Thielaviopsis basicola


Thielaviopsis basicola is the plant-pathogen fungus responsible for black root rot disease. This particular disease has a large host range, affecting woody ornamentals, herbaceous ornamentals, agronomic crops, and even vegetable crops. Examples of susceptible hosts include petunia, pansy, poinsettia, tobacco, cotton, carrot, lettuce, tomato, and others. Symptoms of this disease resemble nutrient deficiency but are truly a result of the decaying root systems of plants. Common symptoms include chlorotic lower foliage, yellowing of plant, stunting or wilting, and black lesions along the roots. The lesions along the roots may appear red at first, getting darker and turning black as the disease progresses. Black root lesions that begin in the middle of a root can also spread further along the roots in either direction. Due to the nature of the pathogen, the disease can easily be identified by the black lesions along the roots, especially when compared to healthy roots. The black lesions that appear along the roots are a result of the formation of chlamydospores, resting spores of the fungus that contribute to its pathogenicity. The chlamydospores are a dark brown-black color and cause the "discoloration" of the roots when they are produced in large amounts.

Environment

As a poor saprophyte and obligate parasite, T. basicola is often dependent upon favorable environmental conditions. Although the pathogen is able to grow in a variety of soil moistures, wet soil is optimal for greater infection since spores are able to move easily in water. Water plays a role in dispersal of spores and can lead to an increased infection rate. Soil temperatures also play an important role, as temperatures between 55 and 65 °F are favorable for the pathogen. However, temperatures that are higher than 86 °F are unfavorable for the fungus and only traces of the pathogen can be found. At lower temperatures, the severity of the disease increases since the temperatures become unfavorable for and induces stress on the hosts. Alkaline clay soils have proven to be conducive to pathogenicity and also favor the pathogen. This can be attributed to the fact that the pathogen is suppressed at soils with pH less than 5.2, so increasing pH is favorable for severity of disease. There are also cultural conditions which may induce stress on the host plants that favor the pathogen including high soluble salts, excessive nitrogen fertilizer, low organic matter, etc. When the plant undergoes stress due to cultural conditions, there is an increase in susceptibility to opportunistic pathogens such as T. basicola. For this reason, it is important to practice proper cultural conditions such as maintaining proper temperatures, amount of nitrogen fertilizer, and pH of the soil to reduce stress of host plants and decrease susceptibility to disease.

Pathogenesis

Thielaviopsis basicola is a soilborne fungus that belongs to the Ascomycota division of the "true fungi" and is a hemibiotrophic parasite. Fungi belonging to Ascomycota are known to produce asexual and sexual spores, however, a sexual stage has yet to be observed and validated in the Thielaviopsis basicola life cycle, which classifies this species as one of the Deuteromycete or an imperfect fungus. During the asexual reproductive cycle of Thielaviopsis basicola, two types of asexual spores are borne from the hyphae including endoconidia and chlamydospores. Endoconidia are a distinctive type of conidium in that they develop within a hollow cavity inside a hyphal tube and are ejected from the end of this tube to disperse. Both of the aforementioned spores must first undergo physical dissemination in order to begin locating an infection court on a new, viable host. Aside from the normal translocation of spores within the soil environment, vectors such as shore flies have been observed carrying and aerially transmitting Thielaviopsis basicola spores, a phenomenon uncharacteristic of soilborne fungal pathogens. Upon landing on an infected plant, the shore flies feed on the infected tissue and ingest spores along with the plant material, only to excrete the hitchhiking spores in their frass, which ultimately lands on healthy plant tissue continuing the disease cycle. However, it is important to note that this association between vector and soilborne fungi has only been observed in commercial agricultural settings in which artificially controlled environments promote conditions that deviate from the natural world.
Following dispersal, the spores will detect an infection site on the host plant and germinate in response to the stimuli produced by the root exudates, some of which include sugars, lecithins, and unsaturated triglycerides. Germ tubes emerge from the spores and directly penetrate into the cells of the root hairs via penetration hyphae. The living host plant will typically respond with the development of cell appositions called papillae, which attempt to block the pathogen from penetrating the cell wall and subsequently parasitizing the host's cells. However, most of these early defense mechanisms prove unsuccessful, hence the significance and prevalence of the disease around the world. Advancing, the vegetative hyphal cells differentiate into feeding structures that resemble haustoria, which absorb nutrients biotrophically from the host cells. Once the pathogen has breached the cell wall of the epidermal root cell, it proceeds to release effector compounds that disrupt the host's systemic defense mechanisms. Systemic acquired resistance is employed by the host to actively address localized infection and initiate defense signaling cascades throughout the plant. For example, the SAR NPR1 gene is of special importance and acts to suppress the infection faculties of Thielaviopsis basicola, effectively imparting resistance to some host plants. Furthermore, research suggests that the NPR1 gene, when over-expressed in transgenic plants, aids in the expression of other defense-related genes such as PR1, effectively improving resistance to infection by Thielaviopsis basicola. ''NPR1 and its associated benefits for enhancing disease resistance have been recognized as possible tools to use when equipping economically indispensable crops with transgenic resistance to disease.
Once penetration and the establishment of biotrophic feeding structures are successful, the pathogen progresses into the root tissue leaving distinctive black/brown lesions in its wake ; it continues proliferating until eventually entering its necrotrophic stage. Hemibiotrophs, like
Thielaviopsis basicola, transition from a biotrophic stage to a necrotrophic stage by way of a coordinated effort between different pathogenesis genes that secrete effector proteins capable of manipulating their host's defense system. Research suggests that during biotrophy, certain types of effectors from the pathogen are expressed over others and vice versa during the necrotrophic stage. Once the biotrophic stage is no longer preferred by the pathogen, it will initiate this complicated genetic transition and commence the necrotrophic stage. In order to digest and metabolize nutritive compounds from a necrotic host plant, Thielaviopsis basicola secretes enzymes such as xylanase and other hemicellulases, which break down cell tissues making them available to the fungus. During this stage, the pathogen also produces its asexual spores in the lesions to reproduce and disseminate more propagules for continued survival in the soil. In addition to its normal infection process, studies have shown that Thielaviopsis basicola and its pathogenesis are synergistically linked to a fortuitous coinfection process involving Meloidogyne incognita nematodes when the two are present in the same soil. It has been observed that the infection of host tissues by Meloidogyne incognita facilitates the infection of Thielaviopsis basicola'' into the root and vascular tissues, effectively allowing the fungal pathogen to optimize infection even when environmental conditions are suboptimal.

Importance

Thielaviopsis basicola was discovered in the mid-1800s and has remained an important plant pathogen affecting ornamental and agricultural plants in over 31 countries around the world. The pathogen is known to stunt or delay maturity in the species it parasitizes, which, coupled with environmental limitations, can lead to severe economic losses. It has been observed that black root rot can delay plant maturity for up to a month and result in over a 40% yield reduction in the affected crop. One crop that is affected by Thielaviopsis basicola and that is of significant economic importance is cotton. In the United States alone, between the years 1995 and 2005, the total annual loss in revenue due to diseases in the cotton crop was $897 million. Thielaviopsis basicola was a significant contributor to that economic loss. In other parts of the world, such as in major cotton producer Australia, Thielaviopsis basicola has a very severe economic impact as well. In Australia, the disease was initially observed in sweet peas in the 1930s. However, black root rot spread to a range of cultivated hosts, especially into Australian cotton production. In fact, surveys taken in 2010 and 2011 of Australian agriculture statistics reported black root rot to be present in 93% of farms and 83% of fields studied. Of the fields affected, yield losses have reached 1.5 bales per acre. The national average of cotton production per hectare in Australia is about 10 bales, so a loss of 1.5 bales per acre to black root rot adds up to a significant loss. In addition to cotton, carrot, lupin, cabbage, clover, and tobacco are all crops cultivated in many different countries that suffer from black root rot. Some important ornamental crops affected by black root rot include: Begonia sp. Daphne ''cneorum,'' poinsettia, African daisy, pansy, marigold, and petunia; the list is quite extensive. However, cultural practices have led to the eradication of this disease in many ornamental crops, including poinsettia. During the 1950s and 1960s, poinsettia production was ravaged by black root rot disease. Despite faltering, once the use of soil mixes was traded for soilless alternatives throughout the floriculture industry, black root rot was no longer a threat to poinsettias. Thielaviopsis basicola has been and will remain a significant threat to crops grown globally in both agricultural and horticultural systems.