While the recently detected charcoal rot disease (caused by the soilborne fungus Macrophomina phaseolina) was causing collapse of strawberry plants from various parts of California, a second soilborne issue was simultaneously affecting other fields. Fusarium wilt was first confirmed on California strawberry in 2006. Initially found in Ventura County, Fusarium wilt is now present on strawberry in Santa Barbara and Monterey counties. The spread of Fusarium wilt in the state, along with the increasing problems with Macrophomina, poses long term threats to the strawberry industry which at present does not have satisfactory plant resistance to both of these pathogens and which is facing a changing future without traditional fumigant products.

Symptoms of Fusarium wilt in strawberry consist of wilting of foliage, plant stunting, and drying and death of foliage (Figure 1). When plant crowns are cut open, internal vascular and cortex tissues are dark to orange brown (Figure 2). Disease is often most severe if the infected plant is subject to stresses such as weather extremes, water stress (shortage of water), poor soil conditions, or heavy fruit loads. In locations where the disease has occurred for more than one season, the patches can be quite large and appear to have spread from the initial problem area (Figure 3). Such patterns are consistent with the spread of a soilborne pathogen. It is noteworthy that in these cases we have never isolated other important, well known pathogens such as Colletotrichum, Phytophthora, or Verticillium. However, it is important to note that Fusarium wilt symptoms are virtually identical to those caused by charcoal rot. To complicate matters further, in some fields we have found both Fusarium and Macrophomina infecting the same crop. This overlap of symptoms means that growers and field personnel should have plants tested by a pathology lab in order to confirm which soilborne disease they are encountering.

Fusarium wilt is caused by the fungus Fusarium oxysporum f. sp. fragariae. This pathogen is host specific to strawberry and can only infect this crop. The fungus survives in the soil for long periods by producing resilient, microscopic structures called chlamydospores (Figure 4). The development of Fusarium wilt has also been associated with changes in the practices of pre-plant soil fumigation. The fungus is spread within and between fields mostly by the transport of contaminated soil during soil tillage and preparation operations. 

Current management strategies involve the following: (1) Crop rotation. Do not plant strawberry in fields having a known history of the problem and avoid back-to-back strawberry plantings in infested locations. (2) Pre-plant fumigation. This remains a useful tool for managing Fusarium and the other soilborne pests, even though bed-applied fumigants may not provide complete control. (3) Avoid stressing the plants. Stress will hasten the development and increase the severity of symptoms, so use appropriate growing and irrigation practices to reduce stress. Note, however, that even in the absence of stress, infected plants will eventually develop the disease. (4) Sanitation. Growers with Fusarium infested fields need to be concerned with limiting the spread of the fungus from infested to clean fields.

Beginning at least as early as 2005 and continuing through 2013, collapsing strawberry plants from various parts of California have been associated with the soilborne fungus Macrophomina phaseolina. The disease, called charcoal rot, appears to be the most important current concern for the industry due to its steady increase over this period of time. Each year finds additional new fields infested, and the disease has now been found in all of the major strawberry producing counties in the state. In 2005-2006, charcoal rot was restricted to southern California in Orange and Ventura counties. Most recently this disease has been confirmed in Santa Barbara, Monterey, Santa Cruz, and Santa Clara counties. The spread of Macrophomina to new fields and counties portends that charcoal rot may be a long term threat to the industry which at present does not have satisfactory plant resistance with which to combat the pathogen.

Symptoms of Macrophomina infection in strawberry consist of wilting of foliage, plant stunting, and drying and death of older leaves, with the central youngest leaves often remaining green and alive. Plants can eventually collapse and die (Figure 1). When plant crowns are cut open, internal vascular and cortex tissues are dark to orange brown (Figure 2). Disease is often most severe if the infected plant is subject to stresses such as weather extremes, water stress (shortage of water), poor soil conditions, or heavy fruit loads. In locations where the disease has occurred for more than one season, the patches can be quite large and appear to have spread from the initial problem area (Figure 3). Such patterns are consistent with the spread of a soilborne pathogen. It is noteworthy that in these cases we have never isolated other important, well known pathogens such as Colletotrichum, Phytophthora, or Verticillium. However, it is important to note that another recently described disease, Fusarium wilt, is also occurring in the same regions; symptoms of Fusarium wilt are identical to those caused by charcoal rot.

Macrophomina produces numerous tiny, black, irregularly shaped microsclerotia (Figure 4). These microsclerotia are survival structures that allow the fungus to persist for extended periods in the soil. The fungus is spread within and between fields mostly by the transport of contaminated soil during soil tillage and preparation operations. Spread of Macrophomina in strawberry fields deals with the same issue of field sanitation that concerns growers of many other commodities. Verticillium wilt (lettuce, strawberry, pepper), clubroot (broccoli, cauliflower), Fusarium wilt (lettuce), Fusarium yellows (celery), and lettuce dieback disease (lettuce) are all problems caused by soilborne pathogens that are spread in infested soil.

Current management strategies involve the following: (1) Crop rotation. Do not plant strawberry in fields having a known history of the problem and avoid back-to-back strawberry plantings in infested locations. (2) Pre-plant fumigation. This remains a useful tool for managing Macrophomina and the other soilborne pests, even though bed-applied fumigants may not provide complete control. (3) Avoid stressing the plants. Stress will hasten the development and increase the severity of symptoms, so use appropriate growing and irrigation practices to reduce stress. Note, however, that even in the absence of stress, infected plants will eventually develop the disease. (4) Sanitation. Growers with Macrophomina infested fields need to be concerned with limiting the spread of the fungus from infested to clean fields.

Verticillium wilt continues to be one of the most potentially damaging diseases caused by soilborne pathogens in strawberries grown in California.  Historically Verticillium was the primary target against which soil pathogen mitigation, i.e. pre-plant soil fumigation, avoidance and crop rotation, and breeding for plant resistance, in strawberries was been directed.

Verticillium wilt symptoms: Early symptoms consist of stunting, delayed development, and the yellowing of lower leaves. As disease progresses the older leaves wilt, dry up, and become brown; typically the younger, central leaves of the plant remain green until the plant dies and all foliage turns brown (Figure 1). In contrast to Verticillium wilt of other crops such as lettuce, vascular discoloration in strawberry crowns may be subtle or absent (Figure 2). Strawberry disease symptoms can be accentuated if the infected plant is subject to stress such as from environmental extremes or mite infestations.

The Pathogen: Verticillium wilt in strawberry is caused by Verticillium dahliae. The host range of this pathogen is quite broad, though in recent years researchers have found sub-groups within V. dahliae that have preferred hosts and therefore narrower host ranges.  For strawberry growers, they should be aware that the Verticillium isolates that infect lettuce and artichoke also infect strawberry. Likewise, the strawberry isolates of Verticillium can infect lettuce and artichoke.  Verticillium gets its name from the whorls of spore-bearing branches (phialides) that are visible when the fungus is viewed under a light microscope (Figure 3).

Verticillium forms a survival structure, the microsclerotium, which allows the pathogen to survive unfavorable conditions and persist between host crops (Figure 4). Microsclerotia are dense masses of thick, dark (melanized) cells that form inside host tissues and are released into the soil when crop residues break down and decay. Researchers have developed methods for measuring the population of viable microsclerotia in soils; such measurements (microsclerotia per gram of soil [ms/gram]) can give growers and others an estimate of potential threat to strawberry plantings. Strawberry has a very low threshold tolerance for Verticillium. A soil test result of 3 ms/gram likely indicates that some disease may develop on the subsequent strawberry crop. With a soil test result of 10 or more ms/gram, strawberry should probably not be planted unless soil fumigation is planned. The picture below is of a field with an average of 30 ms/gram at the end of July (Figure 5).

Disease Development: Verticillium microsclerotia germinate in the soil when activated by exudates from the host plant roots.  Once penetrating the plant root, the fungus grows up into the xylem (the water conducting elements of the plant), degrading the cell walls and most likely releasing toxins. This type of colonization is called a systemic infection. Systemic infections interfere with the plant’s ability to conduct water. For this reason, infected strawberry plants will wilt during times of high water demand, such as during hot and dry weather, if the plant is improperly (too dry) irrigated, or if bearing a heavy fruit load. Diseased plants that show some dieback symptoms may recover if the stress conditions subside; however, such plants are not likely to be as productive as unaffected, healthy plants.

The pattern and distribution of Verticillium wilt disease in the field can be extremely variable and does not necessarily correspond with low spots, heavy soil, or improperly irrigated areas. In contrast, such field conditions may correspond with patterns of Phytophthora crown rot. Instead, many times Verticillium wilt affected plants can be found distributed all over the field, perhaps as individual plants or as patches of affected plants.

Managing Verticillium in Strawberry:

Plant Breeding for Resistance: Strawberry plants genetically resistant to V. dahliae are not yet available commercially. However, resistance should play a big role in the future mitigation of Verticillium wilt in strawberry, though development of completely resistant cultivars has not been easily attained. In a research report (California Agriculture, January/March 2010), it is pointed out that intensive selection for Verticillium resistance resulted in a few genotypes that demonstrated a great amount of resistance when inoculated with the pathogen; however, these selections suffered some yield loss under intense disease pressure.  Furthermore, these highly resistant genotypes all expressed “substantial deficiencies for horticultural or productivity traits,” meaning they weren’t producing the quantity or quality of fruit that we have come to expect in California.

Even so, the University of California strawberry breeding program has made significant advances in improving genetic resistance to Verticillium.   Starting in the late 1980s, less than 40% of the genotypes used in the UC breeding program had moderate tolerance to V. dahliae; twenty years later, between 80 and 100% of the genotypes used had such tolerance.

Soil treatments: Soil fumigation with a mix of methyl bromide and chloropicrin is usually recommended for conventional growers, but this plan of action is becoming quite expensive if not impossible under new regulations and limitations.  Chloropicrin used alone is successful in disinfesting soils of Verticillium, as are mixes of 1,3 – Dichloropropene and chloropicrin (Telone C-35) but generally none of these have been shown to be as effective as methyl bromide and chloropicrin used together in clearing a soil of Verticillium pathogen.

An alternative soil treatment being tested and demonstrated in several commercial fields is anaerobic soil disinfestation (ASD).  ASD works by inducing an anaerobic (oxygen-less) condition in soils that are amended with a carbon source. The resulting proliferation of oxygen-consuming microbes shifts the soil ecology and microbial diversity, resulting in suppression of pathogenic organisms. Researchers are continuing to develop and fine-tune this method.

Biofumigation is another soil treatment that can reduce Verticillium numbers in the soil. Broccoli crop residues release chemicals that both directly reduce Verticillium propagules as well as affecting the soil microbial diversity, which can suppress the pathogen. While mustards and other cruciferous plants show similar effects, broccoli appears to be one of the best choices for this soil biofumigation treatment. A crop rotation that includes broccoli will have the same suppressive effect, since the harvested broccoli florets are not needed for biofumigation to take place.

Sanitation: Being a soilborne pathogen, V. dahliae is readily spread between fields in mud and dirt adhering to equipment and vehicles. Growers should therefore beware of moving contaminated equipment from infested fields into “clean” fields. Because diseased strawberry plants are infested with microsclerotia, strawberry crop residues should not be moved into other fields.

Crop rotation: Crop rotation is a key IPM practice that will help lessen the threat from Verticillium wilt. Consecutive, back-to-back plantings of strawberry is a risky practice if the field has a history of Verticillium wilt and if effective fumigants are not used.  Fields which have been recently planted to lettuce, artichoke, and Solanaceous family crops (potatoes, eggplants, and tomatoes) should likewise be avoided if Verticillium wilt has occurred and if soil fumigation is not implemented. Weeds that are hosts of V. dahliae may not play a critical role in disease development but should be controlled in any case.

Other alternatives: Another experimental alternative to chemical control is the use of organic substrates, such as coconut peels (coir) or peat moss, which are used as the rooting medium in place of the soil but are kept completely separate from the soil by cloth barriers. The substrates are poured into cloth-lined furrows that are constructed into the beds. The intent of this approach is to create a pathogen-free zone above the field soil. This method is still being tested.

Finally, there are a series of commercially available biological fungicides which purport to competitively exclude pathogenic fungi such as Verticillium from the surface of the root, or which produce toxins inhibitory to pathogen growth.   These materials likewise still require research and demonstration of efficacy under field conditions.

The above has been a discussion the biology and management of Verticillium wilt disease in strawberry.  There are pesticides mentioned for the management of Verticillium in this article.  Before using any of these products, check with your local Agricultural Commissioner’s office and consult product labels for current status of product registration, restrictions, and use information.

(The authors thank K. V. Subbarao for assistance with this report.)

References:

California Agriculture, Jan/Mar 2010. http://californiaagriculture.ucanr.org/landingpage.cfm?article=ca.v064n01p37&fulltext=yes

UC IPM Online, strawberry Verticillium wilt. http://www.ipm.ucdavis.edu/PMG/r734100811.html

UC IPM, Guia para el manejo de las plagas, Fresas. http://www.ipm.ucdavis.edu/PDF/PMG/pmgstrawberry_espanol.pdf

A cover crop can be a useful way to prevent weeds in anchor rows.

Cover crops in anchor rows can suppress weed growth and additionally help to minimize soil erosion and nutrient and sediment loss when it rains. Densely planted cover crops can outcompete weed seedlings germinating from the soil and prevent wind-dispersed seeds from reaching the wet soil surface. Have a look at the newly revised weed section in the Caneberries Pest Management Guidelines on the UC IPM web site. 

As readers know, tunnels used for caneberry cultivation have the advantage that even when it rains caneberries remain dry which helps with fruit quality and yield. However, during rains, the water drains from the plastic cover of the tunnel and down into rows that contain the anchoring posts of the tunnel structure. The accelerated runoff in these post rows can cause soil erosion, sediment and nutrient loss. As such, the persistent soil moisture in post rows also promotes weed growth.  These weeds, while maybe not competing directly with canes, can reproduce and quickly spread into neighboring cane rows.

Cover crops in the anchor rows are especially helpful when managing weeds that are difficult to control with fumigation because of their hard impermeable seed coats (mallows and filaree), or that have developed resistance to herbicides such as glyphosate and paraquat (hairy fleabane and horseweed).

Cover crops can be managed with mowing or herbicides to avoid seed production.