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W_TEMP3147: Managing Plant Microbe Interactions in Soil to Promote Sustainable Agriculture

Statement of Issues and Justification

The future of sustainable agriculture in the U.S. will increasingly rely on integrating various advanced technologies with traditional agricultural practices. Although genetic engineering of crop plants promises enhanced yields and new routes to disease resistance, it is also important to recognize that these plants associated with microorganisms, some of which cause plant disease while others protect against disease. Identifying, understanding and using microorganisms or microbial products to control plant disease and enhance crop production are becoming more central parts of sustainable agriculture. Biological control or biologically-based pest management (BBPM) has the potential to control crop diseases while causing no or minimal detrimental environmental impact. For this proposal, we define biological control as the manipulation of microbial populations antagonistic or suppressive to plant pathogens through cultural, physical or biological means, including plant mechanisms. Biological control may affect the populations and/or activity of plant pathogens. Some of the benefits of utilizing microorganisms include:

- Reduced dependence on chemical pesticides, which is important because of expanding demand for organic produce and increasing costs of such petroleum-based inputs
- Reduction in the development of pathogen resistance to biological control organisms,
- More selective action against pathogens and not against beneficial organisms;
- Biodegradability of microbial pesticides and the by-products of their manufacture
- Reduced danger to humans or animals
- Improvement of soil quality and health
- Increased food safety
- Management of diseases in natural ecosystems
- Improve plant productivity via controlling abiotic stress
- Adaption to climate change, as pathogen distributions shift
- Increased N use efficiency and reduced N and P contamination of waterways and oceans

Demand for biopesticides has continued to expand dramatically in the last five to ten years. A 2009 report from research firm Frost & Sullivan put the value of biopesticides in the US and Western Europe combined markets at US $594 million in 2008 and forecasted that the market will nearly double by 2015 to a market value of $1.02 billion (Biopesticide Industry Alliance, 2012). The Biopesticide Industry Alliance, established in 2001, had 31 member companies in 2006 but now has 65 members in 2012. The International Biocontrol Manufacturer's Association currently has over 130 companies marketing microbial biocontrol agents. This growth has been driven by expanding organic markets as well as increased public sensitivity to the risks and hazards of chemical pesticides. Within the last four years, 15 microbial active ingredients have been registered by EPA. Presently, there are 23 bacterial and 17 fungal active ingredients registered in the US.

However, further research is required to overcome problems related to high-volume production, storage, delivery, compatibility with conventional products, and formulation of such products. With increased demand for biological options, new active ingredients or organisms will need to be identified and characterized. In addition, regulatory agencies are increasingly interested in understanding the mode of action of such novel microbials. Therefore, basic research into the physiology and genetics of biocontrol microbes will continue to be needed. More research is also needed on how to use these products with integrated pest management (IPM) programs that have been developed for many crops.

This proposed research fits a number of the Strategic Goals and Objectives for 2010-2015 established by NIFA:
Objective 4.4
Protect Agricultural Health by Minimizing Major Diseases and Pests to Ensure Access to Safe, Plentiful, and Nutritious Food;
Objective 3.3  Support Sustainable Agriculture Production in Food-Insecure Nations and
Objective 1.3  Support a Sustainable and Competitive Agricultural System.
These goals are tied together by biological control and biologically based pest management- using the idea that the environment is enhanced by reducing our reliance on fungicides and nematicides to manage disease. Whether in rural communities or in developing countries, this research is geared toward rational, low input and sustainable agriculture.

Why a Multi-State, Multi-Disciplinary Approach? Because biological control is the result of complex interactions between the agent, the environment, and the pathogen, research in this area must be multi-disciplinary and collaborative. No single research institution has sufficient resources and variety of expertise to solve the diverse disease problems that might be addressed through the use of biological controls. Many of the targeted pathogens occur in multiple states and a coordinated research effort could provide more cost-effective outcomes. Because the results of our efforts are only now beginning to affect U.S. agriculture and the biopesticide industry, continuation of the W-2147 project for another five years will lead to further improvements in the efficacy and adoption of biological controls in American agriculture. In addition, these biological and cultural control techniques need to be tested under a range of environmental conditions and cropping systems that reflect the diversity of U.S. agriculture. The more than 20 researchers in this multistate project also collaborate with researchers in the U.S. and around the world, providing further impact and cross-fertilization of knowledge, as well as conducting the needed outreach activities for implementation of biocontrol options. In addition, because of the Great Recession and strained state and now federal budgets, the number of faculty and researchers in plant protection has been significantly reduced. Because of this reduction in resources and human capital, it is more important than ever to gain synergy by leveraging resources with a multi-state group.

JUSTIFICATION:

Economic Costs Due to Soilborne Plant Pathogens
From 2001-2003, an average of 7% to 15% of the major world crops (wheat, rice potatoes, maize and soybean) were lost due to diseases caused by fungi, nematodes, and bacteria (51). Detailed studies on the wheat crops in the Pacific Northwest had documented loss of up to 36% due to Pythium, Fusarium, Rhizoctonia, and Pratylenchus (16,20, 65,66).

- Soilborne pathogens are an important constraint to vegetable production in the US, as they cause significant reduction in quantity and quality of yield and their control adds greatly to the cost of production
- For root diseases of mature crops, there are few effective and economical post-plant strategies for control.
- About 90% of the 2000 major diseases of the principal crops in the US are caused by soilborne plant pathogens (35).
- Monetary losses due to soilborne diseases in the U.S. are estimated to exceed $4 billion per year (39), and losses due to parasitic nematodes exceed $100 billion per year world-wide (5). In soybeans in the U.S. alone, all diseases combined caused losses of $15 billion from 2000-2007 (76a).
- Since 2010, the stem and bulb nematode (Ditylenchus dipsaci) has re-emerged, with significant losses on garlic in NY, the NE region and Ontario, Canada.
- Several of the top 15 restricted, invasive quarantine pathogens listed by APHIS are soil borne, and could represent a biosecurity risk.
- New invasive species have been discovered in N. America in the last ten years, including Phytophthora ramorum, cause of sudden oak death, the potato cyst nematode, Globodera pallida in Idaho and most recently golden cyst nematode G. rostochiensis in Alberta and Quebec. The root knot nematode Meloidogyne enterolobii (syn. M. mayaguensis) was first detected in the U.S. in Florida a few years ago, and is aggressively spreading around the world. Once they become established in natural ecosystems, these pathogens cannot be easily managed.
- In the last three years, citrus greening (Huanglongbing disease) has decimated the citrus industry of Florida, and has been found in Texas and just recently (2012) in California.
- Laurel wilt, caused by Raffaelea lauricola and vectored by exotic ambrosia beetles, threatens the native laurels of the East Coast and the avocado industry in Florida and California.
- Changing climate will result in more plant stress, drought conditions, salinity or in some cases a wetter climate, which will predispose plants to more disease.

Environmental Costs of Soilborne Plant Pathogens
The cost of soilborne plant pathogens to society and the environment far exceeds the direct costs to growers and consumers. The use of chemical pesticides to control soilborne pathogens has caused significant changes in air and water quality, altered natural ecosystems resulting in direct and indirect affects on wildlife, and caused human health problems. For example, methyl bromide, a fumigant used to control soilborne diseases, has become notorious in recent years for contributing to the depletion of the ozone layer. The planned ban on production and importation of methyl bromide has been repeatedly delayed by a lack of cost-effective alternatives, and there remains an intensive search for replacement control methods. This fumigant was to be totally banned by 2005, but critical use exemptions for the U.S. resulted in 2011 usage that was still 10% of the 1991 levels. A potential alternative, methyl iodide, was recently (2012) withdrawn from the U.S. market for health concerns. Bayer, the maker of aldicarb (Temik), a widely used nematicide and insecticide on cotton and potatoes, has decided not to renew the EPA registration. A US distributor (Ag Logic) for Chinese pesticides picked up the aldicarb (Memik) registration, which raises serious questions concerning product stewardship of one of the most toxic compounds ever present in US agriculture. Telone (2,3-dichloropropene), a soil fumigant/nematicide widely used in potato production, has reduced supply and restrictions by township quotas in California. Larger buffers and restriction zones are needed for many pesticides. For example, in many counties in Florida, Telone is restricted to soils with a shallow hard pan in order to restrict water movement into the shallow water table. The registration for maneb, a protectant fungicide widely used for almost 70 years, was cancelled in 2010. Development of fungicide resistance continues to be a problem with the newer generation of low impact fungicides with specific modes of action, such as the strobularins.

Additionally, plants evolved in the presence of microorganisms and are dependent on them in order to carry out many activities necessary for growth and reproduction. Thus, long-term chemical applications may permanently alter the microbial community structure sufficiently such that sustainable agriculture may be impossible.

Society's Expectations
As is readily apparent from reading the popular press, consumers are demanding plentiful, low cost and safe food while simultaneously requiring the use of fewer chemical controls. In 2010, the organic industry grew almost 8% from the previous year, and the value of organic fruits and vegetables was $10.6 billion in the US, 12% of the total market (Organic Trade Association 2011 survey). Organic food sales have increased 337% from 2000 to 2010. In 2008, there were 2.6 million acres of certified organic cropland in the US, an increase of 117% since 2000 (NASS). Several other trends have accelerated since our last renewal. Organic food is now available from large retailers such as Wal Mart, Kroger Co and others. There is an increasing "locovore" movement where people want locally-grown food, usually grown organically, from farmer's markets, CSA (community supported agriculture) or community gardens. USDA has initiated a BioPreferredĀ® Program for labeling certified biobased products and for encouraging their use by federal agencies. This labeling will tell the consumer the percent of biobased ingredients in a product.

Organically-grown crops require non-synthetic methods for management of diseases, and organic growers are seeking scientifically-based disease management methods. Recent national surveys (2004) by the Organic Farming Research Foundation have identified pest and disease problems as a major concern for organic growers. Many of our products are certified as organic with the Organic Materials Review Institute (OMRI). During the last few years, more and more pesticides that control soilborne diseases have been taken off the market or regulated, including methyl bromide. Soilborne pathogens are well adapted to soil conditions, and once established are very difficult to eliminate. Even if chemical products are available, they are often too expensive to be economically practical. However, for many pathogens, chemical remedies have yet to be identified. Other approaches with great potential include the development of transgenic crops engineered with resistance genes to several pathogens. However, there is widespread public reluctance to accept these crops as evidenced by protests both here and in Europe. This has resulted in reluctance by growers to adopt such technology since consumer boycotts could be devastating, especially in small or specialty crop markets. These concerns, combined with the natural ability of pathogens to overcome introduced resistance genes, has frustrated efforts to maximize this approach.

The ultimate goals of this collaborative work of W-3147 are to:
- Provide society with a safe, low cost food supply
- Reduce the environmental impact of soilborne disease control on ornamental, bioenergy, fiber and food crop production
- Protect natural ecosystems from invasive species
- Development of new industries and products for biologically based disease control

Biological Control and Soil IPM Systems As Attractive Alternatives
Biological control is an attractive approach for the control of soilborne diseases (18,19,28,35,72,73,53,74,75,48,49,40,13,32,19). Advantages of a biological approach to disease control include a lack of environmental damage, reduced human health risks, lack of resistance development in the pathogen, selectivity in mode of action, lack of activity against most beneficial microorganisms, and improved soil conditions and agricultural sustainability.

Biological control of soilborne plant pathogens has made large strides over the past several years. Much of this success is due to activities of the members of W-3147. Today the EPA lists more than 40 commercial biocontrol agents that are registered and commercially available in North America. Nearly all of them have been registered during the past five to ten years. Within the last few years, several new products containing Trichoderma and Bacillus have been released. However, most of these products are for seed and seedling diseases. W-3147 project is unique in emphasizing biological control of root diseases of perennial crops, including tree fruits and turfgrass, which are generally not treatable as annual crops with chemicals or other methods. Since our last renewal, members of the former NC-125 have joined our group, extending expertise to important field crops, including soybean, corn, and alfalfa.

Interest and enthusiasm about biocontrol continues within the science of plant pathology. Since 2000, over 2,200 peer-reviewed articles have been published on biological control of plant pathogens (Web of Science, April 2012). In fact, two new journals were launched in the 1990s-the journal Biological Control, which covers arthropod, nematode and microorganism-mediated control methods, and Biocontrol Science and Technology. Combined with the increasing resistance in parts of the world to transgenic plants, it appears that the W-3147 regional project is both very timely and successful. Commercial interest has also increased substantially. In the past five years, a number of new companies have been formed that develop and market biopesticides. The industry is forecasted to expand considerably in the next five years.

In spite of the strides made in biological control research and development, there are many areas that require work before biocontrol will be used extensively. Current areas of research include:
- Identification of more effective agents. Workers are isolating potential antagonists from soils where many pathogens originated and testing on a range of pathogens.
- New bioinformatics information through the genomic analysis of the biocontrol agents and using microarrays to study gene expression in the plant. Within the last 3 years, seven Pseudomonas fluorescens isolates with biocontrol ability have been sequenced (38), while that of Lysobacter enzymogenes strain C3 is near completion. This initiative was spearheaded by members of W-3147, and included several biocontrol agent strains studied by members, including P. fluorescens Pf-5, Q8r1-96, 30-84 and Q2-87 and L. enzymogenes C3. Data mining of these genomes has resulted in the discovery of many new antimicrobial and insecticidal compounds.
- Advances in metabolomics and proteomics are also being used to study the biochemical pathways and in-situ detection of antifungal metabolites produced by biocontrol bacteria.
- -Omic advances have been used to identify and create new systems for the control of abiotic stresses, improve biological control, and increase abilities of plants to utilize nitrogen
- Understanding the genetic diversity of pathogens, biocontrol agents and beneficial microbes, using advances in DNA sequencing, such as pyrosequencing.
- Identification and characterization of natural disease suppressive soils. In the past 4 years, members have used next generation pyrosequencing to describe microbial communities associated with the natural decline of fungal and nematode diseases.
- Integration of biocontrol into current agronomic practices.
- Identification of parameters affecting efficacy and survival after application.
- Understanding the mechanisms of action of control, especially at the molecular and biochemical level.
- Investigation of manipulation of cultural parameters that advance biological control (eg. uses of compost, green manures, and rotation crops) and improve soil health and productivity.
- Understanding the role of the plant in biological control (vis-a-vis induced resistance pathways).
- Use of microbial products or metabolites and other biorational approaches, such as compost teas, plant strengtheners, etc.
- Controlling replant diseases in apples and mitigating root-knot nematode crop damage by use of Brassica seed meals

The promise, public acceptance and environmental benefits of non-chemical management of root diseases continue to make research on this area both timely and of critical importance to the future of U.S. and world agriculture.

Clearly there is much to be done in order to improve biocontrol agents so that they will continue to become major factors in the control of soilborne diseases. Biocontrol agents isolated by participants of W-3147 at ARS-WA, ARS-CA, CA-R, OR, MT, AK, OH, NE and NY have the ability to suppress a wide variety of plant pathogens that cause serious diseases of food, fiber and ornamental crops. The need for "high quality" biocontrol agents has never been more critical because of the pending loss of nematicides, fungicides and soil fumigants that agriculture has depended on for the last 50 years. Understanding the complex biological and environmental interactions that must occur for biocontrol to be effective requires the combined efforts of multiple investigators at multiple institutions focusing on different aspects of the problem, from applied to basic research. This logical approach is an area in which the W-3147 regional project has excelled and will continue to depend on during the next five years.

This project fits the goals of numerous other NIFA and USDA initiatives. But the need for this project has become even greater in the last few years, given changes in funding priorities. The panel on Biologically-Based Pest Management was eliminated in 2004, leaving many biocontrol researchers with reduced or eliminated funding, and this research has not been funded by other programs. The recent changes in NIFA grants toward larger multidisciplinary cooperative (CAP) grants has also made it more difficult for individual researchers to work on projects that do not fit the grand themes of these programs. This project will support the need for multidisciplinary research, without the high administrative costs associated with large CAP grants.

Last Modified: 17-Jun-2013

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