A. The Problem

Soilborne diseases continue to be a serious problem in US agriculture. They are caused primarily by fungi and nematodes, and attack the root systems, reducing the ability of plants to take up water and nutrients. They are difficult to diagnose, because above-ground symptoms may not be distinctive, and could be mistaken for nutrient deficiencies or drought. Unlike foliar diseases, they are difficult to manage with chemicals. They form survival structures in the soil that are resistant to chemicals, and it is near impossible to treat all the soil, except with fumigation, which can result in environmental degradation. Unlike with biotrophic diseases like rusts, there is little genetic resistance to soilborne diseases in available and industry accepted crop cultivars. Although some exceptions exist (i.e., Fusarium wilt, Fusarium oxysporum), in most cases host resistance to soilborne diseases is multigenic and difficult to breed for.

Economic Costs Due to Soilborne Plant Pathogens

According to the Food and Agriculture Organization (FAO) of the United Nations, plant diseases and pests reduce agricultural production by 20-40%, which represents a global cost of approximately 220 billion USD for diseases alone (Lazo, 2023). As such, 2020 was declared the International Year of Plant Health. For root diseases of mature crops, there are few effective and economical post-planting strategies for control. About 90% of the 2000 major diseases of the principal crops in the U.S. are caused by soilborne plant pathogens, most of which are fungi or fungus-like organisms (Panth et al., 2020). Many pathogens have a soil- or debris-borne over seasoning stage. In many cases, resistance to soilborne diseases is quantitative and specific pathogen race structures and population diversity parameters remain understudied.

Table 1. Crop production (million metric tons) for the top 10 crops (excluding vegetables) in the U.S. in 2021 (NASS, 2023).

As examples, certain commodities quantify and report yield loss data to all categories of diseases including those caused by soilborne pathogens. Corn data from 2016 to 2019 showed an average yearly loss of 9.6 million metric tons (Mmt) (2.4% of the 2021 production value; Table 1) to soilborne diseases including Fusarium stalk rot (F. verticilliodes, others) (5.1 Mmt yr^-1), nematodes (1.7 Mmt yr^-1), Gibberella stalk rot (Gibberella zeae) (1.3 Mmt yr^-1), seedling blights (0.9 Mmt yr^-1), and root rots (0.7 Mmt yr^-1) (Mueller et al., 2020). Likewise, soybean data from 2015 to 2019 showed an average yearly loss of 3.9 Mmt (3.2% of the 2021 production value; Table 1) to soilborne diseases including seedling diseases (1.29 Mmt yr^-1), white mold (Sclerotinia sclerotiorum) (1.10 Mmt yr^-1), sudden death syndrome (Fusarium virguliforme) (1.01 Mmt yr^-1), Phytophthora root rot (Phytophthora sojae, others) (0.66 Mmt yr^-1), and charcoal rot (Macrophomina phaseolina) (0.04 Mmt yr^-1) throughout the northern and southern soybean- producing states. Detailed studies on the wheat crops in the Pacific Northwest had documented loss due to Pythium, Fusarium, and Rhizoctonia. For 2021, the cotton disease committee (Cotton, Inc.) estimated losses in 480 lb bales to Fusarium wilt, Verticillium wilt (Verticillium dahliae), cotton root rot (Phymatotrichopsis omnivora), and seedling diseases (several fungi) to be 64800 bales (0.35%), 67600 bales (0.37%), 26500 bales (0.14%), and 146100 bales (0.80%), respectively.

New or re-emerging soilborne diseases are a constant threat to crop production in the United States. Such issues arise through pathogen introductions, changes in host germplasm, and altered control measures. For example, 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 crown rot (Macrophomina phaseolina) and Fusarium wilt in strawberries have become new problems, because of the loss of methyl bromide. In corn, tar spot (Phyllachora maydis) has emerged and caused disease losses in the U.S. since 2018 (Kleczewski et al., 2021). In soybean, Xylaria necrophora has emerged as a root rot and taproot decline pathogen in the southern U.S. (Garcia-Aroca et al., 2021) since ~2017. Several of the top 15 restricted, invasive quarantine pathogens listed by APHIS are soilborne and could represent biosecurity risks.

New invasive species have been discovered in North America in the last fifteen years, including Phytophthora ramorum, cause of sudden oak death, and Phytophthora tenticulata, have decimated native ecosystems in California. In natural ecosystems, once they become established, these pathogens cannot be easily managed. 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.

Finally, the changing climate represents a challenge and an opportunity to address soilborne pathogen problems. 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. Models based on global field surveys have shown that increasing soil temperature may increase the abundance of soilborne fungal pathogens (Delgado-Baquerizo et al. 2020). Further, Chaloner et al. (2021) project that as climate changes, higher latitudes will see greater yields, but pathogen turnover is projected to increase in some of the most productive swaths of global agricultural land. This includes the central Great Plains of the United States. Charcoal rot, a drought and high-temperature disease, was in the top 10 soybean diseases for the southern United States every year from 2015-2019, but had appeared in the top 10 diseases of the northern U.S. more often (3 of 5 yrs) during this period compared to previous disease loss reports (≤ 2 of 5 yrs).

Cost to the environment

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. 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 reduced-risk 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 impossible.

B. The Solution.

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 and increasing costs of such petroleum-based inputs


• 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 their by-products


• 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


• Adaptation to climate change, as pathogen distributions shift


• Increased N use efficiency and reduced N and P contamination of waterways and oceans

In the last five years, there has also been an increased awareness of soil health and the importance of microbes in providing benefits to plant health and productivity. Over the last 10 years, almost 30,000 papers have been published on the topic of soil health. There is an established non-profit (Soil Health Institute, https://soilhealthinstitute.org). States such as Washington have funded a soil health institute via legislative appropriations (Washington State Department of Agriculture, 2023). While NRCS has developed on-line resources to inform growers about soil health, there are no validated protocols for assessing soil health for all cropping systems and growers are clamoring for tests to help them determine their soil’s health. Additionally, THERE IS A LACK OF UNDERSTANDING ABOUT HOW SPECIFIC MICROBIAL GROUPS DRIVE SOIL HEALTH. Research proposed BY THIS PROJECT addresses these knowledge gaps and is ADVANCING THE FIELD.

Objectives

To address this problem, this project will propose four objectives

1. Objective 1. Biocontrol via one or a small number of microbes and/or their products


2. Objective 2. Biocontrol via microbial communities and soil health


3. Objective 3. Creating and testing disease management and/or soil health strategies


4. Objective 4. Extension and outreach

How this project fits the goals of USDA and REE

This project fits REE Action Goal Framework Goal 1: Sustainable Intensification of Agricultural Production. In 2017, USDA also issued a set of goals, and this overlaps with USDA GOALS 2 & 3. GOAL 2: Maximize the Ability of American Agricultural Producers To Prosper by Feeding and Clothing the World and GOAL 3. Promote American Agricultural Products and Exports. This entire project is designed to help farmers and growers manage soilborne pathogens in an environmentally sustainable way, thus directly impacting the large agricultural industry of the United States.

C. Addressing the Needs of the Stakeholders

1. The Biopesticide Industry.

Biopesticides are the fastest-growing crop protection market sector exhibiting substantial growth over the past three decades as the market has grown into a multibillion-dollar business. Demand for biopesticides has continued to expand dramatically in the last five to ten years. In the 5 years since our previous proposal, the global market for biopesticides has doubled from $1.5 billion to $3 billion US (Biological Pesticide Products Industry Alliance, 2023) and is expected to triple by 2027 (Batista and Singh, 2021; Sessitsch et al. 2018). Recent policy changes, such as the new Green Deal of the European Union, have expanded the biological product market. The Biological Pesticide Products Industry Alliance, established in 2001, had 31 member companies in 2006, 65 members in 2012 and now has over 120 members. The International Biocontrol Manufacturers Association had 130 companies marketing microbial biocontrol agents in 2012. But now there are approximately 2530 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, 2017). In the last 5 years, there has been a concerted effort by larger companies, such as Syngenta, BASF, FMC, and Bayer, to develop inhouse expertise by partnering or acquiring smaller companies, to increase their investment in this field. For example, Bayer CropScience bought AgraQuest, acquiring Serenade and other Bacillus products.

Additionally, the recent development of next-generation sequencing technologies and capacity to analyze metagenomic data has led to a greater understanding of how soil microbial communities function and influence plant tolerance to biotic and abiotic stressors. This technology is presently being utilized by our members to gain insights into plant-microbe interactions and identify implications for biocontrol. In fact, there has been a significant increase in research publications on the use of soil inoculants and consortia of microbes for disease control (Canfora et al. 2021).

2. The Microbiome Industry.

This is an industry that did not exist 15 years ago. The total agricultural microbial industry is estimated to increase by 17% yearly, with a value of $12 billion by 2026 (Research and Markets, 2018). Much of this growth is in “microbiome companies” such as Indigo, which has developed seed endophytes, AgBiome, Robigo, Inviao, and BioConsortia. Monsanto (now part of Bayer) invested a significant amount of money in microbiome research in the last 10 years. In addition, there are dozens of startup companies getting into the field. This involves a major paradigm shift.

Instead of just relying on developing biological control agents (BCAs) to apply to agriculture, the emphasis is to manage the rhizosphere and soil microbiome by management of the agricultural system, to promote disease suppression, nutrient uptake, and tolerance to abiotic stress. Nevertheless, many of these companies are using microbiome research to discover and market potential new inoculants. They are also marketing microbiome tests for farmers that would give them a diagnostic assessment of the soil health of fields, much in the same way companies have exploited this for the human gut microbiome. There is a large “probiotics” market for agriculture, but many of the claims made by developers of probiotics and soil health products and services are not based on sound research. Researchers in this project can provide sound, science-based evidence to help support adoption of products, services, and management practices that will be most valuable to growers.

3. The Organic Industry

As is readily apparent from reading the popular press, consumers are demanding plentiful low cost but safe food while simultaneously requiring reduced use of chemical 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 (NASS, 2023), almost double the acreage from 2008. In 2019, this number increased to 5,495,270 acres. with 16,585 farms. The total farm gate value of organic products in 2016 was $7.5 billion, compared to 3.5 billion in 2011 (NASS, 2023). By 2019, sales increased to 9.9 billion dollars. Organic food is now available from large retailers such as Walmart, Whole Foods, Kroger, and others.

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 (Jenkins and Ory, 2016). In 2020, The Organic Farming Research Foundation (OFRF) and Organic Seed Alliance (OSA) released an update survey in 2020 for California growers.

Some of the production concerns that were identified include controlling disease pressure, minimizing adverse impacts of tillage on soil health, and adapting to climate change. One of the top research priorities is maintaining yield and soil health. Members of this project are doing this research. Many products that members of W-4147 have researched 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. 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 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 and 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. These concerns, combined with the natural ability of pathogens to overcome introduced resistance genes, has frustrated efforts to maximize this approach.

Why a Multi-State, Multi-Disciplinary Approach?    This multistate project has a diverse group of researchers, with a long history of productivity and collaboration in the area of biological management of soilborne pathogens and diseases. Unlike some smaller groups that focus on one particular experiment or field trial across states, our group has fostered collaboration via the annual meetings.  These often lead to new ideas and new collaborations, especially when we meet in person.  This happens organically, rather than top down. This has resulted in large group projects (See Coordinated Agricultural Projects in Methods section).  These are focused on a common crop (eg. potato, camelina, soybean) or pathogen (cyst nematode). This synergy would not be possible without the support of a multistate group. This group has been extremely productive over the last 5 years. We have published 362 peer reviewed publications, 23 book chapters, 3 theses and 66 conference proceedings/abstracts by our members, among many other activities. Few other multistate groups can show this level of productivity. 

Goals and potential impact of the Project

 The ultimate goals of this collaborative work of W-5147 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 and agroecosystems from invasive species


• Development of new industries and products for biologically based disease control