Thecaphora frezzii

Thecaphora frezzii, commonly referred to as peanut smut, is a species of smut fungus of the genus Thecaphora and the family Glomosporiaceae. It is a basidiomycete fungus that infects peanut plants (Arachis hypogaea).[1] It is currently only found in South America, more specifically in Argentinian peanut farms.[2]

Thecaphora frezzii
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Ustilaginomycetes
Order: Urocystidales
Family: Glomosporiaceae
Genus: Thecaphora
Species:
T. frezzii
Binomial name
Thecaphora frezzii
J.M. Carranza and J.C. Lindquist (1962)

Taxonomy

Thecaphora frezzii was described by J.M. Carranza and J.C. Lindquist in 1962.[3] It was originally spelled as "frezii" but was later changed to "frezzii."[4]

Description

Physical description

An infected host's pod will have hypertrophic cells in the form of galls and a spongy consistency.[5] The cells of the grains inside the pods are destroyed and replaced by reddish-brown teliospores.[5] Something characteristic of all Thecaphora species is that they all produce sori in the host plant.[6] For T. frezzii, these sori are produced on the peanut seeds and are composed of 1 to 10 tightly bound spores.[6]

Lifecycle

Thecophora frezzii is a biotrophic obligate parasite of peanut plants.[1] It is monocyclic, so an infection cycle occurs once per growing season.[1] The fungus causes a partial or total destruction of the peanut fruit.[2] Throughout the biological cycle of the fungus, there are three main structures: teliospores, basidiospores, and hyphae.

Teliospores

The teliospores are present during the state of dormancy and act as resistance structures.[7][2]They have thick walls allowing the fungus to survive in the soil and crop residue until germination.[7] Teliospores germinate in response to the plant root exudates, therefore infection occurs once the peanut peg enters the soil.[4] Teliospores disperse most commonly via wind or machinery when peanuts are harvested and remain dormant until germination is triggered.[8][7]

Basidiospores

Following the germination of teliospores, the probasidum forms. The probasidium has two haploid nuclei which fuse to form a diploid nucleus.[2] From this nucleus, the basidium arises, which forms basidiospores via meiosis.[2] During basidiospore germination, compatible haploid germ tubes fuse.[2]

Hyphal stage

Germination of the basidiospores leads to the formation of a dikaryotic mycelium, which is the infection structure of Thecaphora frezzii.[2] The mycelium infects the host by penetrating the gynophore.[8] It uses effectors to suppress the host's immune responses to insure successful penetration and infection.[8]

Habitat and range

Thecaphora frezzii is only found in South America. Cases of peanut smut on domesticated peanuts are only reported in Argentina, while wild peanuts were found to be infected in other parts of the continent.[1] The fungus never breaches to the surface and remains in humid soils.[2] Prevalence of the fungus is higher in soils in which crop rotation is rare and peanut farming has been the only usage for an extended period.[2]

Thecaphora frezzii infection of Argentinian peanut farms

T. frezzii was first detected in 1955 in the Córdoba Province.[9] By 2011, the fungus had reached 100% prevalence in production fields, with disease incidence reaching up to 52% of plants[10].[9][11] In 2016, the reported total yield loss was equal to $14,151,800 for Argentina.[2]

Many methods of management have been attempted but have proven to be ineffective against the fungus.[12] The most effective method reported is cultivating resistant strains of peanut.[11] While cultivated peanut plants have low genetic diversity, T. frezzii has high genetic variability making it difficult to cultivate resistant plants.[9]

Recent studies have begun testing biological control options by using other organisms such as bacteria or fungi to control the fungus. One organism that has been tested in Argentina is Trichoderma harazianum [13].


References
  1. Arias, Silvina L.; Mary, Verónica S.; Velez, Pilar A.; Rodriguez, María G.; Otaiza-González, Santiago N.; Theumer, Martín G. (2021-09-01). "Where Does the Peanut Smut Pathogen, Thecaphora frezii , Fit in the Spectrum of Smut Diseases?". Plant Disease. 105 (9): 2268–2280. doi:10.1094/PDIS-11-20-2438-FE. ISSN 0191-2917. PMID 33904333. S2CID 233409797.
  2. Rago, Alejandro Mario; Cazón, Luis Ignacio; Paredes, Juan Andrés; Molina, Juan Pablo Edwards; Conforto, Erica Cinthia; Bisonard, Eduardo Matías; Oddino, Claudio (March 2017). "Peanut Smut: From an Emerging Disease to an Actual Threat to Argentine Peanut Production". Plant Disease. 101 (3): 400–408. doi:10.1094/PDIS-09-16-1248-FE. ISSN 0191-2917. PMID 30677350.
  3. "Index Fungorum - Names Record". www.indexfungorum.org. Retrieved 2023-05-05.
  4. Bennett, Rebecca S.; Rodriguez, Ana V.; Baldessari, Jorge J.; Chamberlin, Kelly D.; Payton, Mark E.; Wang, Ning (2021-02-03). "A Note on the Association Between Thecaphora frezzii Infection and Peanut Pod Density". Peanut Science. 48: 54–60. doi:10.3146/ps20-27.1. ISSN 0095-3679. S2CID 234039623.
  5. Cazón, Luis Ignacio; Paredes, Juan Andrés; Rago, Alejandro Mario (2018-08-29). The Biology of Thecaphora frezii Smut and Its Effects on Argentine Peanut Production. IntechOpen. doi:10.5772/intechopen.75837. ISBN 978-1-78923-609-5. S2CID 55818040.
  6. Ospina-Maldonado, Susana; Castlebury, Lisa A.; Bennett, Rebecca S.; Salgado-Salazar, Catalina (2022-01-01). "Peanut Smut: A Diagnostic Guide". Plant Health Progress. 23 (4): 492–496. doi:10.1094/PHP-10-21-0131-DG. ISSN 1535-1025. S2CID 249488555.
  7. Diaz, M.S.; Figueroa, A.C.; Alasino, V.R.; Turco, M; Fernández, A; Marino, B; Soria, N.W.; Beltramo, D.M (2023). "Changes of lipids composition in different ontogenetic stages of Thecaphora frezii: expression of key enzymes for lipid biosynthetic pathways". Journal of Applied Microbiology (published 2023-01-01). doi:10.1093/jambio/lxac022. PMID 36724262. Retrieved 2023-05-05.
  8. Soria, Néstor W.; Badariotti, Esteban H.; Alasino, Valeria R.; Figueroa, Ana C.; Díaz, María S.; Yang, Pablo; Beltramo, Dante M. (2022-11-01). "Elucidating potential effectors, pathogenicity and virulence factors expressed by the phytopathogenic fungus Thecaphora frezii through analysis of its transcriptome". European Journal of Plant Pathology. 164 (3): 325–335. doi:10.1007/s10658-022-02562-2. ISSN 1573-8469. S2CID 251664168.
  9. Kearney, Marcelo Isaías; Kearney, M.; Zuza, M.; Ibañez, M.; Peralta, V.; Peiretti, G.; Alcalde, M.; Mojica, C.; Rago, A. (2021-02-03). "Response of peanut (Arachis hypogaea L.) genotypes to smut (Thecaphora frezii) in the peanut growing region of Argentina". Peanut Science. 48: 61–67. doi:10.3146/ps20-18.1. hdl:20.500.12123/9409. ISSN 0095-3679. S2CID 234016610.
  10. Paredes, Juan A.; Edwards Molina, Juan P.; Cazón, Luis I.; Asinari, Florencia; Monguillot, Joaquín H.; Morichetti, Sergio A.; Rago, Alejandro M.; Torres, Adriana M. (2022-04-01). "Relationship between incidence and severity of peanut smut and its regional distribution in the main growing region of Argentina". Tropical Plant Pathology. 47 (2): 233–244. doi:10.1007/s40858-021-00473-x. ISSN 1983-2052. S2CID 242948493.
  11. de Blas, Francisco J.; Bruno, Cecilia I.; Arias, Renee S.; Ballén-Taborda, Carolina; Mamani, Eva; Oddino, Claudio; Rosso, Melina; Costero, Beatriz P.; Bressano, Marina; Soave, Juan H.; Soave, Sara J.; Buteler, Mario I.; Seijo, J. Guillermo; Massa, Alicia N. (2021-07-02). "Genetic mapping and QTL analysis for peanut smut resistance". BMC Plant Biology. 21 (1): 312. doi:10.1186/s12870-021-03023-4. ISSN 1471-2229. PMC 8252251. PMID 34215182.
  12. Paredes, J. A.; Cazón, L. I.; Oddino, C.; Monguillot, J. H.; Rago, A. M.; Molina, J. P. Edwards (2021-02-01). "Efficacy of fungicides against peanut smut in Argentina". Crop Protection. 140: 105403. doi:10.1016/j.cropro.2020.105403. ISSN 0261-2194. S2CID 224896574.
  13. Ganuza, M.; Pastor, N.; Erazo, J.; Andrés, J.; Reynoso, M. M.; Rovera, M.; Torres, A. M. (2018-05-01). "Efficacy of the biocontrol agent Trichoderma harzianum ITEM 3636 against peanut smut, an emergent disease caused by Thecaphora frezii". European Journal of Plant Pathology. 151 (1): 257–262. doi:10.1007/s10658-017-1360-0. ISSN 1573-8469. S2CID 254473702.
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