Agricultural and horticultural crops are produced with an estimated market value of $212.3 billion in the United States each year (USDA, 2014). Soil-borne plant pathogens are diverse and encompass microorganisms such as fungi, oomycetes, bacteria, viruses and nematodes that cause pre- and post-emergence damping-off, root and crown rots, vascular wilts, as well as foliar blight in these crops and amenity plantings. Soil-borne pathogens often survive for long periods on host plant residue, soil organic matter, or as free-living organisms. Soil-borne pathogens may have broad host ranges, and crop species may be susceptible to several different pathogens. Due to the menagerie of plant species produced by growers, and hectares managed, soil-borne disease management is challenging. Interactions with soil texture, chemistry, and environmental conditions make soil-borne disease management challenging. Diseases caused by these pathogens reduce plant performance; increase costs to the grower and cause potential ecological damage to the natural environment. As an example, losses due to soil-borne diseases in Georgia in 2014 were estimated to be $149 million in ornamental and turf production (Little, 2014).

The National Integrated Pest Management (IPM) Road Map has listed “Develop advanced management tactics for specific settings that prevent or avoid pest/disease attack” and efforts to “Improve the efficiency of suppression tactics and demonstrate least-cost options and pest/disease management alternatives” as critical research needs (IPM, 2013). Soil-borne diseases are becoming more difficult to manage because of increased pathogen resistance and restrictions of the use of some chemicals. Conventionally, soil-borne diseases are controlled by using soil fumigants, in-furrow fungicides, or fungicide seed treatment. Once a widely used fumigant, methyl bromide, was phased out of use in 2005 due to its negative effect on the stratospheric ozone layer (Dungan et al., 2003). The loss of methyl bromide has promoted increased interest in alternative methods to control soil-borne diseases. Although safer or less environmentally impactful chemical and non-chemical plant disease management methods have been developed, their results are still inconsistent (Keinath et al., 2000) and less effective than the previous standard, methyl bromide (Gerik and Hanson, 2011).

Some soil-borne pathogens have broad host ranges, reducing the effectiveness of crop rotations in soil-borne disease management. Further, the susceptibility of plants to disease is related to their macro- and micronutrient status; both excesses and deficiencies in nutrients predispose plants to disease (Dick and McCoy, 1993; Maynard, 1994; Workneh and van Bruggen, 1994). Clearly, additional soil-borne disease management strategies suited to the practice of sustainable production are urgently needed.

Over the last 15 years there have been surprising and exciting innovative discoveries for natural methods to suppress or eliminate plant pathogens, and/or protect crop plants. Intensive studies of disease-suppressive soils have led to the development of new methods of analysis (Gross et al., 2007; Borneman et al., 2007; Bolwerk et al., 2005; Benitez et al., 2007) and new insights into the nature of soil-borne disease suppression (Hoitink and Boehm, 1999; Han et al., 2000; Krause et al., 2003; Alfano et al., 2007). Such advances indicate that active management of soil microbial communities can be an effective approach to developing natural suppression of diseases and improve crop productivity (Mazzola, 2004). This involves adjusting the types and timing of organic inputs, such as cover crops, animal manures, composts, compost teas, and crop sequencing. Such approaches have been shown to provide site-specific reductions in disease incidence (Abbasi et al., 2002; Rotenberg et al., 2005, Stone et al., 2003; Darby et al., 2006; Larkin et al.,2006; Larkin, 2008). This technology fits the general requirements of sustainable agriculture in that it utilizes natural means to control diseases. However, standardized and reliable techniques for pathogen suppression have not been developed and widely tested on different crop production systems for controlling soil-borne diseases. In part, this is due to the wide variety of organic amendments that are available and their variable effects depending on the chemical makeup of organic substrates, soil types, and/or local climatic conditions.

Soil incorporation of Brassica or other cover crops has the ability to suppress soil microorganisms through the hydrolysis of glucosinolates (GSL) into isothiocyanate, a natural biofumigant (Kirkegaard et al., 1993, Matthiessen and Kirkegaard, 2006). GSL content and concentration differs among Brassica cultivars, the development stage of the plant (Bellostas et al., 2007), and the end product formed by hydrolysis of the GSL, so that different Brassica cultivars may have different levels of potential to control pathogens (Motisi et al., 2009). Therefore, it is important to study the different GSL-hydrolyzed end products produced by different Brassica crops and their effect on major soil-borne diseases. Incorporation of biofumigant use in the crop production cycle may provide additional successful and sustainable solutions for improving soil quality and enhancing natural soil-borne disease control. The effective use of biofumigants in crop production appears to be limited by a range of factors, which needs to be examined to provide effective recommendations to growers.

Several commercially available biopesticides are composed of specific isolates of soil microorganisms that were selected for their capacity to suppress a range of pathogens. These biopesticides may operate through multiple mechanisms, such as niche exclusion, biocidal/biostatic effects, antibiosis, predation, and parasitism (Handelsman and Stabb, 1996; Fravel, 2005). Some of the most common microbe-based biopesticides contain bacterial isolates of Bacillus spp., Pseudomonas spp., or Streptomyces spp., or fungal isolates of Gliocladium spp. or Trichoderma spp. (Fravel, 2005). Many of these organisms suppress disease and associated pathogen populations through multiple mechanisms. Numerous studies and reviews have documented the potential of microbe-based biopesticides to suppress both foliar and root diseases (Doumbou et al., 2001; El-Tarabily and Sivasithamparam, 2006; Emmert and Handelsman, 1999; Fravel, 2005; Jacobsen et al., 2004). However, the general consensus among these reviews is that integration is the key to obtaining consistent activity from biopesticides (Fravel, 2005; Jacobsen et al., 2004). Amongst the microorganisms developed for biological control of plant diseases, Bacillus spp. particularly have been exploited due to their stability for long periods of time and their antimicrobial activity (Fravel, 2005). Suppression has been attributed to the direct antagonism of pathogen growth through the production of various metabolic byproducts (Peypoux et al., 1999; Bonmatin et al., 2003). Additional work also demonstrated that some of these metabolites may also stimulate plant defenses, conferring an additional layer of control (Ongena et al., 2007).
Several species of Streptomyces have also been evaluated for disease control, mostly against fungal pathogens. A screen using the fermentative products from several Streptomyces spp. isolated from soil were found to inhibit several fungal pathogens, including Pyricularia grisea, Botrytis cinerea, Phytophthora infestans, Puccinia recondita, and Blumeria graminis (Park et al., 2003). Streptomyces spp. have also been evaluated as possible agents for the control of potato scab, caused by S. scabies (Liu et al., 1995).

Adoption of biopesticides has increased. But there is a need for biopesticides to provide workable disease management solutions for growers. Demand for biopesticides has continued to expand dramatically in the last 15 years. However, despite substantial growth in the industry and markets, there is still a lack of publicly available data that substantiates efficacy and return on investment for most products. There is a critical need to develop and disseminate science-based informational resources that will promote useful and sustainable adoption by growers that experience significant plant disease pressure. Lack of knowledge about disease management and fears of extensive losses due to disease and other pests contribute to lack of adoption of farming practices (Walz, 1999; Lotter, 2003). However, growers' specific knowledge gaps regarding disease management in agricultural crops are not well documented. It is critical that growers not only choose but also use biopesticides appropriately within a comprehensive disease management system or sound integrated pest management.

Given the need for sound integrated pest management, approaches coordinating chemical and biological controls are needed. Recently emphasis has been placed on understanding the phytobiome of plants or microbiome of production soils. While metagenomic techniques, in theory, should allow for identification and association with soil-borne diseases, more importantly, these techniques offer the opportunity to understand biological suppressiveness (Weller et al., 2002). However, there are limitations to these methods (Nesme et al., 2016) so evidence must be combined with spatial analysis (Liu, Griffin, and Kirkpatrick, 2014) or analyzed across multiple locations and years to limit sampling error and bias (Paul et al., 2011).
Recently, the use of indigenous vs. synthetic microbiomes to control soil-borne diseases was explored (Mazzola and Freilich, 2017). There are clear advantages with respect to survival and likely efficacy when microorganisms adapted to the specific environment or competing for a similar niche in the phytobiome are used. Numerous examples are presented in the literature (albeit determined with more traditional laboratory and field techniques). For example, fungi antagonistic to Rhizoctonia have been identified and have been shown to have the ability to reduce the severity of disease on numerous crops. Of these, some are other nonpathogenic Rhizoctonia solani, binucleate Rhizoctonia or fungi in other genera such as Trichoderma spp. or a sterile white basidiomycete. Recently, R. solani AG11 was shown to be associated with reduced soybean seedling disease caused by Pythium spp. (Spurlock et al., 2016). Ichielevich-Auster (Ichielevich-Auster et al., 1985) showed that a nonpathogenic isolate of R. solani AG4 reduced damping off in seedlings of cotton, radish, and wheat by R. solani and R. zea by 76-94%. Cardoso and Echandi (Cardoso and Echandi, 1987b) reported binucleate Rhizoctonia protected bean seedlings from a virulent root rot-causing isolate of AG4. At least one T. harzianum isolate also lessened disease. In another study (Cardoso and Echandi, 1987a), binucleate Rhizoctonia isolates protected snap bean seedlings from an isolate of AG4 causing root rot by what was deemed a metabolic mechanism of protection. Snap bean seedlings were exposed to the binucleate isolate and then replanted. Replanted seedlings maintained a level of suppression of the pathogen. Root exudates from the binucleate treated seedlings were also inhibitory to the pathogen in vitro. Burpee and Goulty (1984) also reported disease suppression by binucleate Rhizoctonia on brown patch disease caused by R. solani AG2-2 III B on creeping bentgrass. Sumner and Bell (1994) reported a significant efficacy of a binucleate Rhizoctonia AG-2 and T. hamatum against R. solani AG4, and recently Spurlock (2009) found an unidentified sterile white basidiomycete that protected zoysiagrass from R. solani AG2-2.

New project members include researchers with diverse expertise that will work together to address the objectives set from different but complementary perspectives within the context of the phytobiome initiative and IPM, including mycology, microbiology, basic molecular biology, genetics, bioinformatics, population biology, evolutionary biology, metagenomics, metatranscriptomics, plant disease monitoring, spatial analysis, as well as traditional chemical and non-chemical control. The integrated effort of our research will lead to productive collaborations of relevance at the regional and national levels. The results obtained will be reported in peer reviewed scientific journals, specialized disease management journals and on-line publications, and transferred to the broader community (such as growers, educators, academic, and industry collaborators) through extension education, college and graduate level courses, informational web pages, short video segments and fact sheets.
The long-term goals of the proposed multi-state project are to investigate the impact of rhizosphere microbial communities on plant health and on the productivity of diverse cropping systems, and to validate and evaluate different soil-borne disease management strategies under different environmental conditions. In order to coordinate multi-state efforts and provide effective and sustainable recommendations to growers at a regional level with a useful synthesis of our results, the following objectives will be pursued:

Objective 1. Evaluate the biology and diversity of soil-borne pathogens, associated antagonistic microorganisms, and environmental conditions in the context of the whole-system phytobiome. This objective includes traditional, metagenomics, and spatial/temporal methodologies to understand microbial community dynamics that determine soil-borne disease incidence and severity on economically important crops in the U.S.

Objective 2. Evaluate the efficacy of soil-borne disease management strategies (chemical, biorational/biological, cultural) and characterize the associations among microbial community profile, soil physicochemical properties, environmental factors and disease suppression.