Natural Resistance of Plants to Pests - ACS Publications - American

11 Consequences of Modifying Biochemically Mediated Insect Resistance in Lycopersicon Species Downloaded by MONASH UNIV on September 15, 2017 | http://pubs.acs.org Publication Date: January 16, 1986 | doi: 10.1021/bk-1986-0296.ch011

George G. Kennedy Department of Entomology, North Carolina State University, Raleigh, North Carolina 27695-7630

Phenols, alkaloids and methyl ketones have been demonstrated to play important roles in the mediation of insect resistance in plants of the genus Lycopersicon. Although they are considered likely candidates for genetic manipulation, through plant breeding to achieve insect resistance, their use is complex. The actual level of resistance which results from the presence of a given level of a particular compound often depends upon the larger chemical context within which that compound occurs in the plant (i.e. the presence of other biologically active compounds). In addition the introduction of biochemically-based resistance to a particular insect species may have unanticipated and undesirable effects on other, nontarget insect species. Examples of these phenomena are presented and discussed in relation to their implications for utilizing insect resistant tomato cultivars for crop protection. The c u l t i v a t e d tomato, Lycopersicon esculentum M i l l . , i s attacked by a number of very serious arthropod pests which, at present, are c o n t r o l l e d l a r g e l y through the use of insecticides 0,2). In recent years, research has been directed towards the i d e n t i f i c a t i o n and mechanistic understanding of arthropod resistant tomato germplasm for use i n developing tomato c u l t i v a r s resistant to arthropods. As a r e s u l t , s e v e r a l p o t e n t i a l l y useful sources of arthropod resistant germplasm have been Identified (3 and references therein) and an understanding of the complexity of biochemical factors mediating arthropod resistance i n members of the genus Lycopersicon i s beginning to emerge. Several chemicals including the catecholic phenols r u t i n and chlorogenic acid (4^7), the g l y c o a l k a l o i d «-tomatine, (8-10) and the methyl-ketones 2-tridecanone and 2undecanone (11-17) which occur i n tomato f o l i a g e have been

0097-6156/86/0296-O130$06.00/0 © 1986 American Chemical Society

Green and Hedin; Natural Resistance of Plants to Pests ACS Symposium Series; American Chemical Society: Washington, DC, 1986.

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Implicated i n arthropod resistance. This paper w i l l describe the known effects of these compounds on selected Insect pests of tomato and describe some of complexities i n v o l v e d i n manipulating the presence and amounts of these chemicals i n the tomato plant to enhance the l e v e l of insect resistance. Emphasis w i l l be on three Insect species for which the greatest amount of information i s a v a i l a b l e : the tobacco hornworm, Manduca sexta L.; the tomato fruitworm, H e l i o t h i s zea (Boddle), and the Colorado potato beetle Leptinotar8a decemlineata (Say).

Downloaded by MONASH UNIV on September 15, 2017 | http://pubs.acs.org Publication Date: January 16, 1986 | doi: 10.1021/bk-1986-0296.ch011

The Catecholic Phenols Rutin and Chlorogenlc Acid F o l i a r phenol ice of tomato have been investigated extensively as possible factors i n the growth i n h i b i t o r y effects of tomato f o l i a g e on 1L_ zea larvae. The c a t e c h o l i c phenols chlorogenlc acid and r u t i n account for over 60 percent of the t o t a l phenolic content of tomato f o l i a g e (6, 7) and occur i n both the l e a f l a m e l l a and the tips of the type VI glandular trlchomes (Figure 1) which abound on tomato f o l i a g e . Duffey and Isman (5) reported that r u t i n was the major phenolic (80-90Z) i n the tips of type VI glandular trlchomes of esculentum, with chlorogenlc acid and other caf f eic acid conjugates comprising the remainder of the c a t e c h o l i c d e r i v a t i v e s . Is man and Duffey (6) found that c a t e c h o l i c phenols i n tomato f o l i a g e can act i n an a d d i t i v e fashion to i n h i b i t growth of Η*_ zea larvae and that a s e r i a l d i l u t i o n of a t o t a l phenolic extract of tomato f o l i a g e gave r i s e to a dose-response (growth i n h i b i t i o n ) i n larvae s i m i l a r to that produced by pure chlorogenlc acid or rutin. These r e s u l t s and those of E l l i g e r et a l . (4), which are based on the incorporation of phenolles i n a r t i f i c i a l diet, lend support to the hypothesis that tomato phenolice contribute to the a n t i b i o t i c potential of tomato f o l i a g e to zea. However, i n a subsequent study i n which they examined phenolic content of f o l i a g e from d i f f e r e n t tomato c u l t i v a r s and l a r v a l growth on those c u l t i v a r s , Isman and Duffey (_7) found no c o r r e l a t i o n between the phenolic content and l a r v a l growth, despite the fact that the l e v e l s of phenollce i n the f o l i a g e were comparable to those causing s i g n i f i c a n t reductions i n l a r v a l growth on diet. The l e v e l of growth on f o l i a g e (even that containing low l e v e l s of phenollce) i n those experiments was low compared to growth on a r t i f i c i a l diet, suggesting that other factors either Interfered with or over-rode the b i o l o g i c a l a c t i v i t y of the phenollce. The interaction that occurs between phenollce and dietary protein and affecte phenolic t o x i c i t y may explain the lack of c o r r e l a t i o n between phenolic content and l a r v a l growth on tomato f o l i a g e . Duffey (18) hae found that the growth i n h i b i t o r y effecte of r u t i n on H. zea larvae are dependent upon the amount of protein in the diet. The growth i n h i b i t o r y effecte of a given concentration of r u t i n i n diet increaeed with the protein content of the diet over the range of protein l e v e l e teeted (0.6-4.8Z). Further, d i f f e r e n t typee of protein varied i n their a b i l i t y to enhance rutin-induced t o x i c i t y . I f this type of interaction operates i n f o l i a g e as i t doee i n a r t i f i c i a l diet, i t may make the breeding of tomato c u l t i v a r s with elevated l e v e l e of H. zea resistance by s e l e c t i n g for high l e v e l s of f o l i a r phenollce d i f f i c u l t to achieve because



NATURAL RESISTANCE OF PLANTS TO PESTS

Figure 1. Type YI glandular trlchomes of the c u l t i v a t e d tomato L. esculentum.


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s e l e c t i o n would have to be f o r high l e v e l s of f o l i a r protein as w e l l . Confounding the problem of using high phenolic and high leaf protein l e v e l s as a basis for zea resistance In tomato i s the fact that the l e v e l e of both phenollce and proteins i n tomato f o l i a g e are h i g h l y v a r i a b l e both within and between plants of the same and d i f f e r e n t c u l t i v a r s (e.g. protein l e v e l s range from 0.04% to 6.0% f r wt.; 18).


«-Tomatine The g l y c o a l k a l o i d «-tomatine has been implicated i n the resistance of tomato to both H. zea (4, 10, 18) and to L. d e c e m l l n e a t a ( 8 ) . «-Tomatine has been found i n a l l Lycopersicon species surveyed (19, 20). I t i s present i n both tomato f o l i a g e and f r u i t , although the concentration of «-tomatine i n the f r u i t decreases as the f r u i t matures (4, K), 20). For at l e a s t two tomato species which have been examined (L^ esculentum and hirsutum f. glabra turn), f o l i a r «-tomatine has been found associated with the l e a f lamellae but not the t i p s of the type VI trlchomes (5, 21). H e l i o t h i s zea. «-Tomatine has been shown to i n h i b i t growth and development of IL_ zea when added to a r t i f i c i a l diet at concentrations comparable to those found i n tomato f o l i a g e (4, 18). E l l i g e r et a l . (4), f o r example, reported that f o l i a g e of the commercial tomato c u l t i v a r s ^Ace' and ^Campbell 29" contained 0.76 and 0.61 mg «-tomatine per gm fresh weight, r e s p e c t i v e l y , while f o l i a g e of the highly Insect resistant accession PI134417 of the wild tomato species Lycopersicon hirsutum f. glabraturn contained 2.45 mg «-tomatine per gm fresh weight. A l l of these values were i n excèss of the amount of «-tomatine required to reduce l a r v a l growth of H. zea to a l e v e l 50% of that of the controls i n a r t i f i c i a l diet studies (ED Q-0.40 mg «-tomatine/gm f r . wt. diet). However, E l l i g e r et a l . (4) made no attempt to r e l a t e l a r v a l growth on f o l i a g e with the α-tomatine content of the f o l i a g e . In studies by Juvik and Stevens (10), performance of H^ zea larvae on tomato f r u i t s of varying developmental ages from three accessions of Lycopersicon was related to the «-tomatine content of the f r u i t s . The l o g of «-tomatine content was n e g a t i v e l y correlated with l a r v a l growth rate and adult weight but p o s i t i v e l y correlated with time to pupation and m o r t a l i t y (10), suggesting «-tomatine contributes to the resistance of immature tomato f r u i t s to H. zea larvae. The growth of H. zea larvae on tomato f o l i a g e , however, could not be related to the «-tomatine content of the f o l i a g e of d i f f e r e n t c u l t i v a r s (refs. 4 & 5 cited i n 7). A p a r t i a l explanation for this may l i e i n the a b i l i t y of equimolar quantities of phytosterols to a l l e v i a t e the t o x i c i t y of «-tomatine to H. zea (18), e s p e c i a l l y since Campbell and Duffey (9) found the amounts of free s t e r o l or s t e r o l ester and of «-tomatine i n the f o l i a g e of d i f f e r e n t tomato c u l t i v a r s to vary independently. Thus, to the extent that «-tomatine i s i n v o l v e d i n the a n t i b i o s i s of tomato f o l i a g e towards H. zea larvae, current evidence Indicates that the i n t e r a c t i o n between «-tomatine and phytosterols i s at least as important as the absolute quantity of «-tomatine present i n determining the l e v e l of a n t i b i o s i s . 5

n



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Determining the potential value of e x p l o i t i n g elevated l e v e l s of «-tomatine as a basis for enhanced resistance to Η·_ zea i s further complicated by the finding that elevated l e v e l e of «tomatine i n the diet of zea adversely affect Hyposoter exiguae, an ichneumonid parasitoid attacking ]L_ zea (9, 22). However, the toxic effects of «-tomatine on H. exiguae are a l s o a l l e v i a t e d by the presence of equlmolar or supramolar quantities of c e r t a i n phytosterols i n the diet of i t s host, H^ zea (9). Thus, the a v a i l a b l e data indicate that In order to u t i l i z e «-tomatine as a basis for f o l i a r resistance to H. zea, one would have to breed for plants having high l e v e l s of «-tomatine and low l e v e l s of certain phytosterols. If this were achieved, the toxic e f f e c t s of «tomatine might extend beyond the H. zea population and adversely affect the parasitoid H. exiguae, a p o t e n t i a l l y important natural enemy of H. zea (23, it). Leptinotar8a decemlineata. «-Tomatine a l s o acts as a feeding deterrent for decemlineata (25) and the tomatine content of the wild tomato species that are resistant to L. decemlineata i s g e n e r a l l y higher than that of commercial tomato c u l t i v a r s (8). Nonetheless, the evidence that «-tomatine i s responsible for the resistance of any tomato genotypes to decemlineata i s inconclusive, but suggestive. In experiments i n which adult beetles were fed L. esculentum l e a f disks infused with «-tomatine, Slnden et a l . (8) found a p o s i t i v e r e l a t i o n s h i p between Inhibition of feeding and «-tomatine content of the i n f i l t r a t e d leaf disk. Further, they demonstrated that feeding by adult beetles on f o l i a g e of L. esculentum and L. hirsutum f. glabraturn (PI134417) plants of d i f f e r e n t ages or from plants grown under d i f f e r e n t daylength regimes was n e g a t i v e l y correlated with «-tomatine content. The c o r r e l a t i o n was higher for h . esculentum f o l i a g e (r—0.897) than for hirsutum f. glabratum f o l i a g e (r—0.613). However, because their studies revealed s i g n i f i c a n t differences between the two plant species, they concluded that although important, «-tomatine content was less Important i n determining feeding rate on U_ hirsutum f. glabratum than on esculentum. Subsequent research (12, 13, 26, 27) has implicated the methyl ketone 2-tridecanone as an additional factor i n the reels tance of 1^ hirsutum f. glabratum to decemlineata. Unlike the s i t u a t i o n with H. zea, where «-tomatine exerts an a n t i b i o t i c e f f e c t (i.e. chronic t o x i c i t y ) when ingested by the larvae, «-tomatine appears to operate against L. decemlineata adults p r i m a r i l y as a feeding deterrent. None of the a v a i l a b l e data Indicate any interaction between «-tomatine and phytosterols or any other compounds s u f f i c i e n t to obscure the feeding deterrent effects of «-tomatine on potato beetle. However, experiments s p e c i f i c a l l y designed to detect such interactions apparently have not been conducted. If the r o l e of «-tomatine i n resistance to L. decemlineata i s v e r i f i e d , i t should be r e l a t i v e l y easy to s e l e c t for high l e v e l s of f o l i a r «-tomatine i n a tomato breeding program because the genetic v a r i a t i o n i n «-tomatine i s c o n t r o l l e d by the segregation of 2 codominant a l l e l e s at a s i n g l e locus (28). One possible l i m i t a t i o n on the u t i l i t y of «-tomatine-mediated resistance to L. decemlineata i s


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that the «-tomatine content of the f o l i a g e i s not only influenced by day length, but a l s o increases as the plant ages (8). Since L. decemlineata i s often a serious pest of young plants, to be most useful i n combating the potato beetle, high l e v e l s of «-tomatine would have to be present i n the f o l i a g e of young plants.


The Methyl-Ketones

2-Tridecanone and 2-Undecanone

The w i l d tomato L. hirsutum f. glabratum PI134417 i s highly res i s tant to sexta, L. decemlineata and IL_ zea because i t s f o l i a g e i s toxic to the l a r v a e of a l l three species (16, 26, 29). The type VI glandular trlchomes (30) present on the f o l i a g e play an important r o l e i n the acute t o x i c i t y of the f o l i a g e to these insects, although their importance i n the resistance to M. sexta and L. decemlineata i s greater than that to zea (Table I). Table I.

E f f e c t of Removing Type VI Glandular Trichome Tips on Toxicity of L. hirsutum f . glabratum (PI134417) Foliage.

Percent Mortality!/ H. zea 2/ Test l£ j

L. hirsutum f . glabratum Trlchomes Intact Tips Removed L. esculentum

i-

1

. ^ —'

83a 34b 18b

Test I l i '

65a 47b 16c

M. sexta

L. decemlineata

100a 10b 7b

97a 15b 17b

Mortality recorded at 96 hr f o r H. zea and 72 hr for M. sexta and L. decemlineata. Mean separation v e r t i c a l P

Natural Resistance of Plants to Pests - ACS Publications - American

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