Journal of Nematology 28(1):8-14. 1996. © The Society of Nematologists 1996. Allelopathy in the Management of Plant-Parasitic Nematodes 1 J. M. HALBRENDT 2 Abstract: There are numerous reports of nematicidal chemicals in crude plant homogenates, leach- ates, and decomposing residues. These compounds are usually assumed to be secondary metabolites, which serve as chemical defenses against disease and parasites. When such compounds are released into the rhizosphere, they are known as allelochemicals. The possibility exists to exploit allelochem- icals for nematode control, and there have been many attempts to use this approach either by rotation, intercropping, or green manure treatments. Results have met with mixed success. Proof of allelochemical activity in field situations is difficult to obtain, but it is evident that some rotation crops are significantly better at reducing nematode populations than others. Rotations with non-host plants may simply deny the nematode population an adequate food source for reproduction (passive suppression), whereas allelopathic crops kill nematodes by the production of toxic compounds (ac- tive suppression). Progress toward sustainable agriculture should benefit from studies on allelopathic nematode control. However, grower acceptance of new plant-rotation strategies are based on eco- nomic and logistical considerations as well as efficacy. A potential practical application of allelopathic nematode control that involves using rapeseed as a green manure crop to reduce populations of Xiphinema americanum sensu lato in temperate orchards is presented. Key words: allelopathy, amendment, Brassica, glucosinolate, green manure, isothiocyanate, man- agement, nematode, rapeseed, rotation, thioglucosidase, Xiphinema.

The term allelopathy was coined in 1937 Use of the term allelopathy is somewhat by Molisch to designate plant-plant and controversial. Various disciplines have ex- plant-microorganism biochemical interac- panded the meaning to include plant- tions. In a review of the subject, Rice stated insect and plant-higher animal biochemi- that Molisch intended the term to include cal interactions (32,39), and Lovett and both inhibitory and stimulatory interac- Ryuntyu (20) proposed that chemical com- tions. Rice (30) defined allelopathy as "any munications between plants and between direct or indirect, harmful or beneficial ef- plants and other organisms also be consid- fect by one plant (including microorgan- ered as examples of allelopathic interac- isms) on another through production of tion. Einhellig (11) suggested that allelop- chemical compounds that escape into the athy should be considered an umbrella environment." Many studies of allelopathy term to describe all of these interactions, have focused only on interactions in which including the chemical defenses of plants. one organism is detrimentally affected by Some authors have proposed that the term the association, and only infrequently has "chemical ecology" encompasses all bio- reference been made to possible beneficial chemical interactions between organisms or stimulatory interactions. In the fifth and that use of the term allelopathy should edition of 'The Dictionary of Scientific and be restricted to only plant-plant interac- Technical Terms' by McGraw-Hill (2), al- tions (27). However, through usage, the lelopathy is defined simply as "the harmful broad definition of allelopathy has become effect of one plant or microorganism on widely accepted. another owing to the release of secondary A major principle that separates allelop- metabolic products into the environment." athy from other types of interactions such as competition is that allelopathy is caused by allelochemicals. Allelochemicals are Received for publication 13 September 1995. plant metabolites or their products that are 1 Symposium paper presented at the Annual Meeting of released into the microenvironment. AI- the Society of Nematologists, 5-9 August 1995, Little Rock, AR. Paper number 2029 in the Department of Plant Pathol- lelopathic compounds are released ogy, The Pennsylvania State University. through volatilization, exudation from ~Associate Professor, Department of Plant Pathology, The Pennsylvania State University, P.O. Box 309, Biglerville, PA roots, leaching from plants or residues, 17307-0309. and decomposition of residues (11,27,39). Allelopathy in Nematode Management: Halbrendt 9

Allelopathic interactions have been rec- have since shown that various species and ognized for centuries, with one of the ear- cultivars of marigold can effectively con- liest recorded examples in agriculture dat- trol nematodes on agronomic crops when ing from 285 BC (28,30). However, it was grown in rotation, interplanted with the not until Molisch theorized that biochemi- crop, or used as a soil amendment (3,29). cal processes might explain these observa- Also, several nematicidal compounds have tions that the principles of allelopathy been isolated from marigold, with alpha- were first established. Only during the past terthienyl being one of the most potent 20 years has there been significant (17,37,38). progress in the study of allelopathic chem- Many crops and weeds have been evalu- istry resulting from new techniques which ated for chemical activity against nema- enable the isolation, identification, and todes. Results from these experiments re- quantitative determination of trace natural vealed that numerous species, represent- products in complex matrices such as soil. ing many plant families, produce It was not until such a firm foundation was nematicidal compounds. However, the ex- established that allelopathy became widely perimental design and sophistication of recognized as a scientific discipline (27,31, the techniques used in these studies varied 39). greatly. Only a few studies have provided unequivocal evidence of allelopathy, with ALLELOPATHY IN PLANT NEMATOLOGY most having provided only circumstantial evidence and needing to be substantiated Plant compounds elicit nematode behav- (3,17,28). iors such as attraction or repulsion from roots and, therefore, allelopathic research PROOF OF ALLELOPATHY may be considered a fundamental compo- Many claims of allelopathic activity have nent of nematological research. Because been based on results of bioassays using nematodes are recognized as economically plant homogenates. Merely showing that important pests, many studies have fo- substances extracted from the roots or cused on nematode suppressive crops as leaves of plants cause adverse effects on potential management tools in cropping nematodes in vitro does not provide un- systems. Such studies have shown that equivocal evidence that these compounds some crops "actively" reduce nematode are causing allelopathy under natural con- populations by the production of nemati- ditions. Plant homogenates contain various cidal compounds while others are simply intracellular metabolites, and it seems un- nonhosts (33). The prospect of exploiting likely that the chemicals extracted from a naturally occurring allelochemicals for plant are the same ones normally released nematode control has advantages over the into the soil. Such work should not be dis- current use of toxic chemicals, and there couraged, but many plant tissues contain have been many attempts to utilize this ap- chemicals with potential allelopathic activ- proach either by rotation, intercropping, ity and whether these same compounds or green manure treatments. are released into the rhizosphere in suffi- The most comprehensively studied ex- cient quantities and with enough persis- ample of allelopathy in nematology is that tence to affect nematodes remains a critical of marigold (Tagetes spp.). Marigold has question in many cases of alleged allelopa- been an important medicinal plant since thy (8). the first century, and often medicinal There is no specific protocol (similar to plants have been shown to have allelo- Koch's postulates for proof of disease) to pathic activity (28). Empirical observations establish proof of allelopathy. Neverthe- indicated that many species of marigold less, to establish a cause-and-effect rela- were resistant to a number of nematode tionship, the following events must occur species (35,36). Numerous experiments in sequence: 1) the allelochemical is pro- 10 Journal of Nematology, Volume 28, No. 1, March 1996 duced, 2) the chemical is transported need to develop safer and more ecologi- through the environment from the plant cally sound pest control strategies. At least to the target organism, and 3) the target two potential benefits may be obtained organism is exposed to the chemical in suf- from allelopathy research. One possibility ficient quantity and for sufficient time to is the discovery of plant compounds that have an effect. Many reports of allelo- may lead to new pesticide chemistry having pathic activity have provided evidence for greater efficacy, specificity, and(or) com- the first and third events, but the critical plete decomposition in soil. A second possi- link between production and exposure has bility is the identification of efficacious rota- only infrequently been established (7). tion or green manure crops which could be Soil is a dynamic and complicated phys- used to control nematodes using conven- ical, chemical, and biological medium, and tional or only slightly modified farming organic compounds released into it may be practices, thus reducing or eliminating the altered and transported by biological and need to apply nematicides. This latter pos- physical means. Cheng (7) broadly classi- sibility appears most likely to provide im- fied these processes as retention, transfor- mediate and practical application. mation, and transport. The retention pro- Allelochemicals probably evolved as nat- cesses retard the movement of a chemical, ural defenses against disease, parasites, the transformation processes change the herbivores, or encroachment by other form or structure of the chemical leading plants (15). It has been suggested that to partial alteration or total decomposition, plant breeding programs may have unwit- and the transport processes define how the tingly selected out allelopathic capabilities chemical moves in the soil environment. from crops. Assays to detect allelochemi- Each of these processes is complex, and it cals appear to support this suggestion. is beyond the scope of this paper to discuss Screening tests have shown a wide range of each in detail. However, the nature of the allelopathic activity in domestic crops. allelochemical, the microorganisms Even among different cultivars of the present, the properties of the soil, and the same crop, some varieties may have sub- environmental conditions are key factors stantial allelopathic activity, whereas oth- that can influence these processes (7,8,11, ers apparently have little or none. This sit- 27). uation is analogous to the recognition of The fate of allelochemicals in the envi- genetic resistance in crops to nematodes. ronment may vary considerably in differ- When suitable bioassays have been estab- ent soils and under different conditions, lished, it will be possible to select for and and this may provide an explanation as to breed crops with increased allelopathic ac- why identical (or similar) field experiments tivity (16,18). have often yielded equivocal results when After decades of high-input farming, performed by different workers in differ- agriculture is developing more sustainable ent locations. Detailed understanding of practices based on ecologically sound man- allelochemical behavior in soil requires an agement techniques. These changes in- interdisciplinary approach, and nematolo- volve reduced pesticide use, integrated gists who study allelopathic interactions pest management, greater use of biological would benefit from collaboration with soil controls, and maintenance and improve- scientists, natural product chemists, and ment of the quality of ground water and rhizosphere biologists. soil. Allelopathy appears to be a promising and natural component of sustainable ag- ALLELOPATHY AND riculture since the benefits of crop rotation SUSTAINABLE AGRICULTURE and cover cropping are already well estab- lished with regard to maintaining and im- The increasing interest in allelopathy in proving soil quality. However, consider- recent years has resulted in part from a able development is required for the effi- Allelopathy in Nematode Management: Halbrendt 11 cient utilization of allelopathic crops in present only in sublethal concentrations in commercial agriculture. Rotations will the rhizosphere of the growing plant. In probably need to be developed specifically the field, a single green manure treatment for different regions, soil types, nematode was not as effective as the nematicide ox- problems, and crop production systems. amyl, but two successive rotations pro- Grower acceptance of allelopathic strate- vided acceptable control. gies for controlling nematodes will involve In Pennsylvania, two rotations are possi- practical considerations such as cost, plant- ble within 1 year by planting a winter rape- ing requirements, availability of seed, and seed variety in the autumn and again in efficacy of treatment compared to com- the spring. The autumn-planted crop will mercial nematicides. overwinter and resume growth in the spring. The first crop can be turned under in early spring and a second planting made POTENTIAL OF ALLELOPATHY FOR 1 or 2 weeks later. A winter rapeseed vari- RENOVATION OF ORCHARD LAND ety planted in spring grows vegetatively and does not bolt, thus producing abun- Various Brassica spp. (particularly rape- dant biomass. This second crop can be in- seed and mustard) have been recognized corporated in late summer and the site as beneficial crops for suppression of prepared for replanting with fruit trees in nematodes, soil-borne diseases, and weeds the autumn. in crop rotations (6,13,22,24,25,34). Bio- Economic considerations are important chemical studies have provided a plausible in commercial agriculture, and since green explanation for the allelopathic activity of manure treatments do not provide a crop this crop. The Brassicaceae are character- income and also prevent the growing of ized by the production of glucosinolates. alternative crops, it is reasonable to ques- These are sulfur-containing glycosides tion the acceptance of allelopathy as a which have a common functional group nematode management technique by and a variable side chain (R) that can be growers. In many cropping systems the aliphatic, aromatic, or heteroaromatic. use of a green manure rotation may not be Upon hydrolysis, glucosinolates produce justified. However, it appears that this D-glucose, a sulfate ion, and a range of technique may prove acceptable in tree compounds that can include isothiocy- fruit production because it can be incorpo- anates, thiocyanates, and nitriles. Some of rated into the existing cropping system. these byproducts of decomposition can Old orchard land usually requires exten- be toxic, and bioassays have shown that sive renovation in preparation for a new they are effective against nematodes planting. Major steps in the process in- (5,9,10,12,14,19,21,23,26,34,40). In labo- clude removal of old stumps and roots, ratory experiments several of these com- suppression of plant-parasitic nematodes, pounds were detected in soil that had been adjustments to soil fertility and pH, and amended with crop residue (1,4,5). management of weeds. In addition, old or- Field and greenhouse experiments in chard soil is typically compacted from Pennsylvania have shown that rapeseed years of machinery traffic and loss of or- has potential as a preplant treatment for ganic matter where herbicides were used dagger nematodes (Xiphinema americanum to maintain a vegetation-free zone around Cobb) in replanted orchards when used as trees. One or two years of crop rotation are green manure (18). In these experiments often used to help remediate these prob- the greatest decline in the nematode pop- lems since rotations reduce compaction ulation occurred after incorporation of the and add organic matter. Tilling the rota- crop, and decomposition, presumably, re- tion crop provides a window of opportu- suited in a release of toxic compounds nity to ameliorate fertility and pH prob- which either were not present or were lems by incorporation of nutrients and 12 Journal of Nematology, Volume 28, No. 1, March 1996 lime. Also, rotations offer an excellent op- nomical and compatible with farming portunity to control weed populations with practices. Despite the apparent potential herbicides before the new orchard is estab- of this approach, most known allelopathic lished. The ideal rotation crop would also plants do not fulfill these basic require- suppress plant-parasitic nematodes and ments. Common problems encountered soil-borne diseases by the production of al- include: crops are not adapted to the cli- lelochemicals. mate or soil, seeds are too expensive or not The conventional orchard rotation available, lack of proper equipment to crops in Pennsylvania are typically corn or work the crop, or the benefits of the allelo- soybean, which are both good hosts for Xi- pathic rotation crop are not cost effective phinema americanum. Thus, while these ro- compared to nematicide use. tations may help correct some problems as- The practical application of allelopathy sociated with replanted orchards, they may to control nematodes and(or) other soil- also exacerbate the nematode problem and borne diseases need not necessarily de- thereby increase the need to fumigate or pend upon an understanding of the bio- treat with nematicides. Rapeseed green chemical interaction before it can be im- manure treatments may provide an accept- plemented. By analogy, many crops have able alternative for high-value crops such benefited from the deployment of genetic as tree fruit. Although the green manure resistance to nematodes without an under- crop does not provide an income, the sav- standing of how the resistance works. ings in fumigation costs can offset the dif- However, suitable bioassays need to be de- ference. veloped for use in screening and evaluat- ing the efficacy of allelopathic crops. Such CONCLUSIONS bioassays are essential for breeding and se- lecting more effective allelopathic plants. The study of allelopathy is now widely Allelochemicals in soils are affected by recognized as a scientific discipline, and various biotic and abiotic factors. Inconsis- numerous aspects of allelopathy research tencies reported in the efficacy of allelop- will have practical application in commer- athy to control nematodes may be attrib- cial agriculture to ameliorate pest prob- uted to different soil environments or lems. Nematologists have long recognized miroflora populations (7). For routine ap- the importance of biochemical interactions plication of allelopathic nematode control between plant-parasitic nematodes and in sustainable agriculture, research must their hosts. However, relatively little be focused toward understanding the con- progress has been made to either under- ditions required for consistent results. The standing the details of these interactions or use of allelopathic rotations will probably applying this knowledge toward the devel- need to be adapted to meet the require- opment of practical nematode control ments for different cropping systems and practices. Much of this can be attributed to nematode problems. a lack of appropriate experimental tech- In tree fruit production, a green ma- niques and a paucity of relevant informa- nure treatment may be cost efficient rela- tion regarding natural product chemistry. tive to fumigation or nematicide applica- Greenhouse and microplot studies have tions. In addition to suppression of nema- shown that allelopathic rotation crops or todes, a green manure crop can aid green manure treatments can suppress renovation of the site by reducing soil com- populations of plant-parasitic nematodes, paction, providing organic matter, and but there are few reports of successful ap- helping to control weeds. plication in commercial agriculture (13,18, Rapeseed appears to be a promising 25). In order for allelopathy to be a green manure crop for Xiphinema sp. commercially viable option for nematode nematode control in temperate orchards. control, the technique must be both eco- The crop is commercially available, inex- Allelopathy in Nematode Management: Halbrendt 13 pensive, easily planted, and competitive dahl, C. Anderson, and T. Lanini. 1992. The influ- with weeds. Because rapeseed can be in- ence of Raphanus sativus, Sinapis alba, and Phacelia ta- nacetifolia on California populations of Heterodera corporated into a cropping system with lit- schachtii. Journal of Nematology 24:591. tle modification of existing practices, 14. Grossman, J. 1993. Brassica alternatives to her- growers may be persuaded to try this tech- bicides and soil fumigants. The IPM Practitioner 15: nique. However, acceptance of this tech- 1-10. 15. Herms, D. A., and W.J. Mattson. 1992. The nique as a standard practice will depend dilemma of plants: To grow or defend. 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