l a n t s w i t h a mean content of 1.23% gossypol i n dry l e a f powder, weighed l e s s , had delayed pupation, and a lower pupal weight compared to l a r v a e r a i s e d on a c o t t o n having an intermediate gossypol content (278) . In neonates the e f f e c t was even more pronounced. When S. l i t t o r a l i s l a r v a e were o f f e r e d d i e t s c o n t a i n i n g 0.5% gossypol acetate throughout t h e i r l i f e span, l a r v a l m o r t a l i t y was n e a r l y 70% a f t e r the f i r s t 10 days and only 0.3% of the l a r v a e pupated. At a c o n c e n t r a t i o n of 0.25% gossypol a c e t a t e , 44% of the l a r v a e d i e d w i t h i n 10 days and 26% of the l a r v a e pupated (279). Studies on the spiny bollworm, E a r i a s i n s u l a n a , have given s i m i l a r r e s u l t s (273). S u r v i v a l and average weights of l a r v a e r a i s e d on d i e t s c o n t a i n i n g gossypol were lower than the c o n t r o l . The same was t r u e w i t h regard t o percent pupation and a d u l t emergence. Seventy percent of l a r v a e r a i s e d on a cotton c u l t i v a r w i t h a gossypol content of 0.10% i n the b o l l s pupated, w h i l e only 9% of those r a i s e d on a c u l t i v a r w i t h 2.34% gossypol i n the b o l l s pupated. The e f f e c t of gossypol on three consecutive generations of l i t t o r a l i s has been s t u d i e d by El-Sebae, et a l . (280). Larvae of S_* l i t t o r a l i s were t r e a t e d t o p i c a l l y w i t h d i f f e r e n t concentrations of gossypol. A f t e r emergence, the moths were t r e a t e d t o p i c a l l y at the same concentrations of gossypol and p a i r e d . The number of eggs and percent h a t c h a b i l i t y were c a l c u l a t e d . F i r s t i n s t a r l a r v a e were reared on an a r t i f i c i a l d i e t c o n t a i n i n g d i f f e r e n t gossypol c o n c e n t r a t i o n s . The treatments were repeated i n the next generation. At the lowest c o n c e n t r a t i o n of gossypol i n the d i e t (0.25%), the number of eggs l a i d decreased to about 52% of the c o n t r o l i n the f i r s t generation. In the second and t h i r d generations, the number of eggs l a i d decreased to about 10% and 2%, r e s p e c t i v e l y , of the c o n t r o l . H a t c h a b i l i t y dropped i n the f i r s t , second, and t h i r d generations to 50%, 43%, and 19%, r e s p e c t i v e l y , of the c o n t r o l . At a c o n c e n t r a t i o n of 0.50% gossypol i n the d i e t , the e f f e c t was even more dramatic, w i t h the h a t c h a b i l i t y dropping below 1% i n the t h i r d generation. Meisner, et a l . reported i n h i b i t i o n of growth and protease and amylase a c t i v i t y i n S. l i t t o r a l i s l a r v a e a f t e r f e e d i n g on


5.

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high gossypol c u l t i v a r s of cotton (281). El-Sebae, e t a l . a l s o s t u d i e d the midguts of £. l i t t o r a l i s (280). They found that gossypol: 1) i n h i b i t e d protease a c t i v i t y and l i p i d p e r o x i d a t i o n , 2) increased microsomal N-demethylation a c t i v i t y , 3) s t i m u l a t e d m i t o c h o n d r i a l ATPase a c t i v i t y a t low concentrations ( 10 PM), and 4) i n h i b i t e d ATPase a c t i v i t y a t higher c o n c e n t r a t i o n s . The i n h i b i t i o n of protease and amylase a c t i v i t y and l i p i d p e r o x i d a t i o n agree w i t h g o s s y p o l s a b i l i t y t o r e t a r d growth by reducing p r o t e i n b i o s y n t h e s i s . The i n h i b i t i o n of ATPase, which provides energy f o r b i o s y n t h e s i s , i s a l s o compatible w i t h the observed r e s u l t s . The i m p l i c a t i o n s of increased microsomal N-demethylation a c t i v i t y i s discussed below. Larvae of £. l i t t o r a l i s t r e a t e d t o p i c a l l y w i t h gossypol (100 u g/g body weight) 24 hours before being t r e a t e d w i t h v a r i o u s i n s e c t i c i d e s had a higher L D C Q than c o n t r o l i n s e c t s (272). The i n c r e a s e i n L D ^ Q was highest f o r the c h l o r i n a t e d i n s e c t i c i d e , e n d r i n (200%), f o l l o w e d by the organophosphate i n s e c t i c i d e , Cyolane (154%), the phosphorothioate i n s e c t i c i d e leptophos (123%), and the carbamate i n s e c t i c i d e , Zectran (87%). IS. l i t t o r a l i s l a r v a e had a lower m o r t a l i t y r a t e when allowed to feed on leaves t r e a t e d w i t h the i n s e c t i c i d e , phosfolan, from a c o t t o n c u l t i v a r w i t h a high gossypol content as compared t o a c u l t i v a r w i t h l i t t l e o r no gossypol (282). The a b i l i t y o f S». l i t t o r a l i s larvae to rapidly detoxify insecticides after treatment w i t h gossypol, agrees w i t h the r e s u l t s o f El-Sebae (280) that microsomal N-demethylation reaches i t s maximum a c t i v i t y a f t e r 24 hours. An i n c r e a s e i n microsomal oxidases has a l s o been observed i n the l i v e r of r a t s which were f e d gossypol (283). As opposed t o the r e s u l t s i n d i c a t e d above, the e f f e c t of gossypol on the b o l l w e e v i l i s q u i t e d i f f e r e n t . Gossypol i s a f e e d i n g s t i m u l a n t t o the b o l l w e e v i l (260). B o l l weevils feeding on an a r t i f i c i a l d i e t were h e a l t h i e r and had improved egg hatch when the gossypol f r a c t i o n from c o t t o n seed was used as the p r i n c i p l e p r o t e i n source.


f

Insect Resistance t o Secondary P l a n t A l l e l o c h e m i c s The i n t r o d u c t i o n o f s y n t h e t i c p e s t i c i d e s heralded a new e r a i n which a g r i c u l t u r a l production f l o u r i s h e d . However, the use of p e s t i c i d e s introduced unexpected problems. I n the case o f i n s e c t i c i d e s , b e n e f i c i a l as w e l l as harmful i n s e c t s were k i l l e d . Insects r a p i d l y developed r e s i s t a n c e t o the i n s e c t i c i d e s , r e q u i r i n g the i n t r o d u c t i o n of new and more potent chemicals. This same s c e n a r i o has not been observed w i t h p l a n t a l l e l o c h e m i c s . Phytophagous i n s e c t s and p l a n t s have c o e x i s t e d f o r eons. I n g e n e r a l , p l a n t s , through t h e i r a l l e l o c h e m i c s have exacted t h e i r t o l l on i n s e c t s , w h i l e f a l l i n g prey t o these same i n s e c t s . The reasons f o r these d i f f e r e n c e s deserve comment. Companies manufacturing p e s t i c i d e s , i n a d d i t i o n t o c o n s i d e r a t i o n s such as cost and s a f e t y , s e l e c t only those




88

chemicals that k i l l the m a j o r i t y of the t a r g e t organisms w i t h which they come i n contact. Indeed, the a g r i c u l t u r a l producer demands such products. Even f e d e r a l l i c e n s i n g agencies might balk at p e r m i t t i n g the s a l e of a p e s t i c i d e that was only m a r g i n a l l y e f f e c t i v e . Yet t h i s i s the path p l a n t s commonly f o l l o w . Experience has shown that given adequate pressure, n e a r l y every species of i n s e c t i s capable of developing some t o l e r a n c e to a p a r t i c u l a r i n s e c t i c i d e (285). The development of r e s i s t a n c e depends on the presence of r e s i s t a n c e genes and adequate s e l e c t i o n pressure by which these genes are concentrated and i n t e g r a t e d i n t o the genome of the p o p u l a t i o n . I f the genetic p o t e n t i a l f o r r e s i s t a n c e i s present, the r a t e of t h i s development w i l l depend on f a c t o r s such as the frequency of the r e s i s t a n c e genes, t h e i r dominance, the s e l e c t i o n pressure and previous exposure to the i n s e c t i c i d e . Assuming a s u f f i c i e n t s u r v i v a l r a t e , r e s i s t a n c e w i l l develop more r a p i d l y the more intense the s e l e c t i o n pressure (285). With p l a n t a l l e l o c h e m i c s , the s e l e c t i o n pressure i s g e n e r a l l y not h i g h enough to concentrate the r e s i s t a n c e genes i n the genome of the p o p u l a t i o n . The p l a n t a l l e l o c h e m i c s slow i n s e c t growth and extend the time of pupation. The l a r v a e thus become more s u s c e p t i b l e to disease, predators and environmental s t r e s s . However, some i n s e c t s w i t h s u s c e p t i b l e genes do s u r v i v e and t h e i r genes are c o n t i n u a l l y i n c l u d e d i n the p o o l . P l a n t s that produce " s p e c i f i c " t o x i n s may be plagued by i n s e c t s that develop a t o l e r a n c e to these t o x i n s i n much the same way as i n s e c t s develop t o l e r a n c e to s y n t h e t i c i n s e c t i c i d e s . Two examples from t h i s chapter are the tobacco hornworm and the b o l l w e e v i l which have developed a h i g h t o l e r a n c e to n i c o t i n e and gossypol, r e s p e c t i v e l y . Some occurrence i n the d i s t a n t past may have placed s u f f i c i e n t l y high s e l e c t i o n pressure on these i n s e c t s that they developed t o l e r a n c e to these compounds. A l t e r n a t i v e l y , the same e f f e c t could have occurred by a low s e l e c t i o n pressure a p p l i e d over a very long p e r i o d time. Other p l a n t s p r o t e c t themselves by employing "general" t o x i n s . S e l e c t i o n pressure from t h i s type of t o x i n would be even l e s s . Thus p l a n t s have evolved which produce chemicals which are only m a r g i n a l l y t o x i c to i n s e c t s . Production of chemicals that are extremely t o x i c to i n s e c t s would g i v e a p l a n t only a temporary adaptive advantage. Host-Plant

Resistance and the P e s t i c i d e Industry

The recent advances i n i d e n t i f y i n g and u t i l i z i n g a l l e l o c h e m i c s i n v o l v e d i n h o s t - p l a n t r e s i s t a n c e has drawn the a t t e n t i o n of the p e s t i c i d e i n d u s t r y . A p o t e n t i a l problem that may not be recognized, i s the e f f e c t on i n s e c t s i f analogs of p l a n t p r o t e c t i v e chemicals are sprayed on a g r i c u l t u r a l crops. Insects t r e a t e d w i t h such analogs, could r a p i d l y become t o l e r a n t not only to the analog, but a l s o to the n a t u r a l a l l e l o c h e m i c .



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Insects t r e a t e d w i t h such analogs, could r a p i d l y become t o l e r a n t not only t o the analog, but a l s o t o the n a t u r a l a l l e l o c h e m i c . There are examples o f c r o s s - r e s i s t a n c e i n which an i n s e c t t r e a t e d w i t h one chemical was found t o have r e s i s t a n c e t o a chemical w i t h which i t had never been t r e a t e d . A s t r a i n o f house-fly which had developed r e s i s t a n c e t o the s y n t h e t i c i n s e c t i c i d e , DDT, was found to be r e s i s t a n t t o the n a t u r a l p y r e t h r i n i n s e c t i c i d e s (286)• These two i n s e c t i c i d e s are c h e m i c a l l y very d i f f e r e n t , and y e t they may react a t the same s i t e inducing c r o s s - r e s i s t a n c e . In c o t t o n , f o r example, i t has been observed that some i n s e c t s that are not normally cotton pests, become a pest on g l a n d l e s s cottons which do not c o n t a i n gossypol. Such i n s e c t s , which are minor pests because o f t h e i r avoidance o f gossypol, i f sprayed continuously w i t h the proper i n s e c t i c i d e , could develop, through c r o s s - r e s i s t a n c e , a t o l e r a n c e f o r gossypol and appear as a new major pest on t h i s crop. Thus, the p o t e n t i a l f o r developing such r e s i s t a n c e i s already present even w i t h s y n t h e t i c i n s e c t i c i d e s that are q u i t e d i s t i n c t from the p l a n t ' s a l l e l o chemic. The p o t e n t i a l becomes i n f i n i t e l y greater i f the a l l e l o chemic and s y n t h e t i c i n s e c t i c i d e a r e chemically s i m i l a r . Some may b e l i e v e that an i n s e c t cannot develop a t o l e r a n c e f o n a t u r a l i n s e c t i c i d e s . On the c o n t r a r y , the Mexican bean b e e t l e has developed r e s i s t a n c e t o the n a t u r a l r o t e n o i d i n s e c t i c i d e s (287)• There are already s c a t t e r e d r e p o r t s o f H e l i o t h i s developing r e s i s t a n c e t o the p y r e t h r o i d s a f t e r use o f only a few years. With the one exception o f s e l e c t i o n pressure, a l l other p r e r e q u i s i t e s f o r the development o f r e s i s t a n c e are present i n the p l a n t - i n s e c t r e l a t i o n s h i p . Therefore, c a r e f u l s t u d i e s are needed before such chemicals are introduced as a c o n t r o l measure. Acknowledgement s I thank Jan Cornish, T e r r i Mutchler, Susan C h i l e s , and Glenda Ward f o r t h e i r a s s i s t a n c e i n the p r e p a r a t i o n o f t h i s manuscript and Howard W i l l i a m s f o r h e l p f u l d i s c u s s i o n s .

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RECEIVED August 23,1982


Plant Resistance to Insects - American Chemical Society

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