Healthy strawberry plant (left) and strawberry plant infected with verticillium wilt (right), photo by Howard F. Schwartz, Colorado State University, Bugwood.org

Verticillium wilt is a wilt disease affecting over 350 species of eudicot plants. It is caused by six species of Verticillium fungi: V. dahliae, V. albo-atrum, V. longisporum, V. nubilum, V. theobromae and V. tricorpus.^[1] Many economically important plants are susceptible including cotton, tomatoes, potatoes, oilseed rape, eggplants, peppers and ornamentals, as well as others in natural vegetation communities. Many eudicot species and cultivars are resistant to the disease and all monocots, gymnosperms and ferns are immune.

Signs are superficially similar to Fusarium wilts. There are no fungicides characterized for the control of this disease but soil fumigation with chloropicrin has been proven successful in dramatically reducing Verticillium wilt in diverse crops such as vegetables using plasticulture production methods, and in non-tarped potato production in North America . Additional strategies to manage the disease include crop rotation, the use of resistant varieties and deep plowing (to accelerate the decomposition of infected plant residue). In recent years, pre-plant soil fumigation with chloropicrin in non-tarped, raised beds has proven to be economically viable and beneficial for reducing wilt disease and increasing yield and quality of potato in North America. Soil fumigation is a specialized practice requiring special permits, equipment, and expertise, so qualified personnel must be employed.

Hosts and symptoms

Verticillium dahliae infected sunflowers, photo by Howard F. Schwartz, Colorado State University, Bugwood.org

Verticillium albo-atrum infected tree crown, USDA Forest Service Archive, USDA Forest Service, Bugwood.org

Verticillium spp. attack a very large host range including more than 350 species of vegetables, fruit trees, flowers, field crops, and shade or forest trees. Most vegetable species have some susceptibility, so it has a very wide host range.^[2] A list of known hosts is at the bottom of this page.

The symptoms are similar to most wilts with a few specifics to Verticillium. Wilt itself is the most common symptom, with wilting of the stem and leaves occurring due to the blockage of the xylem vascular tissues and therefore reduced water and nutrient flow. In small plants and seedlings, Verticillium can quickly kill the plant while in larger, more developed plants the severity can vary. Some times only one side of the plant will appear infected because once in the vascular tissues, the disease migrates mostly upward and not as much radially in the stem.^[3] Other symptoms include stunting, chlorosis or yellowing of the leaves, necrosis or tissue death, and defoliation. Internal vascular tissue discoloration might be visible when the stem is cut.^[2]

In Verticillium, the symptoms and effects will often only be on the lower or outer parts of plants or will be localized to only a few branches of a tree. In older plants, the infection can cause death, but often, especially with trees, the plant will be able to recover, or at least continue living with the infection. The severity of the infection plays a large role in how severe the signs are and how quickly they develop.^[2]

Disease cycle

While Verticillium spp. are very diverse, the basic life cycle of the pathogen is similar across species, except in their survival structures. The survival structures vary by species with V. albo-atrum forming mycelium, V. dahliae forming microsclerotia, V. nigrescens and V. nubilum forming chlamydospores, and V. tricorpus forming all three. While resting, many factors such as soil chemistry, temperature, hydration, micro fauna, and non-host crops all have an effect on the viability of the resting structure. Mycelium have been observed remaining viable for at least 4 years,^[4] while microsclerotia have been observed in fields planted with non-host crops for over 10 years ^[5] and even 15 years has been reported.^[2] Viability is reduced at these extremes, but the long survivability of these structures is an important aspect for Verticillium control.

When roots of a host crop come near the resting structure (about 2mm),^[6] root exudate promotes germination and the fungi grows out of the structure and toward the plant. Being a vascular wilt, it will try to get to the vascular system on the inside of the plant, and therefore must enter the plant. Natural root wounds are the easiest way to enter, and these wounds occur naturally, even in healthy plants because of soil abrasion on roots. Verticillium has also been observed entering roots directly, but these infections rarely make it to the vascular system, especially those that enter through root hairs.^[7]

Once the pathogen enters the host, it makes its way to the vascular system, and specifically the xylem. The fungi can spread as hyphae through the plant, but can also spread as spores. Verticillium produce conidia on conidiophores and once conidia are released in the xylem, they can quickly colonize the plant. Conidia have been observed traveling to the top of cotton plants, 115 cm, 24 hours after initial conidia inoculation, so the spread throughout the plant can occur very quickly.^[8] Sometimes the flow of conidia will be stopped by cross sections of the xylem, and here the conidia will spawn, and the fungal hyphae can overcome the barrier, and then produce more conidia on the other side.^[9]

A heavily infected plant can succumb to the disease and die. As this occurs, the Verticillium will form its survival structures and when the plant dies, its survival structures will be where the plant falls, releasing inoculates into the environment. The survival structures will then wait for a host plant to grow nearby and will start the cycle all over again.

Besides being long lasting in the soil, Verticillium can spread in many ways. The most common way of spreading short distances is through root to root contact within the soil. Roots in natural conditions often have small damages or openings in them that are easily colonized by Verticillium from an infected root nearby. Air borne conidia have been detected and some colonies observed, but mostly the conidia have difficulty developing above ground on healthy plants.^[10] In open channel irrigation, V. dahliae have been found in the irrigation ditches up to a mile from the infected crop.

Without fungicidal seed treatments, infected seeds are easily transported and the disease spread, and Verticillium has been observed remaining viable for at least 13 months on some seeds. Planting infected seed potatoes can also be a source of inoculum to a new field. Finally, insects have also been shown to transmit the disease. Many insects including potato leaf hopper, leaf cutter bees, and aphids have been observed transmitting conidia of Verticillium and because these insects can cause damage to the plant creating an entry for the Verticillium, they can help transmit the disease.^[3]

Environment

While Verticillium wilts often have the same symptoms of Fusarium wilts, Verticillium can survive cold weather and winters much better than Fusarium, which prefers warmer climates. The resting structures of Verticillium are able to survive freezing, thawing, heat shock, dehydration, and many other factors and are quite robust and difficult to get rid of. The one factor they do not tolerate well is extended periods of anaerobic conditions (such as during flooding).^[3]

Verticillium will grow best between 20 and 28 degrees Celsius,^[2] but germination and growth can occur well below (or above) those temperatures. Still, Verticillium will generally not survive in the branches and trunks of infected trees during hot, dry seasons in regions such as summer in southern California. This does not generally "cure" the entire tree, however, and recurrence can happen via a reinfection from the roots during winter and spring.^[11] Water is necessary for resting structure germination, but is not as important for the spread of the fungus as in many other fungi. While not an environmental requirement for the fungus, stressed plants, often brought on by environmental changes, are easier to attack than healthy plants, so any conditions that will stress the plant but not directly harm the Verticillium will be beneficial for Verticillium wilt development.^[3]

Management

Verticillium wilt begins as a mild, local infection, which over a few years will grow in strength as more virile strains of the fungus develop. If left unchecked the disease will become so widespread that the crop will need to be replaced with resistant varieties, or a new crop will need to be planted altogether.^[2]

Control of Verticillium can be achieved by planting disease–free plants in uncontaminated soil, planting resistant varieties, and refraining from planting susceptible crops in areas that have been used repeatedly for solanaceous crops. Soil fumigation can also be used, with chloropicrin being particularly effective in reducing disease incidence in contaminated fields.

In tomato plants, the presence of ethylene during the initial stages of infection inhibits disease development, while in later stages of disease development the same hormone will cause greater wilt. Tomato plants are available that have been engineered with resistant genes that will tolerate the fungus while showing significantly lower signs of wilting.^[2]

Verticillium albo-altrum, Verticilium dahliae and V. longisporum can overwinter as melanized mycelium or microsclerotia within live vegetation or plant debris. As a result, it can be important to clear plant debris to lower the spread of disease. Verticilium dahliae and V. longisporum are able to survive as microsclerotia in soil for up to 15 years.^[2]

Importance

Verticillium wilt occurs in a broad range of hosts but has similar devastating effects on many of these plants. In general, it reduces the quality and quantity of a crop by causing discoloration in tissues, stunting, and premature defoliation and death.^[12] Stock from infested nurseries may be restricted. Once a plant is infected, there is no way to cure it. Verticillium wilt is especially a concern in temperate areas and areas that are irrigated. Verticllium spp. can naturally occur in forest soils and when these soils are cultivated, the pathogen will infect the crop.^[2]

The Salinas Valley in California has had severe problems with Verticillium wilt since 1995, most likely due to flooding in the winter of 1995. Many areas in the Salinas and Pajaro Valleys are unable to grow lettuce due to the high levels of Verticillium dahliae in the soil.^[13] Potatoes grown in Verticillium infested soils may have a reduced yield between 30–50% compared to potatoes grown in "clean" soil. Verticillium wilt has also caused a shift in peppermint cultivation from the Midwest in the mid- to late-1800s to western states such as Oregon, Washington and Idaho, to new, non-infested areas within these states now.^[12]

Lists of plants susceptible or resistant

Replanting susceptible species on the site of a removed plant that has succumbed to V. albo-atrum or V. dahliae is inadvisable because of the heightened risk of infection. Instead, resistant or immune varieties should be used. The following two lists show both susceptible and resistant/immune plants by Latin name.^{[11][14][15][16][17][18]}

(*) indicates that the plant occurs on both lists because different varieties or cultivars vary in their resistance.
(#) indicates that some strains are resistant.
(+) indicates susceptibility to some European strains of Verticillium albo-atrum.

References