W3186: Variability, Adaptation, and Management of Nematodes Impacting Crop Production and Trade
Statement of Issues and Justification
The Need as Indicated by Stakeholders:Estimates over the last 25 years indicate that plant-parasitic nematodes cause 10-14% average annual yield loss among the world's major crops (Sasser and Freckman, 1987), and losses ranging from minimal in some localities to as high as 15% in other areas in United States major crops (Koenning et al., 1999; McSorley et al., 1987). Indications from initial results of another global survey by the nematology community of nematode associated crop losses are that these estimates remain at similar levels. In economic terms, these estimated annual crop losses translate to at least $8 billion in the United States and $78 billion worldwide (Smiley, 2005). In addition, economic loss associated with increasing material and application costs of nematicides and associated with trade embargos due to actual or suspected quarantine nematode infestations exacerbate nematode problems in agriculture. Increasingly, scientific evidence and public awareness have heightened concerns about environment quality, food quality, and human health and safety relative to pest management in agricultural production. The need for alternative, integrated nematode management has been propelled by the actions triggered by the Montreal Protocol and the Food Quality Protection Act (FQPA) of the 1990s. Phase-out of methyl bromide is in the latter stages where current use has been reduced by about 96% and is allowed only under negotiated Exceptional Use Permit. Based on FQPA requirements, it is likely that widely-used and efficacious nematicides will be unavailable or greatly restricted in the future. For example, Nemacur, a commonly used nematicide on several crops was canceled in 2007, Furadan, commonly used on corn was cancelled in 2009, and Temik, an important potato nematicide was cancelled in 2011. In addition, the soil fumigant nematicide 1,3-dichloropropene (Telone II) is a B2 carcinogen, reviewed under FQPA and must be used under more rigorous restriction and recently supplies have been limited. Together with another fumigant, metam-sodium, the fumigant nematicides have been identified by California EPA as the largest agricultural source VOC (volatile organic compound) contributors to air pollution by ground level ozone formation. Development of methyl iodide, an anticipated replacement for methyl bromide has recently been abandoned. New US EPA Phase 2 labeling for all soil fumigants, implemented December 1, 2012, establishes mandatory buffer zones surrounding treated fields that will further curtail the use of these products.
Both locally and nationally, the agricultural production community (our stakeholders) is scrambling to find viable and agro-ecologically sustainable alternatives to chemical-based soil pathogen and nematode control. In addition, world travel and commerce have accelerated the dissemination of pest species, including plant-parasitic nematodes. Development and application of new diagnostic protocols for accurate identification of nematode species is beneficial and required for national and international regulatory and quarantine agencies relative to free trade and economics, as exemplified by recent trade restrictions on movement of potatoes due to findings of quarantine-status cyst or root-knot nematodes in US production areas such as Idaho. The nematology community has repeatedly advocated the need for funding support focused on the basic and applied research required to advance agro-ecologically sustainable alternative management approaches and accurate nematode detection and diagnostics. This proposed project renewal addresses these needs directly for the most important groups of plant parasitic nematodes, by building on advances made in the W-2186 project over the last 5 years.
Importance of, and Consequences Without, the Work:
Cyst, root-knot and other nematode species included in this project are the most important groups of plant-parasitic nematodes in the United States. Management of these nematodes in United States agriculture during the past fifty years has been largely via the application of broadly efficacious nematicides. Nematicidal activity, especially of soil fumigants, is generally non-discriminating, even between nematode species and genera. Therefore, understanding the genetic variability and adaptation potential among nematodes was not important for effective nematode control. In contrast, desirable alternative nematode management strategies involve combinations of crop rotation, host plant resistance, cultural manipulations, and biological control. All of these tactics may have specific genotype-level interactions with nematodes and are influenced by the production practices and environmental conditions. Hence, variability and adaptation in nematode populations must be considered to successfully develop and deploy alternative management strategies. This multistate project was initiated because the membership recognized the increasing importance of characterizing the genetic variation in nematode populations and its influence on success of alternative nematode management strategies. An example highlights the value of this project: Years of research went into the development of cyst-nematode resistant soybeans but the potential benefits of the resistance were limited due to the rapid selection of resistance-breaking nematode isolates. The biological processes in nematodes that influence the development of effective management strategies are complex, involving changes over multiple generations and interactions between nematode, host plant and environment. Therefore, a renewal of the project as requested herein is critical for continuing and completing the research required to meet the overall project goals.
A major shift in nematode-management strategies is occurring, from almost exclusive reliance on soil-applied nematicides, to the use of combinations of alternative strategies such as crop rotation, host plant resistance, cultural manipulations and biological control (Ferris et al., 1992). An important difference from nematicides is that the alternatives are influenced directly by genetic variability existing in target nematode field populations. Hence, the successful use of alternatives requires more information to implement than nematicide-based strategies. Herein lies the logic and raison dêtre of W-2186 and its proposed revision: assessment and characterization of variability and adaptation extant in nematode populations and agro-environmental conditions influencing host-nematode interactions will assist in the successful application of alternative management approaches, in addition to guiding initial development and deployment of new strategies. For example, knowing the frequency of virulence genes in a nematode population will allow deployment of corresponding resistance genes and promotion of resistance durability.
Except in the clearly demonstrable instances where resistance-breaking nematode populations are detected, the subtle influence of genetic variability in nematode populations has been considered only to a limited extent. However, the research conducted under the current W-2186 multistate project has provided considerable evidence that this variability is important. Results from current work indicate that genetic variability and adaptation potential in nematode populations are responsible for the aberrant and inconsistent results of many experiments assessing resistance, crop rotations, host ranges, cover/trap cropping, and biological control. The plasticity of nematode responses to abiotic environmental factors such as temperature, moisture, soil conditions, and host nutrient status stems from genetic variability, and such responses require much additional characterization. Greater understanding of nematode genetic response and adaptation to abiotic factors will be important in optimizing the design of cultural management tactics such as manipulations of planting and harvest times, wet or dry fallow, and soil solarization. The potential for invasive nematode pests to establish in our agricultural production systems also can be better determined from studies on genetic response and adaptation to local environments.
Without the proposed work continuing in a coordinated manner, the participants believe that effective nematode management alternatives will be developed more slowly, with success coming more on an ad hoc basis and with economic inefficiencies and a high likelihood of short-term failure of new products or management approaches. Knowledge gained from our main focus on cyst, root-knot and other significant nematodes will be applied and tested between nematode groups within the project matrix (see Table 1 in Attachments). This will strengthen the overall scientific scope of the research activities and will broaden the impact of the findings to benefit agriculture in multiple states.
Technical Feasibility of the Research:
Recent advances in molecular and genetic methodologies and knowledge will facilitate the study of nematode genetic variability and adaptation and promote diagnostic protocols with much greater resolution than has been possible. Some of these protocols have been developed and tested under the current project. For example, shared root-knot and cyst populations led to characterization of a mitochondrial cytochrome oxidase I (COI) gene that promises to alleviate current ambiguities in molecular species identification within these difficulty-to-identify genera. Addition of these and other new sequence information generated by the current project to on-line databases and knowledge-based systems will assist in information transfer to user groups in the relevant agricultural communities.
The root-knot and cyst nematodes are distributed throughout the United States and are damaging pathogens, parasitizing a wide range of important crops. Three groups of nematodes are the primary focus for this project: Group I - The warm-temperature root-knot species (Meloidogyne incognita, M. javanica, M. arenaria); Group II - The temperate root-knot species (M. chitwoodi and M. hapla); Group III - The cyst species (Heterodera schachtii, H. cruciferae, H. glycines, Globodera pallida, and the newly discovered species G. ellingtonae). These nematodes are the subject of research efforts in the designated participating states. Current research is addressing many areas of management for these three groups, including: development and deployment of nematode-resistant plants; rotation to reduce population densities of these pathogens; cover crops, trap crops and soil amendments including green manures to reduce population densities; the role of weed hosts in bringing about phenotypic changes in nematode populations; characterization of resistance genes and resistance responses; the development of molecular diagnostic protocols for nematode identification and the reference databases necessary for their implementation. Thus, the project participants share a strong common interest that will provide the central focus for both project members and other collaborators. In addition, parallel studies will be made by some participants on other endoparasitic nematodes, reniform nematode (Rotylenchulus reniformis), lesion nematodes (Pratylenchus spp.), stem and bulb nematodes (Ditylenchus spp.), important ectoparasitic nematodes including stubby root (Paratrichodorus spp.), dagger (Xiphinema spp.), and ring (Mesocriconema) nematodes; and outgroups including Mermithidae and C. elegans that provide genetic models for assessing variability and underlying mechanisms. This will maximize both the scientific scope of the project and its multi-state impact in agriculture.
Characterizing genetic variability requisite for novel management strategies:
The unifying theme of this proposal is that genetic variability is a critical biological feature that complicates management and enhances the pest status of species and populations of the highly specialized plant parasitic nematodes. W-2186 participants and others have begun to document the extent of genetic variability within populations, and the agro-environmental factors that influence it. Rapid developments in molecular biology techniques and their application through this project will continue to increase our understanding of the genetic processes involved. As understanding of genetic variability in nematode populations increases, it has become clear that the race concept and other means of characterizing nematode population differences are inadequate. Failure of current nematode management, such as breakdown of resistance, and successful development of novel approaches can be resolved through greater understanding of the underlying genetic and biological processes in parasitic nematode populations vis a vis management. For example, the importance of mutation compared to maintained variability in field populations is unclear, and this is a research area that will be pursued.
Genetic variability can impact both the effectiveness and longevity of alternative nematode-management strategies based on host plant resistance, crop rotation, cultural manipulations and biological control. Therefore, continuing the knowledge development in these systems should provide rational guidance for the design and development of management strategies. The project focus is on understanding nematode variability and adaptation, such that it can be identified, characterized, and managed or manipulated to benefit agricultural production systems. This requires research on the phenotypic and genotypic characterization of variability and gene frequencies, including aspects of stability and adaptability, of host range, response to resistance, response to environmental conditions, biological processes (e.g. fecundity) and morphology. This approach is being complemented and aided by development of markers to identify variability by molecular, histochemical, and morphological polymorphisms. The development of molecular techniques with greater efficiency, predictability and ease of use will expedite the nematode genetic analyses and design of management systems. Current and previous work under W-2186 has allowed participants to make advances on these research goals. However, this work cannot be considered complete and pressure for alternatives to nematicides has increased. Relative to our objectives, it is exciting that the arsenal of established and new tools used to address our applied research questions is increasing rapidly (e.g., Atkinson et al., 2001; Brito et al., 2004; Blok and Powers, 2009; Gleason et al., 2008; Handoo et al., 2012; Karl and Avise, 1993; McClure et al, 2012; Powers, 2004; Powers et al., 2005; Sambrook and Russell, 2001; Skantar et al., 2007; Sukno et al., 2007; Vos et al., 1995; Webster, 2004).
Four key considerations based on nematode genetic variability are central to development and deployment of alternative management strategies as proposed under this multistate project:
1. Host plant resistance The genetic composition of nematode populations is changed by the selection pressure imposed by growing resistant cultivars. The changes include shifts in species composition, and shifts in presence and frequency of nematode virulence alleles matching specific resistance genes in crop cultivars (Petrillo et al., 2006). Similar potential shifts may occur in response to nematode-resistant trap crops. Little is known of the existing frequency of virulence alleles, the frequency with which new alleles are generated, or the underlying mechanisms that regulate changes in genetic variability in root-knot, cyst and other nematode populations. As more sources of resistance are bred into cultivars, knowledge of gene frequency and stability effects assumes greater importance in determining the direction and requirements of breeding for nematode resistance, and the effective long-term deployment of available resistant cultivars (Starr et al., 2002; 2009).
2. Host range for rotations and cover-cropping - The host ranges of important nematode species have been defined within general limits, but the extent of variability in host range among populations within species is not well-characterized. Thus, although most cyst nematodes have narrow host ranges and are amenable to control by non-host rotation programs, less is known about the extent of reported hosts outside the typical host taxa, the likelihood of shifts in host range, or the host ranges of new species. For example, although sugarbeet cyst nematode hosts are found almost entirely within the Brassicaceae and Chenopodiaceae, tomato (Solanaceae) has been reported to host this nematode in California and Utah, with potentially serious consequences for rotation planning in western sugarbeet production areas. For the new cyst species Globodera ellingtonae in Oregon, little host range data are available. Evidence for genetic adaptations and modification of nematode host range has also been presented whereby local nematode populations are better adapted to local weed populations. The processes involved in these interactions are poorly understood.
In contrast to cyst nematodes, root-knot nematode species have broad host ranges of more than 2000 plant species from diverse plant families. Much of this host range information has been compiled from numerous tests and observations based on non-standardized host testing procedures, and in most cases with only one or a few isolates per species. Standardized conditions are needed to determine whether differences are due to variability in nematode populations or to differences in susceptibility in the plant lines used. For example, there is evidence that local weed populations influence the behavior of root-knot nematode populations on subsequent crops (Trojan et al., 2007). Resolving the true levels and stability of host range relationships will be critical to development and implementation of non-host crops in rotation and cover-cropping programs, and for determining the role that host weed species play in maintaining nematode population levels.
3. Cultural controls - Many are based on manipulating abiotic effects on nematode populations to suppress nematode activity or infection. Examples include wet or dry fallowing so nematodes starve while active (wet fallow) or die from extreme moisture stress (dry fallow). Soil solarization involves natural heating of soil under plastic cover to attain the thermal death point of nematodes. Avoidance may include changes in planting and harvest dates, such as delaying planting in the fall to avoid infection activity, and early planting or late harvest of crops to avoid additional nematode generations. Genetic variability in nematodes for response to temperature and moisture has been demonstrated, but it is not known how quickly or how stable such adaptive changes are, nor their frequency. Soil amendments such as green manures and various bioproducts show promise for nematode suppression in some systems and require further study.
4. Biological controls - Some potential biological control agents of cyst and root-knot nematodes are known to have specific host ranges among target nematode species, such as the host specificity of the bacterium Pasteuria penetrans among root-knot nematode species and populations. Such specificity may be controlled genetically, through surface protein binding and recognition between bacterium and nematode, suggesting that genetic variability in Meloidogyne may influence the potential of the bacterium and similar organisms as useful biological control agents.
Advantages of a Multistate Effort:
Under the current project, the membership effectively initiated research to apply emerging methodologies to obtain knowledge of the variability and adaptation potential in nematode populations. The W-2186 membership proposes to continue and extend these efforts in this regard, to identify and characterize the variability in cyst, root-knot, and other important nematodes. The participants share research interests on primary nematode pathogens and bring complementary expertise to the project. In this iteration of the project, we will determine gene frequencies, genetic stability, and adaptation and fitness, such that genetic variability can be managed and manipulated in agricultural production systems by appropriate alternative management strategies. The cyst and root-knot species are of primary importance as major nematode pathogens and as actual or potential invasive nematodes in most agricultural production areas and cropping systems throughout the United States. This is reflected in the proposed contributions from participating states across the country. The diversity in cropping systems and rank of importance of nematode groups among participating states clearly provides opportunities for conducting meaningful collaborative research on major nematode pathogens exposed to similarities and variations in crop (host), resistance, environmental and agro-ecological conditions. The participants utilize the opportunity to collaborate in ways that enhance the benefits accrued from the research, as opposed to what might be gleaned if the researchers were to simply pursue individual projects within limited geographic boundaries. For example, the warm climate root-knot species will be studied by participants from 10 of the 15 participating institutions (see Attachment Table 1) a group effort that will pay large dividends in understanding nematode variability relative to management.
Based on benefits of the current project we believe the similarities in the target nematode groups and the problems for nematode management imposed by variability and adaptation can be researched most efficiently through this coordinated multistate project. This team approach enables a pooling of scientific expertise and resources to maximize the amount and quality of the information that can be generated. The resources available to researchers working within the Agricultural Experiment Stations have been continually declining in recent years, and are particularly limited for nematology programs at this time. Conversely, the demands and expectations for new, environmentally friendly management tactics have never been greater. Accordingly, the membership has experienced a do more with less environment. This multistate project can provide some relief, as a necessary forum for rapid scientific advancement in aspects of both basic and applied research directed toward nematode diagnostics and development of alternative management strategies. For example, it is unlikely that all participating states will have programs devoted to molecular research on nematodes, and yet the need for molecular-level approaches for diagnosis and to assess genetic variability is required to address significant problems. This project has ongoing molecular-based programs in a few states (e.g. California, Hawaii, Mississippi, Nebraska, New Mexico, Washington) that can act to facilitate research by other participant states. In turn, those states focusing on phenotypic differences in nematode populations can provide nematode populations and isolates for molecular analysis. This coordinated approach minimizes unnecessary duplication of research programs, and provides fertile opportunities for a seamless, interactive approach to development of integrated nematode management. Most importantly, the project also enhances the quality and applicability of the research findings across geographic locations and agricultural production systems.
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