Strawberries at the Crossroads: Management of Soilborne Diseases in California Without Methyl Bromide

Abstract

Strawberry production in California has historically been affected by soilborne diseases like Verticillium wilt.
Preplant soil fumigation with methyl bromide (MB) was developed in the late 1950s to combat Verticillium wilt, which was a major limiting factor in strawberry production.
MB fumigation was highly effective, with over 90% of California's commercial strawberry production using the technique.
However, MB was linked to ozone depletion and phased out in 2005, with exemptions until 2016 for strawberry fruit production.
MB use continues in strawberry nurseries under an exemption to prevent the spread of nematodes and diseases on planting stock.
The review examines the impact of the MB phase-out on the California strawberry industry and evaluates the outlook for the industry in the absence of one of the most effective tools for managing soilborne diseases.
New soilborne diseases have emerged, and historically important soilborne diseases have reemerged.
Registration of new fumigants has been difficult, and replacement of MB with a new and effective alternative is unlikely in the foreseeable future.
Crop losses due to soilborne diseases are likely to increase.
Host plant resistance to soilborne diseases has become a top priority for strawberry breeding programs, and cultivars are increasingly selected for their resistance to soilborne diseases.
The intelligent integration of a variety of management tactics is necessary to sustain strawberry production in California.

Introduction

In the late 1950s, methyl bromide (MB) was developed as a preplant soil treatment to control soilborne diseases of strawberry.
Chloropicrin, developed earlier, improved the efficacy and pest spectrum of MB when used in combination.
This combination was widely adopted, saving the California strawberry industry from collapse due to diseases like Verticillium wilt.
The impact of fumigation was so impressive that Ansel Adams captured and named “strawberry fumigation” as one of the most important critical contributions of the first 100 years of the University of California system.
The California strawberry industry grew around fumigation as a cornerstone of the production system.
Fumigation allowed for annual strawberry cultivation without crop rotation.
Breeding programs focused on yield and flavor rather than disease resistance.
The industry was deeply concerned when MB was identified as an ozone depleter in the early 1990s.
A 25-year period of research followed to find effective alternatives to MB.
As of December 2016, MB is no longer used in strawberry fruit production in the United States.
This review reports on the current status of soilborne diseases and their management in California strawberry fruit production post-MB.
The Cal Poly Strawberry Center was formed in 2014 to increase the sustainability of California’s strawberry growers through research and education.

History of California Strawberry Production and MB Benefits

In 1953, Wilhelm and Koch reported that chloropicrin controlled Verticillium wilt, resulting in a twofold increase in yield.
By the late 1950s, mixtures of chloropicrin with MB improved disease control and weed control.
In the 1960s, this mixture became the standard due to its broad spectrum of activity and synergistic effect on Verticillium dahliae control.
The chloropicrin-MB mixture required tarping with polyethylene film to improve efficacy.
Efficient application and tarping equipment were developed, and by 1965, nearly 100% of strawberry land was fumigated prior to each crop.
These breakthroughs led to increased yields and production area.
California strawberry hectares increased from 3,157 in 1966 to a peak of 16,518 in 2013.
Industry-wide yields rose from an average of 14,347 kg/ha in 1956 to 82,630 kg/ha in 2018, a 5.8-fold increase.
Increased yield was attributed to higher-yielding cultivars, improved growing techniques, and fumigation with MB and chloropicrin.
Fumigation also results in plant growth promotion and higher yields even in the absence of soilborne diseases.

MB Phase-Out

Concerns about the environmental impacts of soil fumigants began in the 1980s.
MB was implicated in ozone depletion, reducing $O<em>3$ to $O</em>2$ .
The Montreal Protocol on ‘Substances that Deplete the Ozone Layer’ was drafted in 1987.
In 1990, MB was added to the list of substances that deplete the ozone layer.
The international treaty stipulated that MB production between 1993 and 1998 would be held at the 1991 baseline consumption level of 25,401,173 kg/year.
Reduction requirements:
- 25% reduction by 1999
- 50% reduction by 2001
- 70% reduction by 2003
- 100% reduction by 2005
The Montreal Protocol allows for critical use exemptions (CUE), which were applied for in the United States by the U.S. Environmental Protection Agency (EPA).
Between 2005 and 2016, CUEs were granted to commodities that could justify them, requiring demonstration of minimized critical use and efforts to evaluate alternatives.
CUEs for strawberry fruit ended in December 2016.
The second type of exemption under the Montreal Protocol is quarantine and preshipment (QPS), which authorizes MB use to control the introduction or spread of any new pest within the United States.
MB continues to be used in strawberry nurseries under QPS exemption to prevent the spread of soilborne nematodes and pathogens on nursery stock.

Resurgence and Emergence of Soilborne Diseases

Verticillium wilt was the primary threat to strawberry fruit production and the primary target of early research on fumigation.
As MB phased out, two new diseases emerged: Macrophomina charcoal rot (caused by Macrophomina phaseolina) and Fusarium wilt (caused by Fusarium oxysporum f. sp. fragariae).
Macrophomina charcoal rot was reported in Florida, Israel, Spain, Argentina, Iran, Australia, and Chile.
Fusarium wilt has been reported in Argentina, Australia, China, South Korea, Spain, and Japan.

Responding to the Challenges

In 2000, the USDA created the MB Transition Program to fund research on MB alternatives, awarding $47.3 million to 122 projects.
Considering all MB-related grants along with other federal funding to find MB alternatives, this number would exceed $100 million.
Private industry has spent an estimated $300 million in the same pursuit.
The Methyl Bromide Alternatives Outreach (MBAO) conference was organized to share research results in the area of MB alternatives, meeting annually since 1994.
Major chemical alternatives that have been evaluated are methyl isothiocyanate generators, allyl isothiocyanate (AITC), iodomethane, dimethyl disulfide (DMDS), and ethanedinitrile (EDN).

Chemical Alternatives

Chloropicrin (trichloronitromethane) has been used as a soil fumigant since the 1920s and is still in use.
It is typically formulated with other fumigants to increase the spectrum of activity.
Chloropicrin provides excellent control of some fungal and bacterial pathogens but only fair efficacy against weed seeds and nematodes.
Because of its strong odor and eye irritant properties, it is also used to alert users of poisoning.
As MB use has declined, the use of chloropicrin has increased proportionally and is currently the most widely used fumigant in the California strawberry industry.
Metam sodium (sodium N-methyl dithiocarbamate) and metam potassium (potassium N-methyl dithiocarbamate) produce methyl isothiocyanate (MITC) in soil as they degrade.
MITC has broad-spectrum fumigant activity toward plant pathogenic nematodes, weeds, oomycetes, and fungi.
Disadvantages of metam sodium are its limited mobility in soil and the requirement of mechanical placement or water infiltration for product delivery.
Leaching out of the root zone, volatilization of irritant, and off-odors are potential issues with this fumigant.
Both water caps and plastic films have been used to help address some of the problems.
Disease control efficacy and yield from metam sodium use have been inferior to that of the mixture of MB and chloropicrin.
Another disadvantage of MITC generators is that it reacts with chloropicrin and 1,3-D in aqueous solutions.
One solution currently employed is to make sequential applications with several days of lag time.
Larson (1998) reported that shank applications of chloropicrin followed 2 weeks later by drip application of metam sodium yielded near equivalent production of strawberry to that of an MB and chloropicrin combination.
Due to the difficulty of attaining full activation of metam sodium by water infiltration, without causing phytotoxicity, it is typically utilized with another fumigant at lower rates.
Dazomet is still registered for nonbearing strawberry plants and is used to augment weed and volunteer strawberry plant control.
Fennimore et al. (2008) found that all alternative fumigant treatments controlled weeds to a comparable level as the MB–chloropicrin standard.
Allyl isothiocyanates (AITC) are considered to have the highest fungicidal toxicity on fungal pathogens compared with other isothiocyanates (allyl ITC>phenyl ITC>methyl ITC>ethyl ITC).
AITC fumigant under the trade name Dominus was federally registered in 2013 and available for use in Florida and other strawberry producing states. However, AITC is currently under review in California.
In a field trial conducted in Balm and Dover, Florida, efficacy of AITC in controlling M. phaseolina was compared with standard fumigants chloropicrin and 1,3-D with chloropicrin in tarped beds. Survival of the pathogen was significantly reduced in the AITC treatment in bags of inoculum buried at 7.6 and 20.3 cm deep in the center and 7.6 cm deep in the shoulder of the bed (Baggio et al. 2018).
Another aspect of current research involves combining AITC with other treatments, such as steam (Hoffmann et al. 2017) and crop termination where AITC is applied via drip irrigation to kill a crop quickly and prevent inoculum production in crop residue (Chellemi et al. 2016).
Methyl iodide (iodomethane) has efficacy similar to that of MB, but it is not an ozone-depleting substance.
Researchers at the University of California-Riverside patented the use of methyl iodide as a soil fumigant and then transferred the license to Arysta LifeScience.
The EPA registered methyl iodide in 2008, but it encountered legal challenges to its registration in California leading Arysta to eventually withdraw the product from the market in 2012 citing market disruption and economic limitations as the basis.
Dimethyl disulfide (DMDS) (Paladin) is an MB alternative fumigant that does not deplete ozone.
DMDS alone or in combination with chloropicrin has shown efficacy toward controlling nematodes and soilborne diseases in both France and Italy.
DMDS has registered in the United States in 2010 a very strong odor described as pungent garlic, propane, or decaying fish.
In 2015, Arkema voluntarily withdrew their application for registration of Paladin in California, perhaps due to the risk its pungent odor presents in a more urbanized environment.
Ethanedinitrile (EDN) was first approved as a preplant soil fumigant for both strawberry plant and strawberry fruit production fields in Australia in 2018.
An in vitro study generated EDN dose-response curves against pathogenic fungi, parasitic nematodes, and weeds. The lethal concentration at which 90% of the pathogen propagules are expected die ( $LC_{90}$ ) for F. oxysporum f. sp. fragariae, M. phaseolina, V. dahliae, and Pythium ultimum were 76, 180, 76, and 63 mg/kg of soil for California silt loam soil (pH 5 7.5) and 21, 78, 37, and 32 mg/kg for Florida loamy sand soil (pH 5.6), respectively (Ajwa et al. 2018).
In strawberry field trials conducted at the Gulf Coast Research Education Center and Dover, Florida, EDN applied in water through drip tape at 336, 448, and 560 kg/ha showed higher efficacy in controlling M. phaseolina compared with Paladin-Pic 21EC (dimethyl disulfide 78.1%: chloropicrin 20.9%) at 426 kg/ha and Pic-Clor 60 EC (1,3-D 39.0%: chloropicrin 59.6%) at 280 kg/ha using cultivar Radiance (Thalavaisundaram et al. 2018). EDN along with Pic 100 (chloropicrin 99%), using cultivar Sensation, significantly reduced M. phaseolina CFU compared with EDN or Pic-Clor 60 (Thalavaisundaram et al. 2018).

Low Permeability Films

Currently all strawberry production fields in California use raised beds covered with plastic mulch or film.
Plastic film on raised beds serves several purposes, including optimum hydrothermal soil conditions, weed control and as a barrier between soil and fruit.
Plastic film improves fumigant efficacy against soilborne diseases and limits fumigant emissions by minimizing fumigant escape from volatilization and thereby reduces the amount of fumigant to be applied.
Several types of plastic, from a fumigant permeability aspect, have been studied and are in use including high density polyethylene (HDPE), virtually impermeable film (VIF), and totally impermeable film (TIF).
The difference between traditional single-layer-high-density plastic (HDPE) and VIF or TIF is the presence of at least one gas-impermeable layer (e.g., nylon or polyamines) between polyethylene layers (VIF), or the presence of five layers with two ethylene vinyl alcohol layers (TIF).
TIF has been found to be better than VIF in retaining fumigant, weed suppression, soil pathogen control and improving strawberry yields.
These features have permitted the application of less fumigant while achieving similar efficacy compared with standard 1.25-mil film and reduces regulatory restrictions (e.g., size of buffer zones) on fumigant use.

Nonfumigants Applied Through Drip Irrigation (Fungicides and Microbials)

A variety of conventional and organic products have been evaluated as soil treatments applied through the drip irrigation system and as preplant transplant dips.
These include registered conventional fungicides such as flutriafol (Rhyme), biologicals such as Trichoderma spp. (BioTam), mycorrhizae, Streptomyces-based products, and proprietary mixtures of single or multiple microbial species isolated from the strawberry rhizosphere.
Several controlled environment and a few field studies have shown efficacy of various fungal and bacterial species including Bacillus spp., Serratia spp., and Trichoderma spp. against Fusarium wilt, Verticillium wilt and Phytophthora crown rot, and Macrophomina crown rot.
Most recently, research programs at the University of Florida and Cal Poly San Luis Obispo have evaluated more than 40 products over the course of 8 years without identifying any that deliver consistent performance.
California strawberry growers experience a continuous stream of marketing and sales efforts to use these products without much knowledge or information on their mode of action and efficacy.
Currently, none of these products has gained widespread use.
Mazzola and Freilich (2017) discuss several reasons for the failure of biocontrol products, including inadequate colonization of the host rhizosphere.

Anaerobic Soil Disinfestation

Anaerobic soil disinfestation (ASD) was originally developed in Japan (Shinmura 2000) and in the Netherlands (Blok et al. 2000) independently.
The ASD process involves generation of anaerobic conditions and disinfestation but not sterilization of soil (Butler et al. 2012).
The three main steps of ASD are incorporation of an easily degradable carbon source into soil, irrigation of soil to fill the pore spaces, and covering with an oxygen-impermeable film to generate anaerobic conditions.
The main carbon sources utilized for ASD in strawberry are rice bran, molasses, mustard seed meal, olive pomace, sugar beet vinasse, and composted poultry manure.
The length of incubation has varied from 2 (Hewavitharana et al. 2014) to 15 weeks (Blok et al. 2000).
Mechanisms of disease control have been extensively investigated; various toxic byproducts of anaerobic decomposition, soil microbial and metabolome shifts, formation of specific metal ions such as $Mn^{2+}$ and $Fe^{2+}$ , and the anaerobic environment are the major effects.
No singularly identifiable mechanism has been found, and thus it may be a combination of effects that result in ASD performance.
Compatibility of ASD with use near urbanized areas where buffer zone restrictions would be most stringent for chemical fumigants is an advantage of the technique in California where strawberries are often grown near residential areas.
Shennan et al. (2009) first evaluated ASD in California strawberries. They identified several challenges to adopting the technique on a commercial scale, including optimum incorporation of the carbon source into the soil and the addition of sufficient water to generate the anaerobic conditions required to induce disease suppression.
The main focal point of early ASD research in California was controlling V. dahliae. Using 20 t/ha of rice bran as the carbon source, preplant application of ASD with at least 75 mm of water in sandy-loam and clay-loam soil consistently reduced V. dahliae microsclerotia by 85 to 100% (Shennan et al. 2013, 2014).
At one site, the effect of soil treatments on strawberry yield was assessed with or without preplant fertilizer. When ASD-RB and Pic-Clor 60 were applied with preplant fertilizer, both treatments performed equally. When the treatments were applied without preplant fertilizer, ASD-RB resulted in a higher yield.
Pathogen suppression with ASD-RB at each site was superior to the no-treatment control at all three sites. Successful ASD treatments were consistently associated with altered composition of soil fungal and bacterial communities with induction of specific functional groups of microorganisms.
Marketable strawberry yield in the ASD treatment was either equal to or higher than the Pic-Clor 60 treatment, according to Shennan et al. (2013).
In trials conducted in Florida with composted broiler litter and blackstrap molasses as carbon sources, plant mortality due to M. phaseolina was significantly reduced (1% mortality) compared with the no-treatment control (3% mortality) although complete elimination of plant death was not attained (Shennan et al. 2014).

Limits of ASD

Although success stories regarding soilborne disease suppression in strawberry using ASD have been reported, its adoption has been slow.
One of the main factors hindering adoption has been the cost for implementation. Cost for just tarping soil with VIF plastic was €3,000 (\$3,334.82) per hectarein 2010 (Lamers et al. 2010).Cost for application of ASD with rice bran at 20t ha_1was \$6,000 compared with $4,400 for Pic-Clor 60) in 2014 (Muramoto et al. 2014).
Disease control efficacy of ASD forFusarium wilt has been lower compared with standard soil fumigation with Pic- Clor 60.
Rice bran application in ASD treatment rates as high as 20 t ha_1 caused high nitrogen input into soil.
The ASD process requires multiple steps.
Because the soil microbiome plays a significant role inthe outcome and is affected by many environmental factors, such as soil pH, temperature, soil texture, and incubation duration, the separation of all the optimum factors is a challenge.
For instance, multiple studies have shown that it is critical to complete ASD application before the end of October to maintain soil temperature above 17°C at 15 cm depth in Watsonville and Santa Maria areas to attain successful disease control.
The technique has not been standardized for every unique situation.
Efficacy of ASD has varied based on the application date due to soil temperature and the carbon source utilized. These factors have necessitated regional optimization of ASD.
One of the limitations for adoption of ASD in Florida has been the requirement for replacement of solarization plastic with dark plastic or application of opaque paint to reduce the temperature for optimum plant growth.
Another hindrance identified in vegetable systems in Florida is connected to composted broiler litter as the carbon source. Even though broiler litter has been composted, food safety concerns of Salmonella originating from it have lowered grower’s adoption.

Benefits of ASD

One of the main benefits of ASD is its compatibility with organic production.
Adoption of ASD in the California strawberry industry was approximately 162 ha in 2016 and is currently approximately 800 ha.
In a large-scale organic trial conducted in Oxnard, CA, ASD using rice bran as the carbon source yielded double the fruit production relative to the grower standard and reduced plant death due to M. phaseolina by 10 to 13%.
Recently, growers have been modifying the purpose of ASD from one of disease suppression to fertilization.
There is evidence that rice bran itself can improve the strawberry yield and reduce V. dahliae in soil comparable to ASD with rice bran.
However, application of rice bran without the optimum temperatures and proper anerobic conditions can induce proliferation of F. oxysporum f. sp. fragariae due to its ability to use rice bran as a substrate.

Sanitation

Disease control through sanitation begins by preventing introduction of soilborne pathogens into field soils.
In California, use of disease-, nematode-, and pathogen-free transplants is paramount.
Nurseries in California produce nearly one billion strawberry plants annually.
Strawberry nurseries can use MB under the QPS exemption because of the threat of spreading nematodes and pathogens on planting stock.
Research is ongoing to improve disease detection and management in nurseries.
The benefits of MB fumigation in nurseries (i.e., disease-free plants) outweigh the costs of spreading soilborne pathogens and nematodes to other nurseries and fruit production fields in California and worldwide.
A disease outbreak in a fruit production field is typically very site-specific whereas a disease outbreak in a nursery has the potential to be spread across many fields among several states and even internationally.
The risk of spreading disease on plants is particularly important in California nurseries which supply plants to other nurseries nationally and internationally. Often international phytosanitary regulations require that imported strawberry plants be grown in soil fumigated with MB to reduce the likelihood of spreading nematodes and diseases.
Furthermore, the amount of MB used in California nurseries represents ap- proximately 10% of the total use prior to the phase-out.
Sanitation also includes preventing field-to-field movement of soil via farm equipment.
Nonetheless, soil movement among fields should be minimized, and the benefits will be proportional to the reduction in soil movement, especially where fields with known soilborne pathogen infestations are involved.

Steam

Steam is an effective means of soil disinfestation and has been used for decades to control soilborne pests in greenhouse soils and potting mixes.
Adapting steam treatment to production fields is challenging because of the requirement for a machine that can introduce steam into field soils at the proper temperature and duration.
Effective treatment requires a temperature of 65°C for 20 to 30 min, making speed of treatment a limiting factor.
Current soil steaming rigs can treat 0.25 ha/10 h at a cost of $12,000/ha which currently is generally cost- and time-prohibitive.
The rigs are also quite long, so they work best in large flat fields where there is enough space to turn.
Steaming soils would require no buffer zones, has no restricted entry period, and no plant-back restrictions; these benefits could become more important as fumigants face increased regulations.

Substrate Production Systems

In parts of Europe, restrictions on soil fumigation combined with pathogen-infested soils and frequent rainfall have pushed strawberry farming to soilless systems.
These range from plastic pots placed on top of raised field beds to table-top production in greenhouses or high plastic high tunnels.
Table-top production has several advantages: the potential elimination of soilborne pathogens and their diseases, ease of harvest, precise control of water and nutrition, and protection from rain and intense sunlight.
However, this growing technique has not been widely adopted in California, and with the increased production costs, table-top production has been adopted on approximately 40 ha.
The California Strawberry Commission conducted five years of research on raised bed trough substrate production as a means of managing soilborne diseases.
In this system, a standard field bed is made with a trough(s) running down the bed. The trough is lined with landscaping fabric, filled with substrate (peat or coconut coir) and the entire bed covered with standard plastic mulch.
Strawberries are planted, grown and maintained just like conventional production, but with greater attention to water and nutrient needs (generally requiring a precision fertigation system).
Legard and Thomas (2015) and Wang et al. (2016) concluded that although the raised bed trough production system was commercially possible for conventional production of strawberry fruit, it is not currently economically viable (increase cost of $8,000 to $19,000/ha), sufficiently free of risk of soilborne disease problems, or easy for California strawberry growers to adopt due the high level of technical expertise needed to successfully operate substrate production systems.

Host Plant Resistance

After the phase out of MB, use of genetic resistance to control soilborne diseases became more attractive.
The recently completed octoploid strawberry genome enables us to analyze disease resistance genetics in strawberries.
Resistance to Verticillium wilt in strawberry is quantitative and under complex control of multiple genes.
Chalavi et al. (2003) transferred the chitinase gene (Pcht28) from Lycopersicon chilense to the strawberry cultivar Joliet in Canada and made it resistant to V. dahliae.
Perez-Jiménez et al. (2012) evaluated nine strawberry cultivars for resistance to V. dahliae in growth chambers and 10 cultivars for Phytophthora cactorum in the greenhouse. Results showed that, area under disease progress curve (AUDPC) of cultivar Sabrosa was not significantly different from the resistant control for both P. cactorum and V. dahliae.
These QTLs are valuable resources that could facilitate marker assisted selection to transfer Verticillium wilt resistance into new breeding lines.
Holmes et al. (2017) showed a wide range of susceptibility among 90 strawberry cultivars and elite breeding lines using a naturally infested field site.
In one study, eleven strawberry cultivars were inoculated using M. phaseolina-colonized oat seed in the greenhouse and using a sclerotial suspension in growth chambers to screen for resistance to this pathogen. Results showed that ‘Festival’, ‘Amiga’, and ‘Naiad’ were resistant by both methods.
In order to increase the level of resistance to M. phaseolina in strawberry plants, Hussein et al. (2016) applied artificial elicitors jasmonic acid (JA) and salicylic acid (SA) along with M. phaseolina at a concentration of 1 × 106 spores/ml in strawberry cell culture. The results showed that, because of JA and SA application the transcription factor Fa WRKY 1, which is a homolog to At WRKY75 in Arabidopsis and plays an important role as a positive regulator of the defense system, was induced in strawberry plants.
Using a naturally infested field site, Holmes et al. (2017) showed that F. oxysporum f. sp. fragariae resistance performs very well under field conditions and is an effective means of controlling this disease.
Cultivar screening done in Europe showed the importance of the plant’s genetic background. Those cultivars that showed resistance had at least one resistant parent (Eikemo et al. 2003).
Mangandi et al. (2017) performed a QTL analysis that covered 21.0 Morgans (28 LG) using two multiparental population sets with Markov Chain Monte Carlo- based Bayesian analysis and FlexQTL software. A major QTL was found on LG 7D at position 63 cM. It was named FaRPc2 and explained 20% of the phenotypic variation.
Host plant resistance holds great potential for managing soilborne diseases.
All major strawberry breeding programs have made soilborne disease resistance a top priority.

Progress Toward Systems-Based Approaches

Crop rotation is a classic method of soilborne disease management adopted in strawberry production.
Integrated management of pathogens involves multiple practices that are intended to produce long-term effects on pathogen and disease reduction.
One example of integrated management of Verticillium wilt of strawberry, especially in organic production systems, would be crop rotation to reduce the overwintering inoculum level in the soil.
Starting from the mid-1990s, rotation with broccoli has been shown to reduce Verticillium wilt in strawberry in conventional production.
They found that pathogen densities in broccoli rotation on conventional plots decreased by 44% in both years of assessment. In organic production, V. dahliae density was reduced 45% in the first year and 25% in the second year in broccoli rotation.
Lettuce-strawberry rotations must be avoided in the absence of preplant soil fumigation due to the danger of increasing Verticillium wilt incidence.
Soil amendments have been used in agriculture for millennia.
The primary goals behind utilization of soil amendments are to shift the soil microbiome toward one that is suppressive to soilborne pathogens, to alter soil structure, or to change chemical properties to optimum levels.
Brassicaceae crops such as broccoli produce glucosinolates that generate AITC, which are toxic to fungal pathogens upon hydrolysis by the enzyme myrosinase.
However, broccoli rotation and incorporation of crop residues after removing the marketable crop itself has not provided sufficient control of Verticillium wilt in the following strawberry crop.
Another soil amendment utilized for soilborne disease manage- ment is chitin derived from byproducts of the seafood industry, such as crab, lobster, and shrimp shells.
In California’s Central Coast, application of compost every 1 to 2 years at 4.4 to 6.6 mt/ha in conventional production and 15.5 to 24.4 mt/ha in organic production is a common practice.
Amended soil harbored more antifungal antagonists than unamended soils did and composed up to 8.9% of all the bacterial sequences in the broccoli plus chitin treatment.
Crop termination is used to reduce inoculum build-up and dissemination due to tillage of infected strawberry plants after harvest when the field is prepared for the next season.
Published literature on crop termination of strawberry is very limited.
Khatri et al. (2018) used metam sodium as a crop-terminating chemistry against M. phaseolina in a field study conducted at an experimental research site in Balm, Florida. All treatments resulted in 100% crop mortality at 14 days after fumigation.
Chellemi et al. (2016) suggested a systems-based approach for managing soilborne plant pathogens using four pillars: (i) avoid introducing and disseminating pathogens into the cropping system, (ii) reduce the pathogen population using natural feedback mechanisms, (iii) introduce activities to the cropping system to promote disease-suppressive soil microbiomes, and (iv) incorporate more integrated approaches rather than using pesticides.
Additional long-term research conducted at multiple sites and dissemination of the results to growers are needed to enhance adoption of overarching methods such as a systems-based approach to mitigate soilborne diseases of strawberry.

Conclusions and Prospects for the Future

The phase-out of MB has resulted in an increased use of other fumigants, especially chloropicrin and 1,3-D.
Registration of new fumigants is very difficult, and none are as effective as MB.
Increasing regulatory pressure to reduce the use of fumigants in California is likely.
A single treatment or tactic is unlikely to be as effective as MB.
The number of soilborne fungal diseases affecting strawberries has increased to include Macrophomina crown rot and Fusarium wilt, while losses due to all soilborne diseases are increasing.
Host plant resistance holds great promise for managing soilborne diseases and this has become a top priority for all strawberry breeding programs worldwide.
New growing systems (e.g., table-top production) may offer solutions to soilborne diseases by eliminating soil while providing improved conditions for workers.
Strawberries as an important specialty crop in California will likely survive.
We will use an increasing variety of management tactics, which, if integrated intelligently, will allow strawberry production to continue indefinitely in California and beyond.