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Allergen Encyclopedia
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Whole Allergen

m201 Tilletia tritici/Ustilago

m201 Tilletia tritici/Ustilago Scientific Information

Type:

Whole Allergen

Display Name:

Tilletia tritici/Ustilago

Allergen code:

m201

Family:

Ustilaginaceae

Species:

tritici/ nuda, tritici, segetum

Route of Exposure:

Inhalation

Latin Name:

Tilletia tritici / Ustilago nuda/tritici/maydis

Other Names:

Tilletia caries-Wheat bunt/ Ustilago nuda – U. tritici - U. segetum-loose wheat smut

Summary

Tilletia spp. (smuts) and Ustilago spp. (bunts) are common molds of the Class Ustilaginomycetes, mostly found in cereal crops and soil. They are well known plant pathogens which may have a role in the sensitization of allergic patients. The particles causing sensitization are spores found in the environment.

Smuts may be involved in the development of asthma and hypersensitivity pneumonitis. Cross reactivity with other molds within the Phylum Basidiomycota may occur.

Allergen

Nature

The molds Tilletia tritici (T. caries) and Ustilago spp. are members of the Phylum Basidiomycota. Members of the subphylum Ustilaginomycotina are able to grow within, or on the surface of the host plants, including stems, leaves, flower parts, bulbs and seeds; teliospores are released in characteristic dark masses (1).

Fungi of the genus Tilletia are usually called “bunts” and those of the genus Ustilago are often collectively named “smuts” (2, 3). Many of these molds are plant pathogens, usually attacking cereal crops and causing different symptoms in the plants, which can appear blackened (4). Tilletia spp. can be found in infected seed and soil; these molds produce teliospores (a type of spore) within the plant ovaries. The spores can have a rough or smooth surface (4). Ustilago spp. produce thick walled teliospores that readily germinate into a cylindrical basidium (a reproductive structure); the teliospores can also survive dormant for years (1, 5, 6).

Smut spores from Ustilago species could be detected in several countries at different times of the year, with peaks in February, May, August – or the rainy season in Nigeria (7-12). Moderate to high winds and temperatures in November increased the presence of Ustilago spores in the air, whereas in spring the peak was due to lawn mowing and disturbances of wheat crops (8). High concentrations of smut spores positively correlated with higher temperatures and negatively correlated with humidity (10). Ustilago spores were also frequently detected in the indoor setting of a hospital outpatient ward (13).

Taxonomy 

Taxonomic tree of Tilletia genus (2, 14)

Domain

Eukaryota

Kingdom

Fungi

Phylum

Basidiomycota

Subphylum

Ustilaginomycotina

Class

Ustilaginomycetes

Order

Tilletiales

Family

Tilletiaceae

Genus

Tilletia

 

Taxonomic tree of Ustilago genus (3, 15)

Domain

Eukaryota

Kingdom

Fungi

Phylum

Basidiomycota

Subphylum

Ustilaginomycotina

Class

Ustilaginomycetes

Order

Ustilaginales

Family

Ustilaginaceae

Genus

Ustilago

Tissue

Tilletia/Ustilago allergens are spread by airborne spores. Those of T. caries were ejected and able to achieve longer distances than the other fungal species studied (16). Smut spores ranged between 1.6–25.6% of the total detected in different studies (8-11, 17). In a study where spore sampling was carried out at altitude and at ground level, Ustilago spores had higher concentrations at ground level and in urban environments (17).

Epidemiology

Worldwide distribution 

There is a distinct lack of specific reports of allergic disease attributed to Tilletia spp. and Ustilago spp.; however, their involvement in developing symptoms of asthma was demonstrated in Australian studies (18, 19). Smut species were also the cause of allergic disease in Japan and Northern America (20, 21).

Risk factors 

Some occupations (e.g. farmers) may be at higher risk of allergic respiratory conditions when exposed to smuts (21), given the prevalence of these species (Tilletia/Ustilago) as cereal pathogens (2, 3).

Environmental Characteristics

Worldwide distribution 

Tilletia tritici (T. caries) can be found worldwide (2). Ustilago nuda (U. tritici/segetum) can be found in many countries (3).

Route of Exposure

Main

Inhalation of spores (22).

Detection

Main methods

Burkard Volumetric Spore Trap (7, 18, 19).

Measures 

The concentration of Ustilago spores detected daily was normally less than 1,000 per m3, though a peak of nearly 6,000 per m3 was also recorded (7).

Clinical Relevance

Asthma

In a study of 2,098 children who received treatment in hospital for asthma, it was shown that in the age group 14–18 there was a significant association between the presence of environmental Ustilago spores and hospitalization (18). People with asthma could show higher inflammation and lower lung function when exposed to Ustilago smuts (19).

Other diseases

Ustilago esculenta has been reported as a cause of hypersensitivity pneumonitis (HP) in a 40-year old patient with symptoms of cough, fever and dyspnea (20). In another study into the development of HP in farmers who experienced respiratory symptoms, 11.2% of positive results (SPTs or RAST assays) were associated with grain smuts extracts (21).

Diagnostics Sensitization

The presence of allergen-specific antibodies is usually determined by skin prick tests (SPTs) and serology for IgE (22). In a study investigating skin test reactions of allergic patients to lesser reported fungi, 56% showed a positive dermal reactivity to fungal extracts, including Ustilago maydis (23). In another study of U. maydis extracts in 200 patients with either asthma or allergic rhinitis, asthmatic patients were more likely to have immediate skin reactions on SPT, whereas the patients with rhinitis were more likely to have late phase sensitivity (24).

Prevention and Therapy

Allergen immunotherapy

Immunotherapy is currently not recommended for patients allergic to molds, due to complexities of the allergens and patient co-allergies (22).

Prevention strategies 

Avoidance is difficult to achieve (22), due to the wide range of environments in which Tilletia spp. and Ustilago spp. can be found (2, 3).

Molecular Aspects

Cross-reactivity

An extract of Ustilago maydis showed cross-reactivity with Cryptococcus neoformans, suggesting that some Basidiomycetes may share antigens (25).

Compiled By

Author: RubyDuke Communications

Reviewer: Dr. Christian  Fischer

 

Last reviewed:January 2022

References
  1. Margulis L, Chapman MJ. Chapter Four - KINGDOM FUNGI. In: Margulis L, Chapman MJ, editors. Kingdoms and Domains (Fourth Edition). London: Academic Press; 2009. p. 379-409.
  2. CABI. Tilletia tritici (wheat bunt) 2020 [cited 2021 16.12.21]. Available from: https://www.cabi.org/isc/datasheet/53923.
  3. CABI. Ustilago nuda f.sp. tritici (loose wheat smut) 2021 [cited 2021 16.12.21]. Available from: https://www.cabi.org/isc/datasheet/55946.
  4. Turgay EB, Oğuz AÇ, Ölmez F. Chapter 15 - Karnal bunt (Tilletia indica) in wheat. In: Ozturk M, Gul A, editors. Climate Change and Food Security with Emphasis on Wheat: Academic Press; 2020. p. 229-41.
  5. Boekhout T, Fonseca Á, Sampaio JP, Bandoni RJ, Fell JW, Kwon-Chung KJ. Chapter 100 - Discussion of Teleomorphic and Anamorphic Basidiomycetous Yeasts. In: Kurtzman CP, Fell JW, Boekhout T, editors. The Yeasts (Fifth Edition). London: Elsevier; 2011. p. 1339-72.
  6. Taylor TN, Krings M, Taylor EL. 9 - Basidiomycota. In: Taylor TN, Krings M, Taylor EL, editors. Fossil Fungi. San Diego: Academic Press; 2015. p. 173-99.
  7. Crotzer V, Levetin E. The aerobiological significance of smut spores in Tulsa, Oklahoma. Aerobiologia. 1996;12(1):177-84.
  8. Gupta SK, Pereira BM, Singh AB. Survey of airborne culturable and non-culturable fungi at different sites in Delhi metropolis. Asian Pacific journal of allergy and immunology. 1993;11 1:19-28.
  9. Hasnain SM, Al-Frayh A, Thorogood R, Harfi HA, Wilson JD. Seasonal Periodicities of Fungal Allergens in the Atmosphere of Riyadh. Annals of Saudi Medicine. 1989;9(4):337-43.
  10. Kilic M, Altunoglu MK, Akdogan GE, Akpınar S, Taskın E, Erkal AH. Airborne fungal spore relationships with meteorological parameters and skin prick test results in Elazig, Turkey. J Environ Health Sci Eng. 2020;18(2):1271-80.
  11. Oliveira M, Ribeiro H, Abreu I. Annual variation of fungal spores in atmosphere of Porto: 2003. Ann Agric Environ Med. 2005;12(2):309-15.
  12. Ezikanyi DN, Sakwari G, Nnamani CV. Aeroallergens in North-Central Nigeria. Allergol Immunopathol (Madr). 2018;46(6):599-606.
  13. Tormo Molina R, Gonzalo Garijo MA, Muñoz Rodríguez AF, Silva Palacios I. Pollen and spores in the air of a hospital out-patient ward. Allergol Immunopathol (Madr). 2002;30(4):232-8.
  14. Uniprot.org. Taxonomy - Tilletia caries (wheat bunt fungus) 2021 [cited 2021 16.12.21]. Available from: https://www.uniprot.org/taxonomy/13290.
  15. Uniprot.org. Taxonomy - Ustilago nuda 2021 [cited 2021 16.12.21]. Available from: https://www.uniprot.org/taxonomy/86802.
  16. Stolze-Rybczynski JL, Cui Y, Stevens MHH, Davis DJ, Fischer MWF, Money NP. Adaptation of the spore discharge mechanism in the basidiomycota. PloS one. 2009;4(1):e4163-e.
  17. Damialis A, Kaimakamis E, Konoglou M, Akritidis I, Traidl-Hoffmann C, Gioulekas D. Estimating the abundance of airborne pollen and fungal spores at variable elevations using an aircraft: how high can they fly? Scientific Reports. 2017;7(1):44535.
  18. Tham R, Katelaris CH, Vicendese D, Dharmage SC, Lowe AJ, Bowatte G, et al. The role of outdoor fungi on asthma hospital admissions in children and adolescents: A 5-year time stratified case-crossover analysis. Environ Res. 2017;154:42-9.
  19. Tham R, Erbas B, Dharmage SC, Tang ML, Aldakheel F, Lodge CJ, et al. Outdoor fungal spores and acute respiratory effects in vulnerable individuals. Environ Res. 2019;178:108675.
  20. Yoshida K, Suga M, Yamasaki H, Nakamura K, Sato T, Kakishima M, et al. Hypersensitivity pneumonitis induced by a smut fungus Ustilago esculenta. Thorax. 1996;51(6):650-7.
  21. Marx JJ, Jr., Twiggs JT, Ault BJ, Merchant JA, Fernandez-Caldas E. Inhaled aeroallergen and storage mite reactivity in a Wisconsin farmer nested case-control study. Am Rev Respir Dis. 1993;147(2):354-8.
  22. Twaroch TE, Curin M, Valenta R, Swoboda I. Mold allergens in respiratory allergy: from structure to therapy. Allergy Asthma Immunol Res. 2015;7(3):205-20.
  23. Giannini EH, Northey WT, Leathers CR. The allergenic significance of certain fungi rarely reported as allergens. Ann Allergy. 1975;35(6):372-6.
  24. Santilli J, Jr., Rockwell WJ, Collins RP. The significance of the spores of the Basidiomycetes (mushrooms and their allies) in bronchial asthma and allergic rhinitis. Ann Allergy. 1985;55(3):469-71.
  25. Cheng Matthew P, Nguyen Tien T, Parkes Leighanne O, Dufresne Philippe J, Sheppard Donald C, Warnock David W. Cross-Reacting Ustilago maydis Causing False-Positive Cryptococcal Antigen Test Results. J Clin Microbiol. 2017;55(10):3135-7.