Duration: 10/01/2016 to 09/30/2021
Statement of Issues and Justification
Plant-parasitic nematodes are ubiquitous pests and serve as a major constraint to agricultural production across the North Central Region (NCR). The NCR includes the major U.S. production areas of corn, soybeans, and small grains. The NCR is also home to major production sites for several vegetable crops (e.g. sugar beets, cucurbits, potatoes). Plant-parasitic nematodes cause yield loss in all of these production systems. The long-term goal of our committee is the effective and economic control of plant-parasitic nematodes in the NCR.
The need, as indicated by stakeholders
Stakeholders (growers, crop consultants, breeders, agrochemical companies) require unbiased data regarding the management and biology of regionally important plant-parasitic nematodes. The soybean cyst nematode (SCN), Heterodera glycines, is the most damaging pathogen of soybean in the U.S. resulting in annual yield losses greater than $100 billion (Wrather and Koenning, 2006). Plant-parasitic nematodes on corn cause an estimated annual 5% yield loss (Society of Nematologists Crop Loss Assessment Committee, 1987). Economically significant yield losses caused by plant-parasitic nematodes on other regionally important field and vegetable crops are also well documented (Koenning et al., 1999). This project will answer fundamental and applied questions to address yield loss caused by plant-parasitic nematodes.
The importance of the work, and what the consequences are if it is not done
Numerous species of plant-parasitic nematodes are found throughout the NCR. However, there is substantial variability across the region in both the biology of individual nematode populations and edaphic factors affecting nematode populations. For example, the ability of SCN to reproduce on soybeans with a common source of resistance has changed over time and varies substantially across regions (Niblack et al., 2008). There is a critical need to coordinate research that will lead to improved plant-parasitic nematode control strategies that reach beyond the borders of individual states. Through our coordinated research activities, we can effectively dissect such variability in order to develop regional recommendations for managing plant-parasitic nematodes. Without such coordination, we will miss opportunities for synchronizing experimental design and for meaningful data comparisons across the NCR. This would, ultimately, reduce scientific progress and result in a stagnation of development of new plant-parasitic nematode control strategies.
The technical feasibility of the research
All proposed objectives utilize standard nematology techniques. The participants in this technical committee represent the primary nematology expertise from each participating NCR state and are, therefore, technically capable of completing all proposed research. Previous accomplishments from committee members include the standardization of nematode extraction techniques, the assessment of nematode resistance in commercial cultivars, assessment of nematode-protectant seed treatments, and the determination of risk thresholds for plant-parasitic nematodes on corn (MacGuidwin and Bender, 2012; Tylka et al., 2011).
The advantages for doing the work as a multistate effort
Because nematodes do not recognize state borders, data regarding the biology and control of these pests are most effectively collected through collaborative multistate research. For example, SCN is distributed throughout the NCR (Tylka and Marett, 2014); however SCN shows significant geographical variability in its ability to overcome host resistance (Niblack et al., 2008). A coordinated multistate effort is essential to develop novel plant-parasitic nematode control strategies that surpass individual site-specific considerations. While local conditions remain fundamentally important for the control of plant-parasitic nematodes, the integration of research strategies among nematologists and plant pathologists who work with nematode pests in the NCR are indispensable for rapid progress in the field. Furthermore, each NCRA member institution employs, on average, only 1.25 faculty nematologists. Multistate research is therefore essential for collaborative research in nematology.
What the likely impacts will be from successfully completing the work
This project will lead to an increase in environmentally sustainable crop production by reducing yield loss caused by plant-parasitic nematodes. Based on 2012 crop production data (USDA Economic Research Service), a conservative estimate of 1% yield loss due to plant-parasitic nematodes translates into approximately $950 million in crop production loss for the NCR due to plant-parasitic nematodes. By combining applied and fundamental research with outreach activities, our project will improve the near- and long-term outlook for managing plant-parasitic nematodes.
Related, Current and Previous Work
Related, Current, and Previous Work
The research described in this renewal proposal for NC1197 will supplement and extend current knowledge regarding the management of plant-parasitic nematodes. The proposed multistate research is a continuation of a longstanding (previously NC1035) collaboration among NCR nematologists to solve the ever changing challenges due to plant-parasitic nematodes. A complete listing of accomplishments from the previous five-year period is available from yearly reports. The following are a subset of accomplishments during the previous project period:
- Tested the efficacy of resistance to SCN in thousands of soybean cultivars.
- Determined the efficacy of seed treatments for control of plant-parasitic nematodes on corn and soybeans.
- Resolved the relationship between plant-parasitic nematodes and fungal pathogens.
- Developed a risk matrix for plant-parasitic nematodes on corn.
- Determined the reproductive ability of thousands of SCN populations throughout the NCR on select soybean genotypes.
- Provided data-driven information on the economic management of plant-parasitic nematodes to stakeholders through extension bulletins, electronic communications and on-site visits.
Plant resistance is considered the ideal cornerstone for any plant-parasitic nematode management strategy. However, for many plant-parasitic nematodes, commercial resistance is non-existent or fraught with ongoing challenges. For example, there are no commercially available corn hybrids with nematode resistance. Resistance to SCN in most commercially adapted soybean cultivars is derived from a single common source, PI 88788. Almost every state in the NCR has a program to evaluate the performance of soybean cultivars using crop yield and quality measures. During the past project period, members of NC1197, in collaboration with agronomists and breeders, provided nematology expertise for breeding efforts and analysis of plant-parasitic nematode contributions to yield loss (Brzostowski et al., 2014; Heeren et al., 2012; McCarville et al., 2012; Melakeberhan et al., 2012; Melakeberhan and Wang, 2012; Hong et al., 2011; MacGuidwin et al., 2012; Kim et al., 2011; Bao et al., 2014).
While resistance to plant-parasitic nematodes is desirable, alternative control strategies should be pursued to augment resistance-based control. Furthermore, for many plant-nematode interactions, resistance is unavailable or in danger of losing efficacy (Niblack et al., 2008). Therefore, alternatives to resistance are required for effective management of plant-parasitic nematodes. During the previous project period, NC1197 participants made substantial contributions to the development and testing of alternative methods for control of plant-parasitic nematodes (Mock et al., 2012; MacGuidwin et al., 2012; Bao et al., 2013). A collaborative effort between NC1197 participants from Iowa, Kansas, Illinois, Wisconsin and Nebraska resulted in a publication describing a uniform methodology for the assessment of nematicide seed treatments on corn (Tylka et al., 2011). NC1197 participants are also currently preparing a manuscript that will establish a new risk matrix for plant-parasitic nematodes on corn. This collaborative output will be of substantial value to farmers and will replace the varied economic threshold numbers found throughout the NCR.
In addition to direct control strategies, agronomic practices and soil health affect the damage caused by plant-parasitic nematodes. One well-established metric of soil health is overall nematode diversity, which examines both free-living (non-parasitic) and parasitic species (Ferris, 2010; Bongers and Ferris, 1999; Doran and Zeiss, 2000). NC1197 participants are dissecting the complex interactions between agronomic practices, plant-parasitic nematodes and soil health (Melakeberhan et al., 2015; Nair et al., 2015).
Interactions between plant-parasitic nematodes and other pathogens are of great concern. For example, sudden death syndrome, caused by the fungus Fusarium virguliforme shows enhanced symptoms in the presence of SCN (McLean and Lawrence, 1993). NC1197 participants continue to examine the interactions of plant-parasitic nematodes with other pests and pathogens (Brzostowski et al., 2014; Marburger et al., 2014).
Nematodes are microscopic and live belowground; it is impossible to accurately determine nematode damage from aboveground symptoms. Many plant diagnostic clinics do not have personnel trained for the identification of plant-parasitic nematode genera. Therefore, several NC1197 participants perform diagnostic services through local plant diagnostic clinics or within their own laboratories. Survey work during the previous project period has increased our understanding of current plant-parasitic nematode issues in diverse agricultural systems throughout the NCR (Todd et al., 2014; Lopez-Nicora et al., 2014; Lopez-Nicora et al., 2012; Mekete et al., 2011).
Nematode populations typically contain a high-degree of genetic and phenotypic variability. For example, SCN has a high degree of genetic variability and can adapt to host resistance (Niblack et al., 2008). In 2002, members of NC1197 (formerly NC1035) developed a standardized protocol for the assessment of SCN virulence (Niblack et al., 2002). Since 2002, NC1197 participants have utilized this common assay to evaluate SCN populations throughout the region for their virulence phenotype on multiple sources of resistance. The majority of commercial SCN-resistant soybean cultivars grown in the NCR are derived from PI 88788. Correspondingly, our committee has found that the majority of SCN populations are now capable of reproducing on this source of resistance. This information serves as a critical resource to inform soybean breeders on the future utilization and deployment of resistance genes in the NCR.
The NC1197 has leveraged their expertise to coordinate and promote nematology education among stakeholders. Several members of NC1197 (Ohio, Indiana, Illinois, Wisconsin, Iowa) took part in an industry-sponsored conference in December 2015 to develop new strategies for improving knowledge of SCN across the NCR. This conference directly led to a proposal submitted (May 2016) to the North Central Soybean Research Board for the establishment of a 2nd SCN Coalition. The first SCN coalition (active from late 1990s to early 2000s) used a combination of media platforms to educate stakeholders on the importance of SCN management. We envision the second SCN Coalition to educate stakeholders on the increasing prevalence of SCN populations able to overcome host resistance.
Related multistate research projects
There are currently four multistate research projects focused on plant-parasitic nematodes (NE1040, NC1197, S1066, W3186), one for each regional association of land-grant universities. Each of these multistate projects has the ultimate goal of increasing U.S. agricultural production by reducing the impact of plant-parasitic nematodes. However, the specific objectives, nematode species of interest and agricultural production systems vary substantially among multistate projects. For example, S1066 gives significant attention to root-knot and reniform nematodes (Meloidogyne spp. and Rotylenchulus reniformis, respectively) on crops such as peanut and cotton. NE1040 gives primary attention to the role of soil health in the control of plant-parasitic nematodes. W3186 is focused on diverse agricultural production systems and nematode species with only slight overlap to the NCR. While some overlap exists among these multistate projects, our project renewal is justified by the need to address specific NCR stakeholder concerns regarding plant-parasitic nematodes.
Develop, evaluate, improve, and integrate management techniques for plant-parasitic nematodes in the north-central region (NCR) to increase grower profitability.
Determine interactions of nematodes with other pests and pathogens and the impact of nematodes on plant and soil health.
Develop and disseminate research-based information on the biology and management of plant-parasitic nematodes of economically important crops in the NCR.
Objective 1: Develop, evaluate, improve, and integrate management techniques for plant-parasitic nematodes in the north-central region to increase grower profitability.
A. Evaluate interactions of plant-parasitic nematodes with germplasm of economically important plants.
Soybean germplasm will be screened for SCN resistance using standardized protocols (Niblack et al., 2009). This will increase the number of SCN screening populations and improve the characterization of each cultivar’s resistance. In addition, we will evaluate existing public and private company cultivars for resistance to SCN in greenhouse and field experiments. Germplasm of other regionally important economic crops will be screened for resistance to plant-parasitic nematodes. For example, corn and wheat cultivars will be assessed for resistance to root-lesion and lance nematode species.
B. Assess intraspecific variability in nematode virulence and pathogenicity.
SCN populations will be assessed for virulence using the HG type test on a standard set of resistance sources from their states (Niblack et al., 2002). We will also determine the virulence of populations of other plant-parasitic nematodes through a combination of greenhouse and field experiments. This is typically accomplished through comparison of the initial and final numbers of nematodes on a particular plant variety.
C. Evaluate new commercial products and innovative strategies for the control of SCN, root-lesion and other plant-parasitic nematodes.
Various products are currently marketed as providing effective protection against plant-parasitic nematodes. For example, several nematode protectant seed treatments are currently available for control of plant-parasitic nematodes. It is very likely that additional products will become available to growers who will require unbiased information regarding the efficacy of these products. Our committee has historically served as an important source of data regarding new nematode control products. These data are presented to growers via multiple formats (field days, winter grower meetings, web casts, direct advice to crop consultants, electronic and paper-based guides). We will continue to evaluate new products using laboratory, greenhouse and field experiments. Experiments will assess the efficacy of products and interactive effects between different products and also against different pathogens. For example, the seed treatment iLeVO (fluopyram) is marketed for control of both the fungus Fusarium virguliforme and also SCN. We will also collect yield data from these field experiments across the region and subject them to meta-analysis.
D. Develop innovative methods to detect and quantify plant-parasitic nematodes.
The quantification of plant-parasitic nematodes relies on extraction from soil and roots, typically followed by identification and enumeration with a light microscope. While extraction procedures can be standardized for a targeted pest, they are often laborious and time-consuming. The microscopic identification of plant-parasitic nematodes requires extensive training. In this objective, we will develop molecular techniques for the identification and quantification of economically important plant-parasitic nematodes, making the process of detecting and quantifying plant-parasitic nematodes more efficient.
2: Determine interactions of nematodes with soil microbiota and other pests and pathogens on plant and soil heath.
A. Investigate pest and disease interactions involving plant-parasitic nematodes.
Plant-parasitic nematodes often interact with other pathogens to produce new or enhanced symptoms. This objective will examine the effect of other pests and pathogens on both nematode reproductive success and the ultimate effect of ematodes on plant health. Specifically, we will examine interactions between SCN and the soybean pathogens Fusarium virguliforme and Macrophomina phaseolina. Interactions between root-lesion nematodes and Verticillium dahliae on potato will also be investigated. Furthermore, possible interactions among nematode species will be examined in various crop systems. Experiments will be conducted in both field and greenhouse settings.
B. Determine the temporal and spatial dynamics of nematodes in relation to plant and soil health.
Soil samples will be collected from experiments at appropriate time intervals, and nematodes will be identified, enumerated and assigned to herbivore, bacteriovore, fungivore, predator or omnivore trophic (Okada and Kadota, 2003; Yeates et al., 1993) and colonizer-persister (c-p) groups (Bongers, 1990). Data will be processed to describe nematode diversity and community abundance (Shannon and Weaver, 1949), ecosystem disturbance, fertility and index and decomposition pathways (Bongers, 1990; Bongers et al., 1997), and the structure and function of the soil food web (Ferris et al., 2001). In addition to nematode community analysis, crop yield will be collected at the end of the season. The integrated agrobiological, ecological and environmental efficiency of the agronomic practices relative to soil health will be determined using recent modifications of the fertilizer use efficiency (Melakeberhan and Avendaño, 2008). Principal component analysis showed distinct correlation patterns among crops grown in different soil types with nematode community indices and soil physiochemical properties.
3. Develop and disseminate research-based information on the biology and management of plant-parasitic nematodes of economically important crops in the NCR.
We will coordinate our efforts to produce a consistent message regarding the importance of plant-parasitic nematodes and effective control strategies. We will conduct these outreach activities through traditional outlets such as grower meetings. In addition, we will coordinate the distribution of extension publications, webcasts and press releases throughout the NCR.
Measurement of Progress and Results
Extension and other publications providing unbiased data on the management of plant-parasitic nematodes.
Improved methodology for the extraction and identification of plant-parasitic nematodes.
Extension and other publications providing unbiased data on the management of plant-parasitic nematodes.
A regional database of germplasm with resistance or tolerance to plant-parasitic nematodes.
Outcomes or Projected Impacts
- Increased number of resistant cultivar options for growers and breeders to manage plant-parasitic nematodes.
- Improved efficiency in diagnosis of plant-parasitic nematode issues as measured by turnaround time for processing of samples.
- Increased profitability for growers through reduced plant-parasitic nematode damage.
- Increased awareness of plant-parasitic nematodes and strategies for control of these important and often overlooked crop pests.
(2016):A. Identify coordinators for each sub-objective.
B. Identify potential extramural funding for each sub-objective.
C. Begin laboratory and greenhouse experiments for objectives 1 & 2.
(2017):A. Continue laboratory and greenhouse experiments for objective 1 & 2.
B. Apply for extramural funding.
C. Begin 1st year of field experiments for objectives 1 & 2.
D. Perform preliminary analysis of 2016/2017 data.
(2018):A. Continue laboratory and greenhouse experiments for objectives 1 & 2.
B. Conduct 2nd year of field experiments for objectives 1 & 2.
C. Summarize findings for stakeholders (Objective 3) based on 2016 and 2017 data.
(2019):A. Continue laboratory, greenhouse and field experiments for objectives 1 & 2.
B. Analyze data from 2016-2018.
C. Summarize findings for stakeholders (Objective 3) based on 2016-2018 data.
(2020):A. Complete laboratory, greenhouse and field experiments for objectives 1 & 2.
B. Analyze data from 2016-2019.
C. Summarize findings for stakeholders (Objective 3) based on 2016-2019 data.
D. Coordinators for each sub-objective will begin formatting data for appropriate peer-reviewed journal.
(2021):A. Conclude data analysis.
B. Submit and revise manuscripts to peer-reviewed journal regarding objectives 1 & 2.
C. Summarize findings for stakeholders (Objective 3) based on complete data analysis.
View Appendix E: Participation
Objective 3 directly addresses our plan for outreach. Our audience includes growers, commodity groups, agribusinesses, regulatory agencies, and scientists in industry, government and academia. We will tailor our outreach to the most appropriate audience. For example, the SCN-resistant soybean cultivar information will be of greatest use and interest to growers and agribusinesses. In some individual states/provinces, this information will be disseminated in hard-copy form, published and disseminated by commodity groups. Individual states/provinces will publish applied research results annually through extension outlets, including traditional extension publications, bulletins and newsletters, and web sites. Again, these reports will be gathered for region-wide public access via the internet. Information generated through the fundamental research will be disseminated through refereed research outlets such as the Journal of Nematology, Plant Disease, Plant Health Progress, Phytopathology, and other scientific publications. Specific outreach goals are detailed in the timelines.
The chair and secretary will be nominated and elected by committee members for one year terms. We will use a standard form of governance.
Bao Y, Chen S, Vetsch J, Randall G (2013) Soybean yield and Heterodera glycines responses to liquid swine manure in nematode suppressive soil and conducive soil. J Nematol 45:21-29.
Bao Y, Vuong T, Meinhardt C, Tiffin P, Denny R, Chen S, Nguyen HT, Orf JH, Young ND (2014) Potential of association mapping and genomic selection to explore PI 88788 derived soybean cyst nematode resistance. The Plant Genome 7.
Bongers T (1990) The maturity index: An ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14-19.
Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends in Ecology & Evolution 14:224-228.
Bongers T, van der Meulen H, Korthals G (1997) Inverse relationship between the nematode maturity index and plant parasite index under enriched nutrient conditions. Applied Soil Ecology 6:195-199.
Brzostowski L, Schapaugh W, Rzodkiewicz P, Todd T, Little C (2014) Effect of host resistance to Fusarium virguliforme and Heterodera glycines on sudden death syndrome disease severity and soybean yield. Plant health Progress 15:1. Doran JW, Zeiss MR (2000) Soil health and sustainability: Managing the biotic component of soil quality. Applied Soil Ecology 15:3-11.
Ferris H, Bongers T, De Goede R (2001) A framework for soil food web diagnostics: Extension of the nematode faunal analysis concept. Applied Soil Ecology 18:13-29.
Ferris H (2010) Contribution of nematodes to the structure and function of the soil food web. J Nematol 42:63. Heeren J, Steffey K, Tinsley N, Estes R, Niblack T, Gray M (2012) The interaction of soybean aphids and soybean cyst nematodes on selected resistant and susceptible soybean lines. J Appl Entomol 136:646-655.
Hong S, MacGuidwin A, Gratton C (2011) Soybean aphid and soybean cyst nematode interactions in the field and effects on soybean yield. J Econ Entomol 104:1568-1574.
Kim M, Hyten DL, Niblack TL, Diers BW (2011) Stacking resistance alleles from wild and domestic soybean sources improves soybean cyst nematode resistance. Crop Sci 51:934-943.
Koenning SR, Overstreet C, Noling JW, Donald PA, Becker JO, Fortnum BA (1999) Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994. J Nematol (United States) 31:587-618.
Lopez-Nicora H, Mekete T, Sekora N, Niblack T (2014) First report of the stubby-root nematode (Paratrichodorus allius) from a corn field in Ohio. Plant Dis 98:1164-1164.
Lopez-Nicora H, Mekete T, Taylor N, Niblack T (2012) First report of lesion nematode (Pratylenchus vulnus) on boxwood in Ohio. Plant Dis 96:1385-1385.
MacGuidwin AE, Bender BE (2012) Estimating population densities of root lesion nematodes, Pratylenchus spp., from soil samples using dual active and passive assays. Plant Health Progress. doi:10.1094/PHP-2012-1120-01-RS MacGuidwin AE, Knuteson DL, Connell T, Bland WL, Bartelt KD (2012) Manipulating inoculum densities of Verticillium dahliae and Pratylenchus penetrans with green manure amendments and solarization influence potato yield. Phytopathology 102:519-527.
Marburger D, Conley S, Esker P, MacGuidwin A, Smith D (2014) Relationship between Fusarium virguliforme and Heterodera glycines in commercial soybean fields in Wisconsin. Plant Health Progress 15:11. http://dx.doi.org/10.1094/ PHP-RS-13-0107
McCarville MT, Kanobe C, O'Neal ME, MacIntosh GC, Tylka GL (2012) Effects of an insect–nematode–fungus pest complex on grain yield and composition of specialty low linolenic acid soybean. Crop Protection 42:210-216.
McLean KS, Lawrence GW (1993) Interrelationship of Heterodera glycines and Fusarium solani in sudden death syndrome of soybean. J Nematol 25:434-439.
Mekete T, Reynolds K, Lopez-Nicora HD, Gray ME, Niblack TL (2011) Distribution and diversity of root-lesion nematode (Pratylenchus spp.) associated with Miscanthus× giganteus and Panicum virgatum used for biofuels, and species identification in a multiplex polymerase chain reaction. Nematology 13:673-686.
Melakeberhan H, Avendaño F (2008) Spatio-temporal consideration of soil conditions and site-specific management of nematodes. Precision Agriculture 9:341-354.
Melakeberhan H, Wang W (2012) Suitability of celery cultivars to infection by populations of Meloidogyne hapla. Nematology 14:623-629.
Melakeberhan H, Douches D, Wang W (2012) Interactions of selected potato cultivars and populations of Meloidogyne hapla adapted to the Midwest US soils. Crop Sci 52:1132-1137.
Melakeberhan H, Wang W, Kravchenko A, Thelen K (2015) Effects of agronomic practices on the timeline of Heterodera glycines establishment in a new location. Nematology 17:705-713.
Mock VA, Creech JE, Ferris VR, Faghihi J, Westphal A, Santini JB, Johnson WG (2012) Influence of winter annual weed management and crop rotation on soybean cyst nematode (Heterodera glycines) and winter annual weeds: Years four and five. Weed Sci 60:634-640.
Nair MG, Seenivasan N, Liu Y, Feick RM, Melakeberhan H (2015) Leaf constituents of Curcuma spp. suppress Meloidogyne hapla and increase bacterial-feeding nematodes. Nematology 17:353-361
Niblack T, Tylka GL, Arelli P, Bond J, Diers B, Donald P, Faghihi J, Ferris V, Gallo K, Heinz RD (2009) A standard greenhouse method for assessing soybean cyst nematode resistance in soybean: SCE08 (standardized cyst evaluation 2008). Plant Health Progress 10: doi:10.1094/PHP-2009-0513-01-RV
Niblack T, Colgrove A, Colgrove K, Bond J (2008) Shift in virulence of soybean cyst nematode is associated with use of resistance from PI 88788. Plant Health Prog 10: doi:10.1094/PHP-2008-0118-01-RS
Niblack TL, Arelli PR, Noel GR, Opperman CH, Orf JH, Schmitt DP, Shannon JG, Tylka GL (2002) A revised classification scheme for genetically diverse populations of Heterodera glycines. J Nematol (United States) 34:279-288.
Okada H, Kadota I (2003) Host status of 10 fungal isolates for two nematode species, Filenchus misellus and Aphelenchus avenae. Soil Biol Biochem 35:1601-1607.
Shannon CE, Weaver W (1949) The mathematical theory of information.
Society of Nematologists Crop Loss Assessment Committee (1987) Bibliography of estimated crop losses in the United States due to plant-parasitic nematodes. J Nematol 19:6-12.
Todd T, Appel J, Vogel J (2014) Survey of plant-parasitic nematodes in Kansas and eastern Colorado wheat fields. Plant Health Progress 15:112. doi:10.1094/ PHP-RS-14-0003
Tylka GL, Todd TC, Niblack TL, MacGuidwin AE, Jackson T (2011) Sampling for plant-parasitic nematodes in corn strip trials comparing nematode management products. Plant Health Progress . doi:10.1094/PHP-2011-0901-01-DG
Tylka GL, Marett C (2014) Distribution of the soybean cyst nematode, Heterodera glycines, in the United States and Canada: 1954 to 2014. Plant Health Progress 15:85. doi:10.1094/PHP-BR-14-0006
Wrather JA, Koenning SR (2006) Estimates of disease effects on soybean yields in the United States 2003 to 2005. J Nematol 38:173-180.
Yeates GW, Bongers T, De Goede RG, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera-an outline for soil ecologists. J Nematol 25:315-331.
Land Grant Participating States/Institutions
IA, IL, IN, KS, KY, MI, MN, MO, ND, OH, SD, WI
Non Land Grant Participating States/Institutions