Conference Proceedings
MANAGEMENT OF SOYBEAN CYST NEMATODE POPULATIONS:
CURRENT STRATEGIES AND FUTURE ALTERNATIVES
Gregory L. Tylka
Plant Nematologist
Associate Professor, Department of Plant Pathology
Iowa State University
{Paper presented at the 24th Soybean Seed Research Conference,
Chicago, Illinois, December 6, 1994}
Soybean cyst nematode, Heterodera glycines Ichinohe, is a major factor limiting soybean yields in the United States. First discovered in the United States in 1954 (31), the nematode has since spread to 26 states (23). Soybean cyst nematode has been estimated to cause millions of dollars in damage each year and consistently has been identified as the most destructive pathogen of soybeans in the United States (6, 27). This nematode is a major problem because of its rapid and large increases in population densities, its ability to survive in soil for years in the absence of a host, and its ability to reduce soybean yields at relatively low densities.
Current Management Strategies
For all practical purposes, three options currently exist for management of soybean cyst nematode populations: nematicides, nonhost crops, and resistant soybean varieties. The effectiveness of these existing options can vary considerably, and the use of each has limitations.
Nematicides:
Use of nematicides was once a cost effective option for management of soybean cyst nematode. However, most effective and relatively inexpensive nematicides have been removed from the market due to environmental and human health concerns. Nematicides currently available for management of soybean cyst nematode include aldicarb, carbofuran, 1,3 dichloropropene, and isothiocyanate-generating compounds (3). Management of soybean cyst nematode with nematicides is currently unpopular or uneconomical because of human and environmental toxicity, the high cost of the available compounds, the relatively low per acre dollar value of soybean, and the fact that nematicides usually do not result in season-long control. However, use of nematicides is presented as a management option to growers in Iowa (29), along with the suggestion to first evaluate use of such compounds on a limited scale to determine whether an economic benefit is likely.
Nonhost crops:
Soybean cyst nematode is an obligate parasite; it must feed on living host roots to mature and multiply and cannot reproduce on nonhost crops. Population densities will decline in soils during any season that nonhost crops are grown (7, 14, 26), but the magnitude of decline throughout a single growing season may range from 5 to 50 percent or more and may vary among geographical locations. Population densities generally decrease similarly regardless of the nonhost crop species grown (7, J. Behm and G. Tylka, unpublished). Prolonged use of nonhost crops will not eliminate the nematode from the soil because some eggs are capable of surviving for years in the absence of a host crop (9). Nevertheless, use of nonhost crops is the most effective means to decrease population densities of soybean cyst nematode in infested soils.
The use of nonhost crops for soybean cyst nematode management is limited by economical constraints of the agricultural production systems in a particular region. Soybean producers are unwilling to grow nonhost crops for the sole purpose of nematode management; the nonhost crop must have some marketable value. For example, alfalfa, oat, wheat, and many other crops can be grown in Iowa, but corn is the only economically viable nonhost crop for growers in most of the state. Similar situations exist throughout much of Illinois, Indiana, Minnesota, and Missouri, resulting in soybean cyst nematode infested fields being cropped to corn or soybeans in alternating years. Unfortunately, multiple successive years of nonhost crops are often needed to reduce soybean cyst nematode densities to levels whereby soybeans may be profitably grown again.
Resistant soybean varieties:
Resistant soybean varieties are now widely available in all maturity groups grown in the United States and are very effective at maintaining acceptable soybean yields while suppressing reproduction of the nematode. However, use of resistant soybean varieties will never be the sole solution for managing soybean cyst nematode because of the potential for adaptation of the nematode populations to the race specific resistance.
Currently, there are two main genetic sources for soybean cyst nematode resistance genes in commercial soybean varieties, namely PI 88788 and Peking. A few commercial varieties with resistance genes from PI 90763, PI 209332, and, most recently, PI 437654 also are available. All of these sources of resistance, with the possible exception of PI 437654, allow reproduction by a limited number of individuals in most natural soybean cyst nematode populations. The reproduction of even a few individuals on a resistant soybean variety creates the potential for selection and eventual increase of that nematode subpopulation (16, 18, 32).
The PI 437654 source of resistance appears to be much more durable and effective than the other aforementioned sources of resistance (2). Resistance genes from this plant introduction line have been incorporated into the public variety 'Hartwig' (1), and PI 437654 and 'Hartwig' are currently used as sources of resistance genes in many public and private breeding programs. Initial indications were that PI 437654 was a source of complete resistance to numerous soybean cyst nematode races (2). However, adult nematode females have been observed on the roots of PI 437654 infected by some natural soybean cyst nematode populations (T. Niblack, R. Riggs, R. Ruff, personal communications). To date, females on roots of PI 437654 have been sterile or have produced few eggs which usually were nonviable.
It is risky to rely on the use of PI 437654, alone or in combination with any other source of resistance, as the only strategy for soybean cyst nematode management because of the potential for selection of races of soybean cyst nematode with increased parasitism on resistant soybean varieties and the limited availability of effective, alternative tactics for management of the nematode. Instead, Iowa State University recommends growing nonhost crops, sometimes for several successive years, in conjunction with alternating use of resistant soybean varieties with different sources of resistance, to discourage the selection of new nematode races, for management of soybean cyst nematode (29).
Future Management Alternatives
Clearly, existing options for management of soybean cyst nematode are limited, and a greater selection and diversity of strategies is needed. Several novel tactics for management of soybean cyst nematode are currently being studied and developed for use in the United States. Some of these strategies are variations of tactics used for management of other pathogens and pests, and some are completely innovative disease management tactics. Numerous unique management options may be available for incorporation into soybean cyst nematode management programs in the future. A brief description of four such novel strategies follows.
Engineered resistant soybean varieties:
As described earlier, although resistant soybean varieties are effective at maintaining soybean yield and suppressing reproduction of soybean cyst nematode, there is the potential for selection of races of soybean cyst nematode with increased ability to reproduce on resistant soybean genotypes when natural resistance is used as the sole management tactic (16, 18, 32). Most soybean cyst nematode populations contain sufficient genetic variability that a few individuals are capable of feeding and maturing on currently available resistant soybean varieties.
In 1992, researchers at North Carolina State University identified a root-specific gene that was also expressed in developing root-knot nematode (Meloidogyne spp.) feeding sites (24). Subsequently, a promoter sequence of the gene that was expressed only in the developing nematode feeding sites, presumably in response to nematode feeding, was identified. A reporter gene was fused to the promoter sequence, and the reporter gene product was detected in transgenic tobacco plants only in the developing nematode feeding site (24). More recently, a construct has been developed containing the nematode-feeding-responsive promotor fused to a gene encoding the enzyme Barnase, an RNA-degrading enzyme, resulting in death of the plant cells in which the construct was expressed. Preliminary experiments indicate that root-knot nematode juveniles failed to develop to maturity within roots of tobacco transformed with this construct because of failure of the feeding sites to form due to the death of those specific plant cells (C. Opperman and M. Conkling, personal communication).
The feeding site of soybean cyst nematode is somewhat structurally and functionally similar to the feeding site of root-knot nematodes. Consequently, this genetically engineered root-knot nematode resistance, or some modification thereof, eventually may prove effective against soybean cyst nematode as well. Introduction and manipulation of the engineered resistance in many host crop species should be relatively straightforward because of the detailed knowledge of the promoter and functional genes that confer the resistance. Furthermore, the mechanism of this genetically engineered resistance is so fundamental to the plant cell's basic biology that it is extremely unlikely that a resistance-breaking nematode race could ever develop.
Biological control organisms:
Biological control is the use of living organisms to control or manage a pest or pathogen. Many bacteria and fungi can be isolated from soybean cyst nematode cysts and eggs recovered from naturally infested soils. Isolation of an organism from soybean cyst nematode does not mean that the organism is an active, aggressive parasite of the nematode. Organisms isolated from cysts and eggs may be saprophytes or opportunistic parasites of the nematode (4, 19) that would not be useful in decreasing population densities of the nematode in infested soils. However, aggressively parasitic organisms have been isolated from various life stages of soybean cyst nematode.
A fungus isolated in 1986 from soybean cyst nematode recovered from an infested field in Arkansas (11) appears to have potential for use as a biological control agent for the nematode. The fungus, designated Arkansas Fungus 18 or ARF18 because it does not sporulate in culture and consequently has not been identified, penetrates the body wall of females and cysts and readily infects eggs and juveniles contained within (11). ARF18 is very promising as a biological control agent for soybean cyst nematode; it has provided moderate to excellent management of the nematode in preliminary greenhouse and field experiments (12, 13) and is easily cultured on artificial media in vitro (11). Whether ARF18 is developed into an effective management option for soybean cyst nematode in the future depends on whether a technique can be developed to produce large quantities of inexpensive, shelf-stable inoculum in a formulation that will promote colonization and parasitism of soybean cyst nematodes by the fungus in naturally infested soils.
Pheromones:
Soybean cyst nematode reproduction requires the insemination of females by males. Adult males exist free in the soil and are attracted to females on the surface of roots by a sex hormone or pheromone emitted from the females (25). The attractant has been identified as vanillic acid (10), and structurally similar analogs of the pheromone
exist (28).
Application of the pheromone to infested soils may diminish or obliterate concentration gradients of the natural pheromone in the soil that are vital for males to identify and locate females. If attenuation of pheromone gradients is accomplished, location and subsequent insemination of soybean cyst nematode females by males would likely be reduced. Unfertilized soybean cyst nematode females do not produce eggs, so disruption of mate finding could drastically reduce reproduction of the nematode.
In addition to utilizing the pheromone to disrupt mating, researchers are attempting to exploit the hormone to attract males to antagonistic fungi (8). Once in close proximity with the fungal inoculum, males may be readily parasitized by the fungi, decreasing the number of males in the soybean cyst nematode population, and ultimately reducing mating and reproduction of the nematode population. Preliminary investigations of this approach have been moderately successful (8).
Hatching stimuli:
In 1982, Japanese researchers reported extracting from the roots of kidney bean a complex compound, designated glycinoeclepin A, that stimulated hatching of soybean cyst nematode eggs at extremely low concentrations (17). Compounds which stimulate hatching may be useful in reducing population densities of soybean cyst nematode by increasing hatching of eggs in infested soils when nonhost crops are planted. Hatched soybean cyst nematode juveniles will perish in natural soils in the absence of host root tissue due to starvation, predation, or parasitism. Unfortunately, only milligram quantities of glycinoeclepin A can be obtained from thousands of kilograms of root tissue; it is impractical to obtain sufficient quantities of the natural product for field-scale use.
There have been several published reports of syntheses of glycinoeclepin A or structurally similar analogs (5, 20, 21, 22, 30), but elaborate procedures and expensive materials were needed to produce milligrams of the compounds. Since 1990, researchers at Iowa State University have been attempting to synthesize glycinoeclepin A, or a biologically active analog of the compound, using relatively inexpensive materials and synthetic reactions that can be readily scaled up to produce quantities large enough for field testing. To date, relatively little success has been achieved in producing compounds that stimulate hatching. However, a class of glycinoeclepin A analogs has been discovered that significantly inhibits soybean cyst nematode egg hatching in vitro at parts per million concentrations (15). Additionally, preliminary results indicate that hatching of eggs is significantly inhibited for weeks in sterilized soils treated with the glycinoeclepin A analogs (G. Tylka and G. Kraus, unpublished). Compounds that inhibit hatching may be useful in delaying or reducing early season infection of roots when resistant or susceptible soybeans are grown in infested fields.
Summary
The options that currently exist for management of soybean cyst nematode are very limited. Nonhost crops and resistant soybean varieties currently serve as a foundation for soybean cyst nematode management and will continue to do so in the future. However, a greater diversity of management options is clearly needed to ensure continued successful and profitable soybean production in the United States in the next century. Successful adoption of the novel management options for soybean cyst nematode discussed herein will depend on the cost, ease of use, and effectiveness of the different strategies.
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