Pest Control with Enhanced Environmental Safety - American

Chapter 21

Naturally Occurring Nematicides David J. Chitwood Nematology Laboratory, Beltsville Agricultural Research Center-West, Building 011A, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, MD 20705

This review of naturally occurring phytochemicals with biological activity against plant-parasitic nematodes focuses on several diverse classes of compounds, including polythienyls, alkaloids, phenolics, polyacetylenes, fatty acids, terpenoids, and others. The nematotoxic mode of action and physiological role of most of these compounds in plants are unknown, although some are synthesized in response to nematode infection. Only a few plant families, primarily the Asteraceae and Fabaceae, have been examined for existence of nematotoxic substances. In a few cases, synthetic analogs of naturally occurring compounds have been synthesized and have possessed stronger biological activity than the naturally occurring ones. Enhanced research and development of phytochemical nematicides and analogs could provide safe, selective compounds for minimizing the multibillion dollar annual losses inflicted by phytoparasitic nematodes in the U.S.

Currently available chemicals for management of phytoparasitic nematodes are not only expensive but can also adversely affect the environment or human health (1-3). Consequently, several nematicides have been deregistered or restricted in use during the past decade, and others could face similar restrictions. Because phytoparasitic nematodes inflict annual agricultural losses of 6 billion dollars in the U.S. and 77 billion dollars in the world (4), better management tools are needed urgently. Because higher plants could be expected to be a rich reservoir of interesting compounds with biological activity against phytoparasitic nematodes, isolation and identification of naturally occurring phytochemicals with biological activity against nematodes would be a logical first step for development of new, environmentally safe nematicides. Indeed, higher plants are being increasingly examined as sources for novel compounds with activity against animal-parasitic This chapter not subject to U.S. copyright Published 1993 American Chemical Society

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Naturally Occurring Nematicides

nematodes (5). The development of agronomic nematicides is more difficult than development of mammalian anthelmintics because the former must either move rapidly within the soil without deactivation or else be systemic in plants (6). This review will focus on reports of compounds from higher plants with biological activity against phytoparasitic nematodes. Although direct toxicity is the most common biological activity of these compounds, several have other or unknown effects. In keeping with the chemical orientation of the symposium, this review will not address studies demonstrating the activity of crude plant extracts against nematodes (7-79), although this research can lead to development of management strategies involving incorporation of plant extracts or residues into soil. Although the author's research involves the effects on nematodes of insect molting or juvenile hormones, compounds which do occur in the plant kingdom, this review will exclude these compounds because these investigations have been endocrinologically centered and have not involved plant-parasitic nematodes (20-22). Polythienyls Marigolds (Tagetes spp., Asteraceae) were among the first plants to be examined for nematicidal compounds because they often suppress populations of soil nematodes. Two such compounds identified (Figure 1) were a-terthienyl (I) and 5-(3-buten-l-ynyl)-2,2-bithienyl (II), with the former active against the stem and bulb nematode (Ditylenchus dipsaci) at 5 iig/ml, the wheat seed gall nematode (Anguina tritici) at 0.5 ng/ml, and the potato cyst nematode (Globodera rostochiensis) at 0.1-0.2 pg/ml (25,24). In a survey of 110 different Asteraceae, over 40 species suppressed greenhouse populations of the lesion nematode Pratylenchus penetrans, and thienyls occurred in at least 15 of these species. Two reviews (25, 26) contain excellent summaries of the effects of marigolds on populations of nematodes in soils, the weak nematicidal activity of the two polythienyls or synthetic analogs when incorporated into soil, and the mode of action of the compounds, which involves generation of singlet oxygen by light, peroxidase, or other activators. Interestingly, a simple analog (tetrachlorothiophene) was once a registered nematicide in the U.S. but is now obsolete (6). ,

Alkaloids Several naturally occurring alkaloids (Figure 2) are toxic or otherwise inhibitory to phytoparasitic nematodes. For example, physostigmine (III), an alkaloid from the Calabar bean, Physostigma venenosum (Fabaceae), immobilized D.

I

II

Figure 1. Polythienyls biologically active against nematodes.

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PEST CONTROL WITH ENHANCED ENVIRONMENTAL SAFETY

XII Figure 2. Alkaloids biologically active against nematodes.

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dipsaci at 1 mg/ml (27) but was not toxic, as nematodes regained motility and became infective after transfer to water. Pretreatment of pea seedlings with 30 Hg/ml of physostigmine sulfate protected them against subsequent infection. Another bean alkaloid, monocrotaline (TV) (from the showy crotalaria, Crotalaria spectabilis) inhibited movement of juveniles of the root-knot nematode Meloidogyne incognita at 10 ng/ml (28). Resistance to M. incognita, however, was not correlated with the monocrotaline content of various species of Crotalaria or Cynoglossum. Three other alkaloids— AT-methylcytisine (V), anagyrine (VI), and sophocarpine (VII)—were discovered in another member of the Fabaceae, Sophora flavescens (29, 30). When applied to cotton balls in petri dish cultures of the pinewood nematode (Bursaphelenchus xylophilus) feeding upon the fungus Botrytis cinerea, the alkaloids inhibited reproduction at 3-6 \ig. Three tetracyclic alkaloids—chelerythrine (VIII), sanguinarine (IX), and the previously unknown bocconine (X)—were identified in a poppy, Bocconia cordata (31, 32). Each was active at 50-100 jig/ml against the free-living nematodes Rhabditis and Panagrolaimus. The Solanaceous steroidal glycoalkaloid a-tomatine (XI) was also toxic to the free-living nematode Panagrellus redivivus; the E D expectedly varied with pH and was as low as 50 jig/ml (33). A similar pH-dependent response occurred with another Solanaceous alkaloid, a-chaconine (XII); the most effective E D was 85 \ig/m\ (34). A nonprotonated nitrogen atom was required for maximal activity of either compound. 5 0

5 0

Acetylenes Nematotoxic polyacetylenes (Figure 3) have been isolated from many members of the Asteraceae. The first of these was tridec- l-en-3,5,7,9,11-pentayne (XIII), isolated from Helenium sp. and active against Pratylenchus penetrans (25, 35). Subsequently, 3-cis, 11-trans- and 3-rran^,ll-^ra^-trideca-1,3,1 l-triene-5,7,9triyne (XIV,XV) were obtained from flowers of safflower (Carthamus tinctorius) and were nematicidal against the rice white tip nematode (Aphelenchoides besseyi) at 1.0 \ig/m\ (36, 37). Two acetylenes, tridec-l-en-3,5,7,9,11-pentayne (XIII) and 9,10-epoxyheptadec-16-en-4,6-diyn-8-ol (XVI), were identified from roots of a thistle (Cirsium japonicum) and completely inhibited reproduction of B. xylophilus in the cotton ball bioassay at 16 or 250 \ig, respectively (38). In the same bioassay, l-phenylhepta-l,3,5-triyne (XVII) and 2-phenyl-5-(rpropynyl)-thiophene (XVIII) from tickseed (Coreopsis lanceolata) and cw-dehydromatricaria ester (XIX) from goldenrod [Solidago canadensis (= S. altissima)] completely inhibited nematode reproduction at 110 jig/ball (38). Roots of a daisy (Erigeron philadelphicus) contained methyl 2-trans,Scw-deca-2,8-diene-4,6-diynoate (2-fraflj,8-ds-matricaria ester, XX) and methyl 2-cw,8-cw-deca-2,8-diene-4,6-diynoate (2-cw,8-cw-matricaria ester, XXI). The L D of each against the lesion nematode Pratylenchus coffeae was 3.0 jig/ml (39). Four additional naturally occurring polyacetylenes (cis- and transdehydromatricaria and cis- and fra>w-lachnophyllum esters, (XIX, XXH-XXIV) and four synthetic analogs (lachnophyllic acid, dehydromatricarianol, dehydromatricarianyl acetate, and lachnophyllol XXV-XXVIII) were also active. In an investigation of nematotoxicity against P. coffeae of 28 synthetic analogs, 5 0

304


OH

Figure 3. Acetylenes biologically active against nematodes.

XXIX

OH

o

in

w

HA

306


none with greater than one triple bond, several were active at concentrations below 1.0 pg/ml (40). A triple bond-conjugated ketone, aryl, or ester group resulted in maximal activity. Finally, among non-Asteraceae, heptadeca-l,9-diene-4,6-diyne-3,8-diol (XXIX) from roots of Angelica pubescens (Apiaceae) had nematicidal activity against Aphelenchoides besseyi (41). Fatty Acids and Other Lipids Several lipids (Figure 4) are toxic to nematodes. At 1 mg/ml most of 41 fatty acids or their salts evaluated were toxic against Panagrellus redivivus, as were most of the 13 tested against the tobacco cyst nematode Globodera tabacum (42). Butyric acid (XXX) was identified in decomposing rye (Secale cereale) and timothy (Phleum pratense) and was toxic at 880 pg/ml to M. incognita and P. penetrans but not to the free-living nematodes Rhabditis, Cephalobus, and Plectus (43). Variation of activity with pH indicated that the undissociated acid was nematicidal. Extracts of Iris japonica (Iridaceae) roots were toxic to A. besseyi; purification by HPLC indicated that myristic, palmitic, and linoleic acids (XXXI-XXXIII) were nematicidal components (41). 2-Undecylenic acid was the most active ( L D < 10 pg/ml) of the synthetic fatty acids tested. Di-n-butyl succinate (XXXIV) created artifactually during isolation and identification of nematicidal substances from peanut (Arachis hypogaea, Fabaceae) induced 90% mortality against Pratylenchus coffeae at 100 iig/ml (44). Eleven of 17 additional, synthetic dialkyl succinates were nematicidal. 50

Terpenoids Several investigators have described nematotoxicity of various terpenoids (Figure 5). In a comparison of 20 non traditional chemicals applied as root dips or soil drenches to tomato plants for control of the root-knot nematode Meloidogyne javanica, citral (XXXV) and geraniol (XXXVI) inhibited nematode reproduction by 52% and 86%, respectively, when applied as 100 pg/ml soil drenches (45). Similarly, when limonene (XXXVII), a component of citrus oil and an inhibitor of insect neurotransmission, was applied as a soil drench at 100 jig/ml, population development of the sugarbeet cyst nematode (Heterodera schachtii) was 3% of that of controls (46). Steam-distilled essential oils of several Labiatae and Myrtaceae were toxic to four species of plant-parasitic nematodes, as were five synthetic terpenoids identified in the extracts—geraniol (XXXVI), linalool (XXXVIII), eugenol (XXXIX), menthol (XL), and 1,8-cineole (XLI) (47,48). A foliar spray of eugenol decreased galling of okra (Abelmoschus esculentus) induced by M. incognita (18) Phenolics There has been substantial investigation of the role of elevated preinfectional levels of plant phenolics (Figure 6) in resistance to nematodes (49, 50).

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O

O XXXIV Figure 4. Fatty acids and other lipids biologically active against nematodes.

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Unfortunately, few of these compounds have been isolated from plant roots and examined for nematotoxicity. Pyrocatechol (XLII), isolated from weeping lovegrass (Eragrostis curvula, Gramineae), was toxic to root-knot nematode juveniles (51). As a 400 jig/ml soil drench, the common plant phenolic quercetin (XLIII) inhibited reproduction of M. javanica (45). Postinfectional Compounds Numerous compounds are synthesized by plants after nematode attack; a large body of work has accumulated on the role of these compounds (Figure 7) in resistance to nematodes (25, 26, 49, 50, 52-57). Although lack of space pre cludes a discussion of the function of postinfectionally synthesized compounds, several of these investigations are relevant to the scope of this article. For example, coumestrol (XLIV) was produced by lima beans in response to infection by Pratylenchus scribneri and inhibited the motility of P. scribneri at 5.0 jig/ml (58). Similarly, resistance toM. incognita in cotton (Gossypium hirsutum, Malvaceae) was associated with biosynthesis of terpenoid aldehydes; a crude terpenoid aldehyde extract from cotton inhibited movement of M. incognita at 50 u.g/ml, as did gossypol (XLV) at 125 iig/ml (59, 60). In soybean roots, glyceollin (XLVI) accumulated during incompatibility to root-knot nematodes. At 15 iig/ml, the compound strongly inhibited movement of M. incognita in vitro; nematodes recovered upon removal from glyceollin solutions (61, 62). In potato tubers, levels of rishitin (XLVII) synthesized in response to infection by the potato rot nematode (Ditylenchus destructor) were correlated with resistance to nematodes, and the compound inhibited movement of Ditylenchus dipsaci at 100 \ig/m\ (63). Other Compounds Many additional compounds (Figure 8) possess antagonism towards plantparasitic nematodes. The inhibition of hatching of eggs of Globodera rostochiensis by mustard seedlings was one of the first investigations of chemically mediated plant-nematode interactions. Allyl isothiocyanate (XLVIII), a constituent of seeds of black mustard (Brassica nigra, Cruciferae), inhibited hatching at 50 jig/ml and significantly improved potato yield when incorporated into field soils (64). Several isothiocyanates and related compounds have been evaluated as preplant soil fumigants, including sodium methyldithiocarbamate, a commercially utilized compound which degrades in soil to form methyl isothiocyanate (2). Resistance of garden asparagus (Asparagus officinalis, Liliaceae) to the stubby-root nematode (Paratrichodorus christiei) is associated with a preformed chemical substance in roots and root exudates; the compound was characterized as a glycoside with a low molecular weight aglycone (65). At concentrations of 100 p.g/ml, the purified compound paralyzed four species of plant-parasitic nematodes, and root drenches or foliar sprays of tomato plants reduced populations of M. incognita. Unfortunately, the compound was not identified.

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XXXV

XXXVI OH 0CH

o

OH

xxxvni

XXXVII

xxxix

OH

XL

XLI

Figure 5. Terpenoids biologically active against nematodes.

OH OH

H

0

^

^

HO XLH

.0.

O XLHI

Figure 6. Phenolics biologically active against nematodes.

XLIV XLV

HO

HO

XLVI

XLVII

Figure 7. Postinfectional compounds biologically active against nematodes.

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Much later, asparagusic acid (XLIX) was isolated from 30 kg of asparagus roots at a concentration of 35 pg/ml. It inhibited hatching of the soybean cyst nematode (Heterodera glycines) and G. rostochiensis at 50 p.g/ml, even in the presence of hatching stimulants. The same concentration resulted in 80-99% mortality in Meloidogyne hapla, Pratylenchus penetrans, and the pin nematode Paratylenchus curvitatus (66). Another species of asparagus, A. adescendens, contained several glycosides, e.g., asparanin B (L), which inhibited motility of M. javanica at 200 ng/ml (67). The nematicidal properties of the neem tree (Azadirachta indica, Meliaceae) have been reviewed (68). Although various plant tissues or crude extracts are nematicidal, the specific nematotoxic compounds are unknown. One neem component, azadirachtin (LI), is an insect antifeedant and growth and molt inhibitor (for references, see 69). Because it inhibits microfilarial release in the animal-parasitic nematode Brugia pahangi at 10 pg/ml (70), azadirachtin is likely one of the many neem components active against plantparasitic nematodes. Other phytochemicals with nematicidal activity include 2,3-dihydro-2-hydroxy-3-methylene-6-methylbenzofuran (LII) from Helenium sp. (Asteraceae) (71) and alantolactone (LIII) from elecampane (Inula helenium, Asteraceae) (72). Hannoa undulata (Simarubaceae) seeds contained three polycyclic lactones: chaparrinone (LIV), klaineanone (LV), and glaucarubolone (LVI). A 1.0-jig/ml mixture of these compounds inhibited penetration of tomato roots by M. javanica (73). Roots of Daphne odora (Thymelaeaceae) contained odoracin (LVII) and odoratrin (LVIII), which induced 100% mortality in Aphelenchoides besseyi at

Pest Control with Enhanced Environmental Safety - American

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