Thecaphora frezii (peanut smut)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Latitude/Altitude Ranges
- Air Temperature
- Means of Movement and Dispersal
- Seedborne Aspects
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Impact Summary
- Economic Impact
- Social Impact
- Risk and Impact Factors
- Detection and Inspection
- Prevention and Control
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Thecaphora frezii Carranza & J.C. Lindq.
Preferred Common Name
- peanut smut
International Common Names
- Spanish: carbón del maní
- Portuguese: carvão do amendoim
Summary of InvasivenessTop of page
Thecaphora frezii is the causal agent of peanut smut. The disease was first reported in 1962 in wild peanuts from Aquidauana, Mato Grosso do Sul, Brazil. It was first detected in commercial crops in 1995 in the central-northern area of Córdoba province, Argentina. The prevalence of peanut smut has gradually increased. In the 2011/12 growing season, the disease was found in all production fields in Córdoba province and, two years later, it was found in all peanut production areas of Argentina. The increase in the intensity of peanut smut in Argentina has been accompanied by increasing yield losses.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Ustilaginomycotina
- Class: Ustilaginomycetes
- Order: Urocystidiales
- Family: Glomosporiaceae
- Genus: Thecaphora
- Species: Thecaphora frezii
Notes on Taxonomy and NomenclatureTop of page
Carranza and Lindquist (1962) classified T. frezii on the basis of disease symptoms and morphology of teliospores, but could not complete Koch’s postulates because artificial inoculations were not possible. Conforto et al. (2012) confirmed the original classification using molecular techniques.
DescriptionTop of page
In culture (PDA medium, 39 g/l), colonies are circular-radial, flat, greyish-brown and have a growth rate of 5.3 mm/day at 25 ± 1°C in the dark (Astiz Gassó and Marinelii, 2003; 2013). The mycelium is branched and septate, typical of basidiomycetes. Teliospores are reddish brown and can differ in size depending on the number of cells. A single cell spore is 20 μm, whereas spores composed of eight cells can be 50 μm in size (Marraro Acuña et al., 2013; Rago et al., 2017).
DistributionTop of page
Peanut smut is present in Argentina, Bolivia and Brazil. Argentina is the only country where the disease has been reported in commercial crops. In 1995, it was reported in the central-northern area of Córdoba province, Argentina (Pampayasta, Villa Ascasubi and Ticino) (Marinelli et al., 1995). Bolivia and Brazil only have reported cases of smut in wild peanuts (Carranza and Lindquist, 1962; Soave et al., 2014).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Argentina||Widespread||Introduced||1995||Invasive||Marinelli et al., 1995||First record in Córdoba province|
|Bolivia||Present||Soave et al., 2014||Present in wild peanut|
|Brazil||Present||Present based on regional distribution|
|-Mato Grosso do Sul||Present||Carranza and Lindquist, 1962||Present in wild peanut|
Risk of IntroductionTop of page
Argentina is the leading exporter of edible grain and crushed peanut products (e.g. flour, butter and oil) worldwide (Fernandez and Giayetto, 2006; Fiant et al., 2013). More than 80% of Argentinian production is exported to Europe (mainly the Netherlands, Germany, UK, Spain, Italy, Greece and France) and other countries such as the USA, Canada, China and India. The pathogen could be dispersed to other continents through the export of infected seeds (Marraro Acuña and Haro, 2011).
Hosts/Species AffectedTop of page
Arachis is the only host reported for T. frezii (Rago et al., 2017). The disease has been reported in commercial peanut crops in Argentina, but only occurs in wild peanuts in Brazil and Bolivia (Carranza and Lindquist, 1962; Soave et al., 2014). All of the peanut cultivars that are widely planted in Argentina are susceptible (Cignetti et al., 2010a).
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page Fruiting stage
SymptomsTop of page
Infection is localized and infected plants do not exhibit aerial symptoms. Affected pods exhibit hypertrophy and have a spongy consistency, and kernels can be replaced, partially or totally, by a reddish-brown mass of spores.
List of Symptoms/SignsTop of page
|Fruit / abnormal shape|
|Fruit / lesions: on pods|
|Seeds / distortion|
|Seeds / lesions on seeds|
Biology and EcologyTop of page
There are few genetic studies on T. frezii. Conforto et al. (2012) sequenced the D1/D2 region of the large ribosomal subunit (28S rDNA) of four specimens from different production regions in Argentina. The sequences are available in NCBI (National Center of Biotechnology Information). Cazón et al. (2016b) sequenced the ITS region of different isolates to develop a diagnostic PCR method.
T. frezii produces teliospores that can survive in a metabolically dormant state in the soil without the presence of live hosts. When peanut pegs penetrate the soil, their exudates disrupt telial dormancy, which promotes spore germination and initiates local infections (Astiz Gassó and Marinelli, 2003; Marinelli et al., 2008). According to Marraro Acuña et al. (2013), infection occurs during the peanut pegging process (40 days post-planting). The process of teliospore germination includes the formation of a probasidium, followed by a basidium that forms basidiospores through meiosis. When basidiospores germinate, compatible haploid germ tubes fuse and produce a dikaryotic mycelium, which is responsible for infection. The dikaryotic mycelium can penetrate the peanut gynophore in the soil, colonize the tissues and replace the cells with reddish-brown teliospores (Marinelli et al., 2010; Astiz Gassó and Wojszko, 2011; Astiz Gassó and Marinelli, 2013). During the shelling process, teliospores are released and deposited in the soil.
Peanut smut is considered a monocyclic disease because there is no secondary inoculum produced during the growing season, and polyetic because the annual accumulation of inoculum affects subsequent seasons. The intensity of an epidemic is correlated with the initial amount of inoculum produced in the preceding growing seasons. The number of T. frezii teliospores increases in the soil due to the following factors: 1) closeness to peanut processing factories; 2) number of years of peanut cultivation in the region; and 3) cropping patterns, with back-to-back peanuts producing higher smut severity than rotations with other crops.
Paredes et al. (2016) surveyed peanut smut in the peanut production area of Córdoba, Argentina. Disease intensity was shown to decrease southwards. This gradient occurs because the new production areas in the south are away from processing plants and have a much shorter history of peanut as a crop than in the north. It is important that management strategies in this region prevent an increase of inoculum in the soil. In northern production areas, where soil infestation levels are high, it is important to use resistant varieties supplemented with technological strategies to maintain resistance.
Cazón et al. (2016a) studied the duration of teliospore survival in soil, observing that the infection capacity of T. frezii teliospores was maintained for at least 4 years in an experimental plot.
Arachis is the only host genus reported for T. frezii. Teliospores germinate in PDA medium prepared with grain broth (Astiz Gassó and Marinelli, 2003).
T. frezii has a great capacity to adapt to different environments. Paredes et al. (2017b) reported that water stress favours infection, but that infection still occurs in humid conditions. In Argentina, the pathogen is distributed throughout the peanut-growing area, and is found in different types of soil and climatic conditions (Cazón et al., 2017).
ClimateTop of page
|Af - Tropical rainforest climate||Tolerated||> 60mm precipitation per month|
|Am - Tropical monsoon climate||Preferred||Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Air TemperatureTop of page
|Parameter||Lower limit||Upper limit|
|Absolute minimum temperature (ºC)||-7.1|
|Mean annual temperature (ºC)||12.1||25.2|
|Mean maximum temperature of hottest month (ºC)||18.1||31.1|
|Mean minimum temperature of coldest month (ºC)||5.5||18.6|
Means of Movement and DispersalTop of page
Teliospores of T. frezii can be dispersed by wind from an infected field to adjacent fields (Marinelli et al., 2010; Rago et al., 2017). This process is favoured during harvest time. The fungus may also be moved by natural dispersal of infested seeds.
The biggest source of inoculum is peanut processing plants. During the shelling process, millions of teliospores are released from affected pods. These teliospores are carried by wind to adjacent fields, which results in fields close to peanut processing plants having a higher incidence of infection with T. frezii.
Teliospores can also be carried by agricultural machinery from infected fields to other provinces or to bordering countries. The pathogen can disperse long distances to different countries or continents through the trade of infected seeds (Marraro Acuña and Haro, 2011). During shelling, teliospores can infest kernels externally or through small lesions, which may not be detected during the seed selection process (Marinelli et al., 2008).
Seedborne AspectsTop of page
Teliospores of T. frezii can contaminate asymptomatic seeds, superficially or through small lesions. The latter contamination is easier to identify. There is no correlation between seed contamination and disease in the same growing season. The infection process occurs during pegging and is generally due to the accumulation of inoculum from previous seasons (Rago et al., 2017).
Effect on Seed Quality
T. frezii significantly affects seed quality and quantity. In severely affected plots, the number of seeds can be reduced by 50% (Oddino et al., 2010). Partially affected seeds can be of different size and shape, which interferes with conditioning and planting, as well as with germination in the field (Cazón, 2015).
The spread of T. frezii through seeds went unnoticed for many years, partly because there were no symptoms on the aerial parts of the plants. In the mid-1990s, there was an increase in the scale of peanut production in Argentina, which favoured large companies able to afford large-scale, modern processing techniques. Many small- and medium-sized growers (planting <200 ha), who used to harvest their own seeds, were removed from the production system. The larger growers produced and processed peanuts on a larger scale, which included both healthy and diseased fields. This approach has favoured seed contamination and the spread of the pathogen (Fernandez and Giayetto, 2006; Rago et al., 2017).
Growers use fungicide seed treatments with polymers to protect against pathogens that cause pre- and post- emergence damping-off. However, T. frezii can infect the pegs in the soil, even 40 days post-planting, when seed treatments have lost their protective effects. For this reason, seed treatment with fungicides is not effective for peanut smut. Despite this, fungicides have been studied for control of the disease. A fungicide mixture of carboxin + metalaxyl + thiophanate methyl + captan inhibited in vitro mycelial development in T. frezii by 70% (Astiz Gassó and Wojszko, 2011).
Seed Health Tests
Seed health tests are a good way of determining the pathogenic charge introduced in a field. Marraro Acuña (2012) detected teliospores in asymptomatic seeds by washing them and observing the resulting water under the microscope. Cazón et al. (2016a,c) developed a method of detecting teliospores on seeds based on qPCR using specific primers.
Pathway CausesTop of page
|Crop production||Seed trade, agricultural machinery and harvesting activities can disperse the pathogen between fields||Yes||Cazón, 2015; Rago et al., 2016|
|Seed trade||T. frezii can be dispersed through contaminated seeds||Yes||Yes||Cazón, 2015; Rago et al., 2016; Rago et al., 2017|
Pathway VectorsTop of page
|Clothing, footwear and possessions||Not frequent||Yes||Yes||Marinelli et al., 2010|
|Containers and packaging - non-wood||Spores can contaminate peanut products destined for exportation (edible grain, blanched and crushed peanut)||Yes||Cazón et al., 2016a|
|Machinery and equipment||Spores can adhere to agricultural machinery and be carried to other plots in the same country or bordering countries||Yes||Cazón, 2015; Rago et al., 2016; Rago et al., 2017|
|Wind||Spores can be transported by wind from infested plots to healthy plots. Peanut processing plants are a major source of aerial spores||Yes||Cazón, 2015; Rago et al., 2016; Rago et al., 2017|
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Fruits (inc. pods)||spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|True seeds (inc. grain)||spores||Yes||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Plant parts not known to carry the pest in trade/transport|
|Growing medium accompanying plants|
|Stems (above ground)/Shoots/Trunks/Branches|
Impact SummaryTop of page
Economic ImpactTop of page
Paredes et al. (2017a,c) determined the proportion of loss according to the incidence of the disease. This was estimated using the real and potential weight of grains. The damage function of peanut smut is highly significant (R² = 0.95), with a yield decrease of 0.65% for each incidence point.
In 2016, Paredes et al. (2016) assessed peanut smut in 40 fields from the main peanut-growing region of Córdoba, Argentina. A yield loss of 27,419 MT (USD 14,151.800), representing 3.15% of the total production, was reported. In some fields, losses of 35% were observed.
Capello and Dignani (2015) found that estimation of losses in fields with low inoculum density was erratic, whereas the correlation between losses and the number of teliospores/g of soil in fields with high inoculum density was high. An incidence of peanut smut above 14% was considered as a damage threshold, and the authors estimated that a 1% increase in incidence corresponded to a 2% decrease in yield.
Social ImpactTop of page
Due to the biological characteristics of the pathogen, peanut smut threatens the sustainability of peanut production. More than 92% of peanut production and processing in Argentina is located in the centre of the country, mainly in the province of Córdoba (Departamento Información Agroeconómica, 2015). More than 12,000 jobs are directly or indirectly related to peanut production in this province, and the industry has a significant contribution to the local economy (Cámara Argentina del Maní, 2013). It is therefore a priority to continue producing a high-quality product with high yields (Olivera, 2015).
Risk and Impact FactorsTop of page Impact outcomes
- Negatively impacts agriculture
- Negatively impacts livelihoods
- Pest and disease transmission
- Highly likely to be transported internationally accidentally
- Highly likely to be transported internationally illegally
- Difficult to identify/detect as a commodity contaminant
- Difficult/costly to control
DiagnosisTop of page
To quantify disease intensity in affected fields, incidence (proportion of infected pods out of a total sample) and severity (proportion of damaged pod tissue) are evaluated. Disease severity can be estimated using a diagrammatic scale proposed by Astiz Gassó et al. (2008), which represents five different levels of severity; 0: healthy pods; 1: normal pod with a small sorus in single kernel; 2: deformed or normal pod with half of the kernels affected; 3: deformed pod and a completely smutted kernel; and 4: deformed pod, two completely smutted kernels can be observed (see Pictures). By combining both parameters, incidence and severity, it is possible to calculate disease intensity (Paredes et al., 2014).
Detection and InspectionTop of page
Symptoms of the disease are characteristic and easy to identify in the field. As the aerial part of the plant is asymptomatic, it is necessary to open pods at advanced stages of development to detect the pathogen (Rago et al., 2017). Disease assessment is performed when a given field is to be harvested of mature pods (R8). It is only in this phenological state that it is possible to estimate the severity of the disease in samples. Infection can be seen in immature pods, but it is difficult to estimate severity. One of the tools for monitoring the disease is based on the quantification of spores in the plot to be planted. This is done through sampling and observing soil suspensions under the microscope. Oddino et al. (2010) related the amount of inoculum present in a plot with the incidence of the disease.
Prevention and ControlTop of page
Spores of T. frezii may be present in or on seeds. Australia and the USA have recently restricted the introduction of edible grains from Argentina and Brazil due to the presence of spores in containers originating from these countries. Only blanched peanut with sanitary certification is permitted. Australia and the USA are peanut importers, but also peanut producers, hence the introduction of the pathogen to these countries could be harmful to their crops.
It is difficult to generate a rapid response for peanut smut, because the assessment of the disease is only performed at mature stages of the crop (Rago et al., 2017). Only then is it possible to know the impact of the disease on yield. To avoid high losses, it is necessary to implement preventive management strategies, such as crop rotation, fungicide treatment and the selection of healthy fields and seeds (Paredes et al., 2017d).
Cultural control and sanitary measures
As peanut smut is a monocyclic, polyetic disease, management measures should be focused on the reduction of initial inoculum. Crop rotation schemes of more than 3 years without peanuts showed low T. frezii teliospore density in soil, resulting in reduced levels of smut incidence and severity at crop maturity (Fundación Maní Argentino, 2010). In addition, peanut crops preceded by maize exhibited lower incidence of peanut smut than those preceded by soybean (Marraro Acuña and Haro, 2011). Other disease management practices have been suggested by various authors.
Although the initial report of peanut smut was in wild peanuts in Brazil, soil conditions and characteristics in the productive system in that country have prevented the disease affecting commercial peanuts. In contrast to Argentina, the peanut-growing area of Brazil has soils with a low pH. Moreover, its rotation scheme is more prolonged (5 or 6 years, with sugarcane before), so the organic matter and the microflora of the soil differ from Argentinian soils. Considering the complex life cycle of T. frezii in the soil prior to infection, any practice or technique that modifies the chemical/physical properties of soil will also disrupt the infection sequence. Bonessi et al. (2011) evaluated soil amendments such as gypsum and dolomite as effective disease management practices. They observed that gypsum application can contribute to a partial reduction of peanut smut intensity; however, the causal factors were not clear and are still undetermined. Kearney et al. (2015) and Morla et al. (2015) assessed the use of phosphite-containing products for control of peanut smut. The products provided a 16% reduction in disease intensity, without affecting yield components.
Different physical and mechanical practices have been evaluated for control of peanut smut. Spinazzé and Marraro Acuña (2010) and Cignetti et al. (2010b) concluded that burying teliospores using deep tillage (15-20 cm depth) reduced disease incidence, as peanut pods develop at a planting depth of between 5 and 7 cm. However, T. frezii has been shown to survive in the soil for more than 4 years (Cazón et al., 2016b), indicating that deep tillage cannot completely remove teliospores. Therefore, in addition to tillage, other more conservative soil practices are encouraged to help manage this disease.
In industry, teliospores cannot be eliminated from the grain surface using water, because humidity is favourable to the production of aflatoxins. For this reason, it is necessary to implement and develop new strategies to clean the seeds.
There are few records of field trials using biological control against T. frezii, but it could offer some level of disease reduction. A bioformulation based on Trichoderma harzianum provided a 24% reduction in incidence and 25% reduction in the severity of the disease (Pastor et al., 2015; Ganuza et al., 2018a,b).
As the infection process occurs during pegging, seed treatment with fungicides is not effective for control of peanut smut. Control using foliar fungicides is variable (Cazón et al., 2013; Paredes et al., 2015b). A low reduction in disease severity may be attributed to the difficulty in reaching the target tissue (i.e. flower peg) where infection of T. frezii occurs (Astiz Gassó et al., 2008; Marinelli et al., 2008, 2010).
Paredes et al. (2015c, 2016) observed that soil-directed fungicide applications were more effective at controlling peanut smut than leaf applications. Soils can be sprayed at night when peanut leaves fold up and the soil surface is easily reached (Augusto et al., 2010a,b). In trials, soil applications of strobilurin/triazole mixtures, such as picoxystrobin + cyproconazole, provided 41-47% control in two applications, one in R2 (beginning peg) (Boote, 1982) and another 10 days after (Cazón et al., 2013; Paredes et al., 2014, 2015a). Paredes et al. (2014) evaluated the application of a slow-release granular fungicide for longer protection during pegging. This method provided a 42% reduction in the severity of peg damage using a formulation of picoxystrobin + cyproconazole, which can be applied at flowering. Similar results were observed with two sequential sprays of the same active ingredients in commercial mixtures (Paredes et al., 2015c). Carboxamide fungicides such as solatenol, penthiopyrad, isopyrazam and fluxapyroxad reduced the severity of the disease in pegs by 18.5 to 52.1% (Paredes et al., 2015a). The use of fungicides is an option in peanut smut management, but results can vary widely. Control efficiencies close to 40-50% are acceptable for this pathosystem. Overall, the use of effective fungicides applied at the correct dosage and at the right time, using appropriate application techniques, can contribute to integrated disease management, especially in areas with high levels of disease.
Host resistance (incl. vaccination)
Despite the fact that a limited number of registered cultivars exhibit some level of tolerance to peanut smut (e.g. Pepe ASEM INTA and Manigran), 100% of the peanut cultivars widely planted in Argentina are susceptible to the disease. This has favoured the rapid spread of T. frezii throughout the peanut-growing region of Córdoba (Cignetti et al., 2010a). An economical and effective addition to integrated pest management programmes is therefore the use of resistant cultivars. Farías et al. (2011) evaluated the response of high-oleic cultivars to peanut smut and concluded that the cultivar Pepe ASEM-INTA had 34% disease incidence, versus 71% in the reference susceptible cultivar Colorado Irradiado-INTA.
Wild species, such as Arachis correntina and A. valida, show resistance to T. frezii (Astiz Gassó et al., 2011). Peiretti and colleagues (G Peiretti, Universidad Nacional de Río Cuarto, Córdoba, Argentina, unpublished data) found inconsistent resistance in the commercial cultivar Mapu and in a pre-commercial breeding line from the National University of Río Cuarto, Córdoba. In mid-2017, INTA released a new cultivar, Ascasubi Hispano, with high tolerance to peanut smut (less than 2% of pods affected in highly infested fields).
Molecular methods are among the tools used to facilitate the transfer of resistance. Faustinelli et al. (2015) found molecular markers associated with tolerance to peanut smut. Incorporating resistance genes currently found in commercial lines, pre-commercial lines and in wild relatives will be of great value, and this process can be done with the aid of marker assisted selection.
Monitoring and Surveillance (Incl. Remote Sensing)
Paredes et al. (2017a) assessed the prevalence and incidence of peanut smut in 70 fields from the main peanut-growing region of Córdoba, Argentina, in the 2015/16 and 2016/17 growing seasons. Forty fields were evaluated in the first year and 30 in the second. Prevalence was 100% in both growing seasons. Incidence of the disease was higher in the northern region (Departments of Tercero Arriba, Juarez Celman and General San Martín), ranging from 8 to 55%, whereas in the south (Departments of Río Cuarto and General Roca) it did not exceed 8%. Yield losses of 30,200 tons were estimated in the 2016/17 growing season, 10% more than in the 2015/16 growing season (26,800 tons).
ReferencesTop of page
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OrganizationsTop of page
Argentina: Instituto de Patología Vegetal, Av. 11 de Septiembre 4775, Córdoba Capital, https://inta.gob.ar/instdepatologiavegetal
ContributorsTop of page
13/11/17 Original text by:
Alejandro Rago, Instituto de Patología Vegetal, Avenida 11 de Septiembre 4475, Córdoba, Argentina
Juan Andrés Paredes, Instituto de Patología Vegetal, Avenida 11 de Septiembre 4475, Córdoba, Argentina
Luis Ignacio Cazón, Instituto de Patología Vegetal, Avenida 11 de Septiembre 4475, Córdoba, Argentina
Distribution MapsTop of page
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