The future of sustainable agriculture in the U.S. will increasingly rely on the integration of biotechnology with traditional agricultural practices. Although genetic engineering promises enhanced yields and disease resistance, it is also important to recognize that plants exist in intimate associations with microorganisms, some of which cause plant disease while others protect against disease. Identifying, understanding and utilizing 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 through cultural, physical or biological means including plant mechanisms. Some of the benefits of utilizing microorganisms include:

• Reduced dependence on chemical pesticides, which is important because of expanding demand for organic produce, increasing costs of such petroleum-based inputs and regulatory requirements


• Lack of development of pathogen resistance to biological control organisms


• Lower regulatory costs of registration


• Faster reentry times after application


• 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 biotic and abiotic stress


• Adaptation 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. In the 5 years since our last proposal, the global market for biopesticides has doubled from $1.5 billion to $3 billion US (Biopesticide Industry Alliance, 2017). The Biopesticide Industry Alliance, established in 2001, had 31 member companies in 2006, 65 members in 2012 and now has over 120 members. The International Biocontrol Manufacturer’s Association had 130 companies marketing microbial biocontrol agents in 2012. But now there are approximately 230 biopesticide manufacturers (not including China and India) with about 98 of those in the Americas and 91 in Europe. This segment of the industry is expected to grow between 15% and 20% annually (http://www.ibma-global.org). This growth has been driven by expanding organic markets as well as increased public sensitivity to the risks and hazards of chemical pesticides. From 2008 to 2012, 15 microbial active ingredients have been registered by EPA. From 2012 to 2017, six Bacillus spp., two Trichoderma spp., one Streptomyces sp., one Pseudomonas sp. and one Muscodor sp. have entered the EPA regulatory process (EPA Biopesticide Workplans 2012-2017). 

     In the last 5 years, there has also been a concerted effort by larger companies to acquire and purchase smaller companies or their products, and increase their investment in this field.  For example, Bayer CropScience bought Agraquest, acquiring Serenade and other Bacillus products. At present, Bayer is still marketing legacy biocontrol agents, including those from Gustafson and others (Kodiak), AgroGeen (Bacillus firmus) and Prophyta (MeloCon). However, in their West Sacramento, CA facility, they are investing millions of dollars in discovery and characterizing new biocontrol agents. Other recent acquisitions have been Prophyta, a German company, by Bayer.  Syngenta acquired Pasteuria BioSciences. Monsanto has entered into a partnership with Novozyme.  Most recently, Bayer will be acquiring Monsanto.

 The other more recent development is next-generation sequencing technologies, also known as high-throughput sequencing. This technology is presently being utilized by our members. Companies are engaging in microbiome research, and using this as a tool to discover new products. These include startup companies such as Agbiome (supported by Syngenta and Genective), Bioconsortia, and Indigo.  Monsanto has also invested millions in conducting microbiome studies on the hundreds of test plots for variety development.   

This proposed research fits one of the REE Action Plan Goals- 

Goal 1. Sustainable Intensification of Agriculture Production.  Subgoal 1B.  Crop and Animal Health.  

Two actionable items fit in perfectly with this project and are also shared by ARS and NIFA-

1. Develop and extend effective, affordable, and environmentally-sound integrated control strategies to reduce losses caused by diseases, pests, and weeds, including early detection, identification, monitoring, and implementing biologically-based and area-wide strategies to manage key native and invasive species and postharvest pests.

      2.  Optimize integrated pest management practices for production crops by developing knowledge and tools for            cultural methods, biological control, and host plant resistance management tactics. 

Why a Multi-State, Multi-Disciplinary Approach?

As biological control is the result of complex interactions between the agent, the environment, and the pathogen, this research area must be multi-disciplinary and collaborative. No single research institution has sufficient resources and diversity of expertise to solve the diverse disease problems that might be addressed through the use of biological controls. Many of these 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-3147 project 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 40 researchers in this multistate project collaborate with additional scientists 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. This group is also at the forefront of research in soil health, and in understanding the complex interactions among the soil microbiota which provide benefits to the plant. 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 and bacteria.

• 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.


• In a survey on various crops in 35 US states nematode-caused yield losses were estimated between 5 to 25% (Koenning et al. 1999).


• Projected worldwide crop production losses as a result of nematodes infestation were estimated at 14.6% in tropics and subtropics whereas in the developed temperate countries, it was estimated as 8.8% (Nicol et al. 2011).


• Monetary losses due to soilborne diseases in the U.S. are estimated to exceed $4 billion per year, and losses due to parasitic nematodes exceed $100 billion per year world wide. In soybeans alone, all diseases combined caused losses of $15 billion from 2000-2007.


• Detailed studies on the wheat crops in the Pacific Northwest had documented loss of up to 36% due to Pythium, Fusarium, Rhizoctonia, and Pratylenchus.


• 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 fifteen years, including Phytophthora ramorum, cause of sudden oak death and the potato cyst nematode, Globodera pallida in Idaho. New invasive species such as Phytophthora tenticulata, have decimated native ecosystems in California. In natural ecosystems, once they become established, these pathogens cannot be easily managed.






• In the last few years, citrus greening (Huanglongbing disease) has decimated the citrus industry of Florida, and recently it has been spread to Texas and into California. Plant nutrition and root health are important factors in this disease. 






• 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.


• Boxwood blight, caused by Cylindrocladium buxicola, discovered in the US in 2011, has become endemic in 10 states.


• Wheat blast is a new disease in South America (Brazil) caused by a strain of the pathogen Magnaporthe oryzae. It has recently been detected in Bangladesh, but is not yet present in the United States.


• Macrophomina and Fusarium wilt in strawberries have become new problems, because of the loss of methyl bromide.


• Dickeya dianthicola was reported as a newly emerged pathogen causing blackleg and soft rot of potatoes in the Northeastern United States in 2015 and resulting in significant economic losses.


• 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 effects 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 this product 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 there are still a few critical use exemptions for the U.S. A potential alternative, methyl iodide, was recently (2012) withdrawn from the U.S. market. Telone (1,3-dichloropropene), widely used as a pre-plant soil fumigant- nematicide in potato production, has reduced supply and restrictions by township quotas, application times and methods. Larger buffers and restriction zones are needed for many pesticides. Soil fumigants are major contributors to volatile organic compounds affecting air quality, especially in the Central and Imperial Valley of California. 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 strobilurins. 

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 impaired. 

Society’s Expectations

            As is readily apparent from reading the popular press, consumers are demanding plentiful low cost but safe food while simultaneously requiring the use of fewer synthetic pesticides. This has been evident by the rapid growth of the organic food industry. In 2016, there were 5.1 million acres in organic production (USDA Organic Survey), almost double the acreage from 2008. The total farm gate value of organic products in 2016 was $7.5 billion, compared to $3.5 billion in 2011 (NASS). Total sales were $43 billion last year, up 8.4% from the previous year, representing 5.3% of total retail food sales in the U.S (Organic Trade Association). Several other trends have accelerated since our last renewal. Organic food is now available from large retailers such as Walmart, Whole Foods, Kroger Co and others. Amazon has recently acquired Whole Foods, which may result in further expansion of the organic market. There is an increasing “locovore” movement where people want locally-grown, usually organic food, from farmer’s markets, CSA (community supported agriculture) or community gardens. USDA has initiated a BioPreferred® 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.

A 2015 survey by the Organic Farming Research Foundation (OFRF) identified disease management and soil health as one of the top five research priorities. 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, as well as many carbamate and organophosphate nematicides (1). Soilborne pathogens are well adapted to soil conditions, and once established are very difficult to eliminate. A classic example of a disease shift with the loss of methyl bromide has been the increased incidence of Fusarium wilt and charcoal rot of strawberries (Macrophomina) in California, which were not major problems 10 years ago. 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 in the US and in Europe. This has resulted in grower's reluctance to adopt such technology as consumer boycott 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. 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 with chemicals or other methods as well as annual crops. Members of the former NC-125 have joined our group, extending expertise to important field crops, including soybean, corn, and alfalfa.  We have also had many members join from the southern and lower Midwest of the US since the last renewal, including those from MS, NH, ME, OK, MD, DE, and NJ. 

Continued Interest in Biological Control.

Interest and enthusiasm about biocontrol continues within the science of plant pathology. Since 2012, over 3,804 peer-reviewed articles have been published on biological control of plant pathogens (Web of Science, October 2017). During this same time, 10,360 papers were published on the subject of soil health. Much of this research is based on understanding how soil physical and chemical properties influence plant performance, but soil health must be studied in the context of microbiomes and how these affect plant diseases. This will be focus of the new project. 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, as outlined above. A new biocontrol agent, developed by one of our members, Barry Jacobsen (MT), was just registered in 2017 by EPA as a biological plant activator and is now marketed as LifeGard by Certis.  The active ingredient is a species of Bacillus mycoides that has been shown to induce resistance. This is just one example of the products that have been developed by this project over the last 40 years. 

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 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 upon which agriculture has been dependent 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. 

Relationship of this project with other funding opportunities and national goals.

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. Although NIFA has now shifted away from the CAP grants, there are fewer grants. NSF and AFRI Foundational grants that specifically fund this type of research have a low success rate. This multistate project will fill a niche for research, networking, and outreach in the field of biological control of soilborne plant pathogens and soil health.