Interactions Among Allelochemicals and Insect Resistance in Crop

Jan 8, 1987 - Many crop plants may have the genetic potential to cut production costs, not only of their own allelochemical defense systems against in...
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Chapter 37

Interactions Among Allelochemicals and Insect Resistance in Crop Plants M. R. Berenbaum and J. J . Neal

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Department of Entomology, University of Illinois, Urbana, IL 61801

Many crop plants may have the genetic potential to cut production costs, not only of their own allelochemical defense systems against insect enemies, but also of the synthetic insecticide defense systems humans have devised for plant protection. Common among crop plants are allelochemicals which act as synergists, or chemicals that themselves lack toxicity to insects but can enhance the toxicity of a co-occurring chemical. Most widespread among these synergists are inhibitors of mixed-function oxidases, the membranebound metabolic enzymes responsible for the detoxification of a wide variety of xenobiotics. These inhibitors include methylenedioxyphenyl (MDP) compounds. Myristicin, a common constituent of many umbelliferous crops, is as effective a synergist for carbaryl as is piperonyl butoxide, a commercial synergist of synthetic insecticides. Also ubiquitous are synergists that inhibit glutathione-S-transferases, soluble enzymes involved in a number of xenobiotic transformations. These endogenous allelochemicals can synergize both cooccurring toxicants and exogenous synthetic organic insecticides. Such synergists in leaf tissue can significantly increase the toxicity of an insecticide; carbaryl toxicity is thus greatly influenced by the chemistry of the plant on which i t is applied. While there are possible complications involved in the use of endogenous synergists to potentiate chemical control of insects, there is great potential for using these chemicals to reduce the impact of synthetic insecticides on nontarget organisms and on the environment without compromising insect control. 0097-6156/87/0330-0416$06.00/0 © 1987 American Chemical Society

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

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37.

B E R E N B A U M A N D NE A L

Insect Resistance in Crop

Plants

The term "insect-plant interaction" generally refers to plants of the botanical variety, as opposed to plants of the i n d u s t r i a l variety; however, weeds, wildflowers, and crop plants face many of the same problems that owners of chemical factories do in the process of manufacturing i n s e c t i c i d a l chemicals. One major consideration of i n s e c t i c i d e manufacturers i s to minimize costs of production; higher costs of manufacture are reflected by higher prices and reduced competitive a b i l i t i e s i n the marketplace. Costs are s i m i l a r l y important to plants that synthesize allelochemicals, substances with no known physiological functions which nonetheless possess ecological functions with respect to predators and pathogens of the plant. In the case of plants, "costs" represent biosynthetic costs—energy and material diverted into the formation of defensive chemicals that could otherwise be directed to the production of vegetative and reproductive tissues. That such costs exist and represent a major drain on plant energy and nutrient budges has been long suspected (1), although direct measurements of these costs are infrequent. One case in which these costs have been estimated involves the wild parsnip, Pastinaca sativa, and i t s major insect enemy, the parsnip webworm, Depressaria p a s t i n a c e l l a (2_). Resistance to the parsnip webworm i s largely attributable to the measurable amounts and proportions of furanocoumarins, allelochemicals typical of many plants in the family Umbelliferae. Almost 75% of the variance in s u s c e p t i b i l i t y to the parsnip webworm can be attributed to the r e l a t i v e concentrations of bergapten and sphondin (two furanocoumarins) in the seeds and leaves; the proportion of bergapten in the seeds alone accounts for 36% of the variance. Each of these t r a i t s i s s i g n i f i c a n t l y heritable — that i s , a s i g n i f i c a n t amount of the phenotypic variance i s due to additive genetic factors that can respond to selection. Selection, however i s a two-edged sword; a response to selection i n one t r a i t can, by v i r t u e of linkage or pleiotropy, be correlated with an opposite response in a different t r a i t . A genetic correlation i s the correlation between the additive genetic variance for two t r a i t s measured on a single individual; as such, i t gives an indication of the response of that individual to selection on one t r a i t 03)· Three of the four resistance t r a i t s in parsnip are negatively g e n e t i c a l l y correlated with the number of secondary rays produced by the plant; the secondary rays each bear two seeds and thus r e f l e c t the genetic potential for seed production, the c l a s s i c fitness measure in a biennial plant such as wild parsnip. A negative genetic correlation between a resistance factor and secondary ray number indicates that those individuals that are most resistant to their major insect enemy are also less

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

417

8

ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

competitive when the insect i s absent (2). Reduced fitness could well r e f l e c t the metabolic cost of producing the furanocoumarin resistance factors.

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Synergists That Inhibit Mixed-function Oxidases Insecticide manufacturers have responded to pressures to reduce costs in several ways that have d i r e c t in the plant world. One method i s to use synergists, compounds which may themselves lack t o x i c i t y to insects but which enhance the t o x i c i t y of co-occurring toxicants (4). Most synthetic synergists act by i n t e r f e r i n g with the a b i l i t y of the insect to metabolize the i n s e c t i c i d e ; synergists thus have the additional benefit of restoring potency of i n s e c t i c i d e s to insects resistant because of enhanced metabolic c a p a b i l i t i e s (_5). The most widely used commercial synergists are methylenedioxyphenyl (MDP) compounds such as sesamin; these chemicals interfere with the metabolism of pyrethroid and other i n s e c t i c i d e s by competitive i n h i b i t i o n of microsomal mixed-function oxidases (MFOs), the suite of enzymes responsible for a number of oxidative reactions that convert toxic l i p o p h i l i c materials into excretable hydrophilic materials (J3). The major commercial source of plantproduced pyrethrins, Tanacetum cinerariaefolium, also contains sesamin (7); the plant therefore produces both an i n s e c t i c i d e and a synergist. The widespread occurrence of MDPs and other MFO i n h i b i t o r s in plants grown commercially for food (Table I) raises the p o s s i b i l i t y that resistant c u l t i v a r s may owe their resistance not to v a r i a t i o n in the l e v e l s of toxicant but rather to v a r i a t i o n i n the l e v e l s of synergists. Again, the parsnip plant provides a good example. In at least two species of Lepidoptera (one, Spodoptera eridania, a noctuid generalist, and the other, P a p i l i o polyxenes, a p a p i l i o n i d s p e c i a l i s t pest on parsnip and related umbellifers), furanocoumarins are metabolized by midgut MFOs (27). However, parsnip plants vary considerably i n their content of m y r i s t i c i n , an MDP that i s a potent synergist of furanocoumarins i n the polyphagous H e l i o t h i s zea (Lepidoptera: Noctuidae) (28 (Table II). Inasmuch as only 100 mg/g m y r i s t i c i n can increase the t o x i c i t y of xanthotoxin (a co-occurring furanocoumarin) f i v e f o l d , the 100-fold v a r i a t i o n i n m y r i s t i c i n content i n the leaves of parsnip c u l t i v a r s (Table III) may make a substantial difference i n resistance not only to generalized feeders but also to an adapted pest species such as P. polyxenes.

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

Downloaded by UNIV OF CALIFORNIA SAN DIEGO on December 19, 2016 | http://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch037

37.

B E R E N B A U M A N D NE A L

Insect Resistance in Crop

419

Plants

Table I. Economically Important Plants Containing Methylenedioxyphenyl Compounds

Family

S c i e n t i f i c name

Common name

Ref. 8_

Ericaceae

Vaccinium spp.

blueberry

Myristicaceae

Myristica fragrans

nutmeg

Pedaliaceae

Sesamum indicum

sesame

10

Piperaceae

Piper betel Piper nigrum

betel black pepper

11

Anethum graveolens Anthriscus s y l v e s t r i s Apium graveolens Daucus carota Foeniculum vulgare Levisticum o f f i c i n a l e Pastinaca sativa Petroselinum crispum Pimpinella anisum Oenanthe japonica

dill 9 ,13,14 15 chervil 9 celery 9,16 carrot 9 fennel 9 lovage 17,18 parsnip 9,19 parsley 20 anise 2J_ water celery

Umbelliferae

11

Other MFO synergists i n economically important plants Benzothiazoles ( 2 2 ) : watercress ( 2 3 ) , coconut ( 2 4 ) , tomato ( 2 5 ) , soybean ( 2 6 ) · Benzimidazoles

( 2 2 ) : coffee ( 1 0 ) , tea ( 1 0 ) , cocoa ( 1 0 ) .

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

420

ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

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Table I I . Mortality (%) of F i r s t - i n s t a r Heliothis zea on A r t i f i c i a l Diets (28) Modified with Additives.

Myristicin

(% wet weight)

Xanthotoxin (% wet wt.)

0

0.000

1.1

0.0

0.0

0.0

0.100

0.0

6.7

0.0

6.7

0.250

20.0

13.3

43.3

86.7

0.375

23.3

40.0

38.5

93.3

0.500

16.7

30.0

60.0

86.7

1.500

50.0

100.0

96.7

2.000

86.7

0.57

0.38

LC

5 0

0.01

0.96

0.03

0.10

0.19

(±95% confidence) (0.79-1.17)(0.48-0.67)(0.32-0.46)(0.17-0.20)

Synergistic ratio

1.00

1.85

2.54

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

4.97

37.

BERENBAUM AND NE AL

Insect Resistance in Crop

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Synergists That Inhibit

421

Plants

Glutathione-S-transferases

The mixed-function oxidases are ubiquitous i n plant-feeding insects and are capable of a wide variety of metabolic conversions (4_, 29); they are by no means, however, the only metabolic system involved i n the detoxication of xenobiotics. Glutathione-S^transferases (GST) are soluble enzymes that are known to be involved i n some forms of organophosphate resistance (30, 31). There i s increasing evidence that these enzymes are also involved i n the metabolism of plant allelochemicals. Yu (32) demonstrated that several allelochemicals from plants induce ^e_ novo production of GST and suggested that GST i s involved i n their metabolism. Yu (33) also demonstrated that many ubiquitous plant chemicals can i n h i b i t the a c t i v i t y of GST and are thus p o t e n t i a l synergists. Quercetin (3,3 ,4',5,7pentahydroxyflavone) i s one such i n h i b i t o r (Table IV). Like the MDPs, quercetin and other oxygenated aromatics are widely distributed among crop plants (Table V) and vary within species. Resistant c u l t i v a r s may owe their resistance to v a r i a t i o n i n the levels of these synergists. A preliminary study (35) demonstrated that, i n H e l i o t h i s zea quercetin s i g n i f i c a n t l y increased the t o x i c i t y of s i n i g r i n , a co-occurring constituent of many c r u c i f e r crops. 1

Synergists of Synthetic Organic Insecticides In addition to improving the effect of endogenous toxicants, there i s increasing evidence that naturally occurring synergists i n plants can enhance the t o x i c i t y of synthetic organic i n s e c t i c i d e s . Marcus and Lichtenstein (34) demonstrated that many essential o i l constituents can activate insecticides when applied t o p i c a l l y to Drosophila melanogaster; anisaldehyde and m y r i s t i c i n , both MDPs, increase the t o x i c i t y of parathion. As mentioned previously, m y r i s t i c i n i s comparable to piperonyl butoxide, a commercial synergist, i n increasing the t o x i c i t y of carbaryl to Heliothis zea (35) (Table VI). That m y r i s t i c i n can synergize ingested carbaryl gives r i s e to the i n t r i g u i n g p o s s i b i l i t y that endogenous synergists i n crop plants can be used to enhance the e f f i c a c y of externally applied i n s e c t i c i d e s . If i n t e r n a l synergists can increase the e f f e c t i v e dose of an i n s e c t i c i d e , then lower amounts of i n s e c t i c i d e need be applied to effect equivalent control. Reduced applications are desirable not only i n terms of economic savings i n control costs but also i n terms of ecological impact; reduced applications mean reduced environmental contamination to affect nontarget species. Moreover, decreased environmental residues of i n s e c t i c i d e s may well

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

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ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

Table I I I .

M y r i s t i c i n Content of Seeds of Cultivars of Pastinaca sativa L· (35)

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Cultivar

M y r i s t i c i n (ppm)

Harris Early Model Harris Model Avon Resistor Offenham Tender and True A l l American Gladiator Hollow Crown Improved Fullback Short Thick

3.04 4.96 6.89 10.78 24.37 41.00 63.50 84.02 149.30

Leaf samples for m y r i s t i c i n analysis were weighed into 10-ml screw-top v i a l s . M y r i s t i c i n was extracted i n ca. 4 ml hexane for 24 h. Fifteen micrograms of octadecane was added as an internal standard. The hexane was decanted and the volume reduced to ca. 0.3 ml. M y r i s t i c i n was quantified by GLC-FID (3% OV-17, 2 m χ 4 mm ID, operated isothermally at 125° C) with a Varian 2700 instrument and a HewlettPackard 3390A integrator.

Table IV.

Effect of Plant Substances on Detoxifying Enzymes i n F a l l Armyworm Larvae (34)

Additive (0.27%) to A r t i f i c i a l Diet

None Indole-3-carbinol Quercetin Sinigrin

Glutathione ^-transferase (nmol DCNB conjugated/min/mg protein)

30.3 117.7 18.7 103.7

± 1.0 ±4.9 ± 0.6 ±3.4

a

Newly molted s i x t h - i n s t a r larvae were fed meridic diets containing the compounds for two days prior to enzyme assays·

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

37.

BERENBAUM AND NE AL

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Table V.

Insect Resistance

in Crop

423

Plants

D i s t r i b u t i o n of Quercetin Glycosides i n Edible vs Nonedible Parts of Fruits and Vegetables (mg of aglycone/kg fresh weight) (47).

Quercetin (mg/kg) Species

Other parts of the same plant

Edible part

Small radish

Root

40.1

Leaves

0-30

Radish

Root

0

Leaves

35

Rutabaga

Root

ca.0.1

Leaves

40

Horseradish

Root

0

Leaves

50

Scorzonera

Root