Duration: 10/01/2004 to 09/30/2006

Administrative Advisor(s):

NIFA Reps:

Non-Technical Summary

Statement of Issues and Justification

Nematodes are known as one of the most speciose, abundant, and ubiquitous metazoans on earth. The estimated number of nematode species described worldwide is about 27,000 (Hugot et al., 2001). Of these, some 11,000 are terrestrial species and 3,500 are parasites of invertebrates. An estimated 1.5 million nematodes can be extracted from a square meter of soil, just within the surface 10 centimeters. The subgroups of these organisms that form parasitic relationships with plants and their roots are the best known of soil organisms because of the damage they cause to agricultural crops.
One of the most highly publicized plant parasitic nematode in the North Central Region is the soybean cyst nematode, Heterodera glycines Ichinohe. In the United States, soybean cyst nematode caused more estimated total yield reduction in soybean from1999 to 2002 than any other disease. Yield losses have remained relatively stable despite the use of resistant cultivars. Growers profits were increased by $400 million just from growing cultivar Forrest, resistant to soybean cyst nematode races 1 and 3, in infested fields (Bradley and Duffy, 1982). However, resistant germplasm can impose a selection pressure favoring the reproduction of those individuals in the nematode population with specific virulence alleles. This selection pressure can change the virulence characteristics of the nematode population rendering once useful germplasm no longer effective in reduction of soybean cyst nematode population density.

Considerable research has been conducted on management of plant parasitic nematodes using both resistant germplasm and cultural controls. Much of this research studied the effects of economically important plant parasitic nematode in production fields where the soil was tilled, and pesticides used to control weeds and insects. Crop production techniques have changed as attempts to reduce soil erosion lead to reduced or no tillage. Pesticides readily available ten years ago are mostly unavailable after deleterious environmental and health issues were raised. Management of plant parasitic nematodes now must rely on understanding the biology of the nematodes as they interact with microbes and microfauna in soil communities.


Healthy soil is a universal prerequisite for profitable farming on a sustainable basis. Soil quality is generally defined as the capacity of a soil to take in, store and purify water, to hold and recycle nutrients, to support a diverse and robust biotic community, and to suppress pathogens and other pests (sensu Larson and Pierce 1991). Soil quality can and has been degraded through erosion, excessive tillage, compaction, use of broad-spectrum insecticides and soil fumigants, depletion of nutrients and the accumulation of salt and other minerals. These types of disturbances can shift ecological succession of soil communities to that assembling a depauperate soil matrix. Although recovery occurs eventually, abundance and diversity of nematode communities may take years to achieve pre-disturbance levels. The living microbes and microfauna that comprise the soil food web play critical roles in maintaining soil structure, soil fertility, and mediating important ecosystem processes such as nutrient cycling, carbon storage, and maintenance of plant diversity (Dindal 1990).

Soybean cyst nematode has been the major yield limiting plant pathogen in the North Central Region for the last 30 years. Because of its great economic importance much research has been directed at managing this pest. Nematologists in the North Central Region have a history of cooperative research on economically important plant-parasitic nematodes and successful management decisions has been based on cooperative research that measures the diversity of soils, crop rotations, and climatic conditions. Conflicting research results have come out of tillage research indicating the promise of reducing soybean cyst nematode through this practice may be site specific. In some fields use of non-host crops for soybean cyst nematode has not reduced the population density of the nematode in the soil as rapidly as predicted. Plant resistance overall can reduce the population density of the nematode but, in certain fields the benefits of planting a resistant variety are not as obvious. The nematode-plant interaction is not as clean as expected or forecast.


One of the possible explanations of these unexpected results is the change to less persistent and more environmentally friendly pesticides. However, field and other studies suggest Bt cotton and Cry3A potato have no significant effect on nontarget beneficial microinvertebrates, and pose less risk to the environment than conventional spraying with pesticides (Sims 1995, Dogan et al. 1996, Donegan et al. 1996, Yu et al. 1997, Riddick and Barbosa 1998, Riddick et al. 1998).

Another explanation of conflicting results is the possible interactions of other plant parasitic nematodes and diseases which have not been extensively studied. Disease pressure in soybean/corn rotations from root lesion nematodes, Pratylenchus penetrans, P. scribneri, and other species, is increasing in Wisconsin. Reduced use of corn insecticides with nematicidal activity (Furadan, Counter) is probably one factor responsible for the rise in root lesion incidence, but an unexplored possibility is that reducing SCN population densities during the soybean year by planting resistant cultivars has diminished competitive interactions that formerly kept root lesion populations in check. The pathogenicity of Pratylenchus spp. to soybean in greenhouse trials (Ferris & Bernard) and to other crops, alone and in partnership with common soil fungi, warrant research on this pest in soybean systems.

Nematodes and their antagonists in soil have co-evolved for eons in undisturbed soil ecosystems. Equilibrium between nematode population densities and antagonists exists in the undisturbed soil and in soil with monoculture. Nematode-suppressive soils have been detected in a number of locations throughout the world. A nematode-suppressive soil may be caused by biotic or abiotic factors, but the detailed mechanism of development of nematode-suppressive soil remains unclear. Nematode-trapping fungi, for example, are greatly affected by soil type, organic matter, and other soil elements (Gray, 1987). A few studies have shown that culture practices, such as plant and cropping systems, affected activities of antagonists of nematodes (Bourne and Kerry, 2000; Chen and Reese, 1999; Schuster et al., 1998; Steudel et al., 1990; Timper et al., 2001). Studies of the activities of antagonists and nematode-suppressive soil will generate useful information to understand how the impact of changing management system on the nematode communities, to enhance natural biological control through adopting a best management system, and potentially identify antagonists for commercial use as biological control agents.

Related, Current and Previous Work

A review of CRIS projects using plant-parasitic nematodes and community structure revealed 21 active projects. All projects were from outside of the north central region and are focused on different cropping systems. Other projects had minimal focus on nematodes, were focused on entomophilic nematodes, or were concentrating on plant resistance. This proposed project has some nematodes species in common with other projects which should contribute to the usefulness of research findings of all involved.

NE-171 (Northeastern Region Technical Committee): Biologically based IPM systems for management of plant-parasitic nematodes. Objectives 1. Evaluate the effects of rotational crops, organic amendments and host crop genetics on nematode community structure. 2. Characterization of biological control agents for suppression of plant-parasitic nematodes. 3. Comparison and evaluation of IPM system management of plant-parasitic nematodes based on crop rotation, organic amendments, host crop resistance and biological control agents.

Members of the NC 215 project have conducted cooperative research in the regional project as well as projects funded by North Central Soybean Research Program. In conjunction with our annual meetings we have participated for the last 4 years in a workshop at the close of the business meeting. These workshops have been varied from several hours duration to one day in length and have covered topics of interest to the group.

Cyst nematode identification workshop 2000

Dorylaim workshop 2001

Standardization of procedures for extraction of soybean cyst nematode 2002

Identification of Freeliving Nematodes (Secrenentea) 2003

Objectives

1. Determine the impact of management strategies on nematode communities of regionally important nematodes
   
2. Evaluate the effects of specific biological and ecological processes on communities of regionally important nematodes.
   
3. 
   

Methods

Objective 1. Determine the impact of management strategies on nematode communities of regionally important nematodes. Soil-dwelling nematodes will be extracted from the soil in areas where conventional management is practiced and where management practices have been/are changing. Examples of situations examined are fields planted to conventional cultivars compared with fields planted to GMO cultivars, fields in conventional tillage and fields in no-tillage; and fields in conventional management and fields in certified organic production. Major nematode species will be identified and quantified. Comparison of nematode fauna will be made between the different management strategies to evaluate their usefulness. Current management of soybean cyst nematode includes the use of soybean cyst nematode resistant soybean cultivars with rotation to non-host crops, such as alfalfa, corn and wheat (Niblack, 1999; Donald and Niblack, 1996). Other strategies that work in conjunction with use of resistant cultivars are being explored to reduce population density of the nematode more quickly and thus relieve selection pressure of the nematode on the plant resistance. This project will focus on the management strategies that appear to have the most promise in consistently reducing soybean cyst nematode population densities. One focus has been on the impact of tillage after the increase in implementation of no-tillage practices in soybean production to reduce soil erosion, and improve soil moisture holding capacity (Denton and Cassel, 1989). Although several studies have been conducted on the effects of tillage on soybean cyst nematode, the effects have not been consistent. These results have been summarized by Chen et al., (2001b). Soil pH has also been documented to have an effect on soybean cyst nematode reproduction (Anand et al., 1995; Pike et al., 2002). Selection pressure has been demonstrated when soybean cyst nematode is continually exposed to a resistant plant source (Young, 1998). Because these management strategies appear to affect soybean cyst nematode reproduction, they will also have an impact on selection pressure. Together, efficient management techniques and improved germplasm for nematode resistance will result in durable resistance in soybean. The gap this research is addressing is inconsistent research results following different cultural control measures. These inconsistencies may be due to different cropping systems, soil types, environmental conditions and their interaction with soybean cyst nematode. Schmitt (1991) indicates that a 2-year rotation of corn-wheat-soybean is sufficient to reduce the population density of soybean cyst nematode below the damage threshold. Noel (1992) and Chen et al., (2001a) suggest that a longer rotation is necessary to reduce the population density. Population density levels play a role in the length of time necessary to reduce the egg level present in the soil. Tillage is reported to increase levels of soybean cyst in certain geographic locations while effects differ in other locations fail to see this effect (Chen et al., 2001b). Riggs et al., (2001) have found that over-winter survival of eggs is a function of geography. Date of planting studies using soybean in MG V and later have been conducted, and late planting was found to reduce soybean cyst nematode population density (Schmitt, 1991). Todd (1993) found that late planting was not an effective tool for managing soybean cyst nematode when soybean cultivars in MG III to V were studied. In the Mid South Area there is interest in planting early maturing soybean cultivars to complete the crop prior to summer drought and further reduce risk to the crop. This study is examining the effect of planting soybean cultivars in MG 0 through IV and the plant interaction with soybean cyst nematode. Donald et al. (1999) mapped the distribution of soybean cyst nematode in a field over 4 years. These data indicate that in some fields, site specific management technology may be beneficial to managing the nematode and increasing overall producer profit. Cover/trap crops have been used to reduce levels of plant parasitic nematodes including soybean cyst nematode (Weaver et al., 1995; Bernard and Montgomery-Dee, 1992). Preliminary data from cover crop studies indicates that soybean cyst nematode survived in roots but did not complete a life cycle during the 2002-2003 noncrop period. Preliminary data from the tillage study shows spatial variability in the nematode distribution but fairly uniform population densities across the different tillage regimes. Management strategies that work in conjunction with resistant cultivars are being explored to reduce population density of the nematode more quickly. Companies including Monsanto, Dow Agrosciences, Pioneer Hi-Bred International, and Syngenta Seeds have each developed corn inbreds expressing a new Cry3Bb or VIP-type toxins targeted for the corn rootworm complex, Diabrotica spp. The only rootworm-active product registered at this time is the Monsanto product designated event MON 863 with a Cry3Bb1 gene. This coleopteran-active gene is related evolutionarily to Cry1Ab but is different distinctly in both nucleotide and amino acid sequence with contrasting codon-amplification processes (Cannon 1996). A recent review of nontarget studies, Groot and Dicke (2002) concluded that it is essential to consider of the multi-trophic consequences and food web aspects of Bt transgenic crops. Various reports have been published suggesting that the tiered testing required by EPA to examine impacts of the coleopteran-active endotoxins on non-target organisms is insufficient (EPA 2002). Ingestion of proteins is probably the most hazardous to nontarget species. Nematodes, springtails and some soil mites browse on root cells but it is not certain if these groups ingest the toxin. Laboratory feeding trials suggest that at least four species of soil-inhabiting bacterivorous nematodes (Acrobeloides sp., Panagrellus redivivus, Distolabrellus veechi and Caenorhabditis elegans) are adversely affected by at least three members of the Cry5 family (Cry5B, Cry14A, Cry 21A) and one member of the Cry 6 family (Cry 6A) of proteins (Marroquin et al. 2000, Wei et al. 2003). Cry5B has significant and extensive homology (24% identical and 44% similar across their toxin domains of ~ 570 amino acids) with Cry1Ab, in use commercially. Cry6A has been reported as toxic not only to lepidoptera but also coleoptera (Soares et al. 1989, Uyeda et al. 1991). Nematodes respond similarly as do target lepidopterans when fed Cry5B. Upon ingestion, C. elegans experiences extensive gut damage, decreased fecundity and dose-dependent lethality. Preliminary greenhouse and laboratory tests suggest that abundance of the root-pathogen (Meloidogyne incognita) and bacterivorous (C. elegans) nematode were reduced when exposed to a diluted (compared to the Cry3Bb1 concentration in MON863 roots) root homogenate of MON 863 corn (EPA 2002). In another experiment, root leachate showed no effect. Although farmers may be grateful to have reduced populations of pathogenic nematodes in soil, many nematodes are not pathogens and play essential and beneficial roles in soil. Over 250 edited partial 18S rDNA sequences representative of nematodes from North America are available for plant parasitic and soil dwelling nematodes. These genetic markers act in a similar fashion as bar codes on consumer products. These sequences along with databases of mitochondrial and ITS1 sequences will be used to better define the players in the soybean rhizosphere. Reduced use of corn insecticides with nematicidal activity (Furadan, Counter) is probably one factor responsible for the rise in root lesion incidence, but an unexplored possibility is that reducing SCN population densities during the soybean year by planting resistant cultivars has diminished competitive interactions that formerly kept root lesion populations in check. Melakeberhan detected competition between P. penetrans and H. glycines for the infection of soybean (2003), and in trials simulating a growing season (Miller, 1970; Miller & Wihrheim, 1968), population densities of P. penetrans were reduced on tobacco plants infected with H. tabaccum. Whatever the explanation for the shift in root lesion populations, damage thresholds of this genus for soybean grown in Wisconsin has not been determined. The pathogenicity of Pratylenchus spp. to soybean in greenhouse and field trials (Ferris & Bernard, 1962, 1967) and to other crops, alone and in partnership with common soil fungi, warrant research on this pest in soybean systems. During the course of our work in potato systems, We see patchy growth of soybeans in fields infested with root lesion nematodes but have not studied the Pratylenchus/soybean interaction. Objective 2. Evaluate the effects of specific biological and ecological processes on communities of regionally important nematodes. Almost all SCN-resistant cultivars bred for the north central region share a common source of resistance from PI 88788, and most are effective at reducing SCN population densities to some extent. Cultivars carrying another source of resistance derived from Hartwig and marketed as Cyst-X technology will soon be available for several soybean maturity groups. Field trials using germplasm with CystX-derived resistance show a marked decrease in SCN population densities and there is optimism that SCN populations will be reduced, but it is unlikely that SCN will be eradicated. Multiplication rates of SCN are density-dependent; the rate of population increase is much greater when population densities at the time of planting are low (MacGuidwin et al. 1999, Todd et al., 2003, Francl and Dropkin, 1986). This phenomenon is widely accepted and generally explained by focusing on outcomes at high densities  e.g., intraspecific competition for feeding site is intense at high population densities and limits the number of nematodes able to infect roots. An intriguing study by Kort (1962) with potato cyst nematode found a positive density dependence in the multiplication of the potato cyst nematode, Globodera rostochiensis, when densities were very low. Under the current NC-215 project, Mr. Nathan Schroeder, is conducting experiments to determine if this phenomenon occurs for H. glycines. The data collected thus far support the hypothesis that infection rates of H. glycines on soybean increase as initial nematode densities increase, to a point. We propose to continue and develop further this research under the new project. Understanding how and when this phenomenon occurs, and the role of environmental signals versus nematode signals in regulating density dependent life processes will help us develop strategies to prevent low population densities of SCN from exploding. Nematodes and their antagonists in soil have co-evolved for eons in undisturbed soil ecosystems. An equilibrium between nematode population densities and antagonists exists in the undisturbed soil and in soil with monoculture. Nematode-suppressive soils have been detected in a number of locations throughout the world. The classical example of nematode-suppressive soils is the decline of cereal cyst nematode in Europe. Monoculture of the host crop cereals enhanced activities of nematophagous fungi and resulted in natural control of the nematode (Kerry et al., 1982). A few other examples of suppression of nematode populations by natural antagonists include sugarbeet cyst nematode by fungal parasites (Muller, 1982; Westphal and Becker, 2001), root-knot nematodes by the fungus Dactylella oviparasitica (Stirling and Mankau, 1978) and the bacterium Pasteuria penetrans (Dickson et al., 1994; Weibelzahl et al., 1996), soybean cyst nematode by fungal (Chen et al., 1996; Liu and Wu, 1993) and bacterial (Nishizawa, 1984) parasites, and ring nematode by the fungus Hirsutella rhossiliensis (Eayre et al., 1987). A nematode-suppressive soil may be caused by biotic or abiotic factors, but the detailed mechanism of development of nematode-suppressive soil remains unclear. Nematode-trapping fungi, for example, are greatly affected by soil type, organic matter, and other soil elements (Gray, 1987). A few studies have shown that culture practices, such as plant and cropping systems, affected activities of antagonists of nematodes (Bourne and Kerry, 2000; Chen and Reese, 1999; Schuster et al., 1998; Steudel et al., 1990; Timper et al., 2001). Studies of the activities of antagonists and nematode-suppressive soil will generate useful information to 1) understand the impact of changing management systems on the nematode communities, 2) enhance natural biological control by adoption of a best management system, and 3) identify potential antagonists for commercial use as biological control agents.

Measurement of Progress and Results

Outputs

• A list of sentinel nematodes that are important indicators of changing management strategies in this region will be developed.

Outcomes or Projected Impacts

• Use of bar codes will help identify major nematodes in the rhizosphere.
• Idntification of major rhizosphere nematodes will elucide interactions that have previously been unkown.
• Better understanding of rhizosphere interactions will promote better understanding and management of plant parasitic nematodes.

Milestones

(2005): A draft of sentinel nematodes for corn soybean rotation in conventional tillage will be prepared.

(2006): A draft of sentinel nematodes in a corn/soybean rotation in no tillage will be prepared. Verification for previous drafts will continue.

(2007): A draft of sentinel nematodes in production fields where GMOs are used will be prepared. Verification for previous drafts will continue.

(2008): Preliminary drafts of sentinel nematodes will be prepared for publication.

(2009): Publication of results.

(0):0

Projected Participation

View Appendix E: Participation

Outreach Plan

This research will be published in peer reviewed journals such as Journal of Nematology, Plant Disease, and ecological journals. Journal articles will be preceded by preliminary presentations at annual meetings of professional societies in related disciplines. The lists of sentinel species under the different cropping systems will be shared with extension personnel and commodity groups to aid in more effective management strategies.

Organization/Governance

An election is held every year to select the Secretary of the NC-215 Committee. After serving one year, the Secretary becomes the Chair. The Chair writes the annual report, and prepares an agenda for and presides over the annual meeting. The Secretary takes, prepares, and distributes the minutes for the meeting, and compiles mailing lists. Project leaders are responsible for collecting and compiling results for each project objective. Additional meetings are held at Annual Society of Nematologists meetings and other meetings where a majority of the NC-215 members are present.

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University of Toledo, USDA ARS