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Corn smut

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"Cuitlacoche" redirects here. For the genus of birds otherwise known as "Cuitlacoche", see Toxostoma.

Corn smut
Mycosarcoma maydis diploid teleospores
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Basidiomycota
Class: Ustilaginomycetes
Order: Ustilaginales
Family: Ustilaginaceae
Genus: Mycosarcoma
Species:
M. maydis
Binomial name
Mycosarcoma maydis
Synonyms
Corn smut
Huitlacoche
Common nameshuitlacoche (Mexico), blister smut of maize, boil smut of maize, common smut of maize
Causal agentsMycosarcoma maydis
Hostsmaize and teosinte
EPPO CodeUSTIMA
DistributionWorldwide, where corn is grown[3][4]

Corn smut is a plant disease caused by the pathogenic fungus Mycosarcoma maydis. One of several cereal crop pathogens called smut, the fungus forms galls on all above-ground parts of corn species such as maize and teosinte. The infected corn is edible; in Mexico, it is considered a delicacy, called huitlacoche,[5] often eaten as a filling in quesadillas and other tortilla-based dishes, as well as in soups.

Etymology

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In Mexico, corn smut is known as huitlacoche (Spanish pronunciation: [(ɡ)witlaˈkotʃe], sometimes spelled cuitlacoche). This word entered Spanish in Mexico from Classical Nahuatl, though the Nahuatl words from which huitlacoche is derived are debated. In modern Nahuatl, the word for huitlacoche is cuitlacochin (Nahuatl pronunciation: [kʷit͡ɬɑˈkot͡ʃin]), and some sources deem cuitlacochi to be the classical form.[6]

Some sources wrongly give the etymology as coming from the Nahuatl words cuitlatl [ˈkʷit͡ɬɑt͡ɬ] ("excrement" or "rear-end", actually meaning "excrescence") and cochtli [ˈkot͡ʃt͡ɬi] ("sleeping", from cochi "to sleep"), thus giving a combined mismeaning of "sleeping/hibernating excrement",[6][7] but actually meaning "sleeping excrescence", referring to the fact that the fungus grows between the kernels and impedes them from developing, thus they remain "sleeping".

A second group of sources deem the word to mean "raven's excrement".[8][9] These sources appear to be combining the word cuitlacoche for "thrasher"[10] with cuitla, meaning "excrement", actually meaning "excrescence". However, the avian meaning of cuitlacoche derives from the Nahuatl word "song" cuīcatl [ˈkʷiːkɑt͡ɬ], itself from the verb "to sing" cuīca [ˈkʷiːkɑ].[6] This root then clashes with this reconstruction's second claim that the segment cuitla- comes from cuitla ("excrement").

One source derives the meaning as "corn excrescence", using cuītla again and "maize" tlaōlli [t͡ɬɑˈoːlːi].[11] This requires the linguistically unlikely evolution of tlaōlli "maize" into tlacoche.

In Peru, it is known as chumo or pacho.

Taxonomy

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Mycosarcoma maydis is the best known and studied of the Ustilaginomycetes, a sub class of basidiomycota, and so is often used as the exemplar species when talking about its entire class.[12]

Formerly it was placed in genus Ustilago, but in 2016 it was placed in genus Mycosarcoma.[13]

Characteristics

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This ear of corn has been infected with Mycosarcoma maydis.

The fungus infects all parts of the host plant by invading the ovaries of its host. The infection causes the corn kernels to swell up into tumor-like galls, whose tissues, texture, and developmental pattern are mushroom-like. The galls grow to 4 to 5 inches in diameter. These galls are made up of hypertrophied cells of the infected plant, along with resulting fungal threads, and blue-black spores.[14] These dark-colored spores give the cob a burned, scorched appearance.[citation needed]

Biology

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Life cycle

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Mycosarcoma maydis haploid sporidia

When grown in the lab on very simple media, it behaves like baker's yeast, forming single cells called sporidia. These cells multiply by budding off daughter cells. When two compatible sporidia meet on the surface of the plant, however, they switch to a different mode of growth. First, they produce one or another pheromone, and begin producing one or the other type of pheromone receptor - this depends on mating type a or b, as determined by alleles at two unlinked mating loci. If this signalling is successful they then send out conjugation tubes to find each other,[12] after which they fuse and make a hypha to enter the maize plant. Hyphae growing in the plant are dikaryotic; they possess two haploid nuclei per hyphal compartment. In contrast to sporidia, the dikaryotic phase of M. maydis only occurs during successful infection of a maize plant, and cannot be maintained in the laboratory.

Proliferation of the fungus inside the plant leads to disease symptoms such as chlorosis, anthocyanin formation, reduced growth, and the appearance of tumors harboring the developing teliospores. These teliospores help to overwinter the pathogen into the next season. They survive in the soil.[15][16]

Mature tumors release spores that are dispersed by rain and wind. Under appropriate conditions, a metabasidium is formed in which meiosis occurs. Resulting haploid nuclei migrate into elongated single cells. These cells detach from the metabasidium to become the sporidia, thus completing the life cycle.

Host/pathogen conflict

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Plants have evolved efficient defense systems against pathogenic microbes. A rapid plant defense reaction after pathogen attack is the oxidative burst, which involves the production of reactive oxygen species at the site of the attempted invasion. As a pathogen, M. maydis can respond to such an oxidative burst by an oxidative stress response, regulated by gene YAP1. This response protects M. maydis from the host attack, and is necessary for the pathogen's virulence.[17] Furthermore, M. maydis has a well-established recombinational DNA repair system.[18] This repair system involves a homolog of Rad51 that has a very similar sequence and size to its mammalian counterparts. This system also involves a protein, Rec2 that is more distantly related to Rad51, and Brh2 protein that is a streamlined version of the mammalian Breast Cancer 2 (BRCA2) protein. When any of these proteins is inactivated, sensitivity of M. maydis to DNA damaging agents is increased. Also mitotic recombination becomes deficient, mutation frequency increases and meiosis fails to complete. These observations suggest that recombinational repair during mitosis and meiosis in M. maydis may assist the pathogen in surviving DNA damage arising from the host's oxidative defensive response to infection, as well as from other DNA damaging agents.

Proteome

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Mycosarcoma maydis is known to produce four Gα proteins, and one each of Gβ and Gγ.[12]

Management

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Ear of corn infected with Mycosarcoma maydis

Losses from corn smut can vary greatly; however, annual yield losses rarely exceed 2% when resistant cultivars are planted. This disease can have a large economic impact on sweet corn, specifically when smut galls replace the kernels. There are many ways to control and manage corn smut; however, corn smut cannot be controlled by any common fungicide at this time, as M. maydis infects individual corn kernels instead of infecting the entire cob, like head smut.[19]

Some beneficial ways to contain corn smut include resistant corn plants, crop rotation, and avoiding mechanical injury to the plant. A mechanical injury can cause the corn to become easily accessible to M. maydis, enhancing infection. Additionally, clearing the planting area of debris can help control corn smut, as the teliospores from corn smut overwinter in debris. This is not the best practice, though, because corn smut can also overwinter in the soil; crop rotation is recommended. Lastly, as excess nitrogen in the soil augments infection rate, using fertilizer with low nitrogen levels, or just limiting the amount of nitrogen in the soil proves to be another way to control corn smut.[20]

Environment

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Although not all the conditions that favor growth of Mycosarcoma maydis are known, there are certain environments where corn smut seems to thrive, depending on both abiotic and biotic factors. Hot and dry weather during pollination followed by a heavy rainy season appear to improve the pathogenicity of corn smut.[21] Furthermore, excess manure (and therefore nitrogen) in the soil also increases pathogenicity. Not only do these abiotic factors increase infectability, they also increase disease spread. High winds and heavy rain also increase disease spread as the spores of corn smut can be more easily transmitted. Other biotic factors largely have to do with the extent by which humans interact with the corn and corn smut. If corn debris is not cleared at the end of the season, the spores can overwinter in the corn fragments and live to infect another generation.[22] Finally, humans wounding the corn (with shears or other tools) present the opportunity for corn smut to easily enter the plant.

Culinary use

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See also: List of delicacies
Huitlacoche for sale in the produce department of a Soriana store in Mexico

Smut feeds on the corn plant and decreases the yield. Smut-infected crops are often destroyed, although some farmers use them to prepare silage. However, the immature infected galls are still edible, and in Mexico they are highly esteemed as a delicacy. It is known as huitlacoche, and sold for a significantly higher price than uninfected corn. The consumption of corn smut in Mexico originated directly from Aztec cuisine.[23] For culinary use, the galls are harvested while still immature — fully mature galls are dry and almost entirely spore-filled. The immature galls, gathered two to three weeks after an ear of corn is infected, still retain moisture and, when cooked, have a flavor described as mushroom-like, sweet, savory, woody, and earthy. Flavor compounds include sotolon and vanillin, as well as the sugar glucose.

Huitlacoche is a source of the essential amino acid lysine, which the body requires but cannot manufacture. It also contains levels of beta-glucans similar to, and protein content equal or superior to, most edible fungi.[24]

The fungus has had difficulty entering into the American and European diets as most farmers see it as blight, despite attempts by government and high-profile chefs to introduce it. In the mid-1990s, due to demand created by high-end restaurants, Pennsylvania and Florida farms were allowed by the United States Department of Agriculture (USDA) to intentionally infect corn with huitlacoche. Most observers consider the program to have had little impact,[citation needed] although the initiative is still in progress. The cursory show of interest is significant because the USDA has spent a considerable amount of time and money trying to eradicate corn smut in the United States. Moreover, in 1989, the James Beard Foundation held a high-profile huitlacoche dinner, prepared by Josefina Howard, chef at Rosa Mexicano restaurant.[25] This dinner tried to get Americans to eat more of it by renaming it the "Mexican truffle" and it is often compared to truffles in food articles describing its taste and texture.[25][26][27]

Native American tribes in North America ate corn smut as well. The Hidatsa tribe of North Dakota's practice of preparing and eating corn smut is described vividly in Buffalo Bird Woman's Garden.[28]

Native Americans of the American Southwest, including the Zuni people, have used corn smut in an attempt to induce labor. It has similar medicinal effects to ergot, but weaker, due to the presence of the chemical ustilagine.[29]

Recipes of Mexico

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Huitlacoche corn taco

A simple Mexican-style succotash can be made from chorizo, onions, garlic, serrano peppers, huitlacoche, and shrimp with salsa taquera. The mild, earthy flavors of the huitlacoche blend nicely with the fats of the chorizo and bond to mellow out the heat from the peppers and salsa.

Another Maya favorite on the Riviera Maya (Cancun to Tulum) is to add huitlacoche to omelettes. Its earthy flavors bond with the fats that cook the eggs to mellow the flavors into a truffle-like taste.

Quesadilla de huitlacoche, as it is often served in central Mexico

Huitlacoche is also popular in quesadillas with Mexican cheese, sautéed onions, and tomatoes.

The blueish color transforms into the recognizable black color only with heat. Any dish with huitlacoche must include a slow simmer of the fungus until it becomes black, which also removes most of the starch of the corn, and what is left is a black oily paste.

Availability

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In Mexico, huitlacoche is mostly consumed fresh and can be purchased at restaurants or street or farmer's markets throughout the country and, to a much lesser extent, can also be purchased as a canned good in some markets and via the internet. Farmers in the countryside spread the spores around intentionally to create more of the fungus. In some parts of the country, they call the fungus "hongo de maiz", i.e. "maize fungus".[30]

Nutritional value

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When corn smut grows on a corn cob, it changes the nutritional worth of the corn it affects. Corn smut contains more proteins than the uninfected grains normally do. The amino acid lysine, of which corn contains very little, abounds in corn smut.[31]

Non-culinary uses

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Model organism

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The yeast-like growth of U. maydis makes it an appealing model organism for research, although its relevance in nature is unknown. The fungus is exceptionally well-suited for genetic modification. This allows researchers to study the interaction between the fungus and its host with relative ease. The availability of the entire genome is another advantage of this fungus as a model organism.[32]

U. maydis is not only used to study plant disease, but it also is used to study plant genetics. In 1996, a study on U. maydis genetics led to the discovery of synthesis-dependent strand annealing, a method of homologous recombination used in DNA repair.[33] Other studies in the fungus have also investigated the role of the cytoskeleton in polarized growth.[citation needed] It is largely due to work with U. maydis that the function of the breast-cancer gene BRCA2 is now known.[34] The fungus is mostly studied as model organism for host pathogen interaction and delivery of effectors protein.

Industrial biotechnology

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Mycosarcoma maydis is able to produce a broad range of valuable chemicals such as ustilagic acid, itaconic acid, malic acid, and hydroxyparaconic acid. This ability is gaining corn smut more relevance to industrial applications.[35]

See also

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  • Edible mushroom – Edible fungi fruit bodies
  • Medicinal fungi – Fungi that can be used to develop medications

References

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  1. ^ Mycosarcoma maydis in Index Fungorum
  2. ^ Ustilago maydis in Index Fungorum
  3. ^ "Common smut of corn". apsnet.org. American Phytopathological Society. Retrieved 6 October 2018.
  4. ^ "Ustilago maydis (DC.) Corda". Global Biodiversity Information Facility. Retrieved 6 October 2018.
  5. ^ Peterson, James (27 March 2012). Vegetables, Revised: The Most Authoritative Guide to Buying, Preparing, and Cooking, with More than 300 Recipes. Random House. p. 184. ISBN 978-1-60774-205-0. Retrieved 24 October 2013 – via Google Books.
  6. ^ a b c Gómez de Silva, Guido (2001). Diccionario breve de mexicanismos (in Spanish). Mexico: Fondo de Cultura Económica. See entries for "huitlacoche" and "cuicacoche o cuiltacoche".
  7. ^ "Producción de caviar azteca en invernadero". Teorema Ambiental (in Spanish). 1 August 2006. Archived from the original on 28 August 2010.
  8. ^ Vincent, David (8 November 2008). "Mexico City". City Guide. The Guardian.
  9. ^ Wolff, Barbara (19 September 2006). "Professor introduces unusual edible fungus to Madison". University of Wisconsin - Madison News (Press release).
  10. ^ Marcó del Pont, Raúl (1997). Guía de aves canoras y de ornato. Conabio-ine-semarnap, Instituto Nacional de Ecología, México. pp. 66–70. ISBN 978-968-817-373-2.
  11. ^ Vasconcelos Dueñas, Irene (August 2007). "Los hongos medicinales en México" (in Spanish).
  12. ^ a b c Li, Liande; Wright, Sara J.; Krystofova, Svetlana; Park, Gyungsoon; Borkovich, Katherine A. (2007). "Heterotrimeric G Protein Signaling in Filamentous Fungi". Annual Review of Microbiology. 61 (1). Annual Reviews: 423–452. doi:10.1146/annurev.micro.61.080706.093432. ISSN 0066-4227. PMID 17506673.
  13. ^ McTaggart, Alistair R.; Shivas, Roger G.; Boekhout, Teun; Oberwinkler, Franz; Vánky, Kálmán; Pennycook, Shaun R.; Begerow, Dominik (December 2016). "Mycosarcoma (Ustilaginaceae), a resurrected generic name for corn smut (Ustilago maydis) and its close relatives with hypertrophied, tubular sori". IMA Fungus. Vol. 7, no. 2. pp. 309–315. doi:10.5598/imafungus.2016.07.02.10. ISSN 2210-6359. PMC 5159601. PMID 27990337.
  14. ^ [1] Page 109 By Nicholas P. Money Professor of Botany, Miami University, Ohio; Published by Oxford University Press, Aug 4, 2006. Accessed online vis Google Books October 24, 2013.
  15. ^ Banuett, F. (1995). "Genetics of Ustilago Maydis, A Fungal Pathogen that Induces Tumors in Maize". Annual Review of Genetics. 29 (1): 179–208. doi:10.1146/annurev.ge.29.120195.001143. PMID 8825473.
  16. ^ Christensen, J.J. (1963). "Corn smut caused by Ustilago maydis. Monograph no. 2". Amer. Phytopath. Society.
  17. ^ Molina, L; Kahmann, R (2007). "An Ustilago maydis gene involved in H2O2 detoxification is required for virulence". Plant Cell. 19 (7): 2293–2309. doi:10.1105/tpc.107.052332. PMC 1955693. PMID 17616735.
  18. ^ Kojic, M; Zhou, Q; Lisby, M; Holloman, WK (2006). "Rec2 interplay with both Brh2 and Rad51 balances recombinational repair in Ustilago maydis". Mol Cell Biol. 26 (2): 678–688. doi:10.1128/MCB.26.2.678-688.2006. PMC 1346908. PMID 16382157.
  19. ^ Mohan, S. K., Hamm, P.B., Clough, G.H., and du Toit, L.J. 2013. "Corn Smuts" Oregon State University, A Pacific Northwest Extension. https://catalog.extension.oregonstate.edu/sites/catalog/files/project/pdf/pnw647.pdf (accessed October 12, 2020).
  20. ^ 2020. "Corn Smut" University of Massachusetts Amherst: The Center for Agriculture, Food, and the Environment. https://ag.umass.edu/vegetable/fact-sheets/corn-smut (accessed October 12, 2020)
  21. ^ Hansen, M.A. 2009. "Corn Smut" Virginia Cooperative Extension. https://www.pubs.ext.vt.edu/450/450-706/450-706.html Archived 2020-01-21 at the Wayback Machine (accessed October 13, 2020).
  22. ^ Petruzzello, M. 2017. "Corn Smut" Encyclopedia Britannica. https://www.britannica.com/science/corn-smut (accessed October 13, 2020).
  23. ^ Uribe, Monica Ortiz (20 August 2009). "In Mexico, Tar-Like Fungus Is A Delicacy". NPR. Retrieved 20 August 2009.
  24. ^ Aydoğdu, Mehmet; Gölükçü, Muharrem (21 September 2017). "Nutritional value of huitlacoche, maize mushroom caused by Ustilago maydis". Food Science and Technology. 37 (4): 531–535. doi:10.1590/1678-457X.19416.
  25. ^ a b Newhall, Edith (25 September 1989). "Fungus Feast". New York Magazine: 44.
  26. ^ TEMPTATION; Mexico's Answer To the Truffle By FLORENCE FABRICANT Published: August 30, 2000 New York Times. Accessed via NYTIMES online archives March 17, 2014
  27. ^ Corn Smut, Mexican Truffles by GREEN DEANE, December 2012. Archive of food Blog: Eat the weeds and other things too... - Accessed online March 17, 2014
  28. ^ "Buffalo Bird Woman's Garden". digital.library.upenn.edu. Retrieved 25 November 2023.
  29. ^ O'Dowd, Michael J. (2001). The History of Medications for Women. Taylor & Francis. ISBN 978-1-85070-002-9. p. 410, via Google Books
  30. ^ Laferrière, Joseph E. (1991). "Mountain Pima ethnomycology". Journal of Ethnobiology. 11 (1): 15–160.
  31. ^ Battillo, J. (2018). "The role of corn fungus in Basketmaker II diet: A paleonutrition perspective on early corn farming adaptations". Journal of Archaeological Science: Reports. 21: 64–70. Bibcode:2018JArSR..21...64B. doi:10.1016/j.jasrep.2018.07.003. S2CID 92182019.
  32. ^ Kämper J, Kahmann R, Bölker M, et al. (November 2006). "Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis". Nature. 444 (7115): 97–101. Bibcode:2006Natur.444...97K. doi:10.1038/nature05248. hdl:10261/339644. PMID 17080091.
  33. ^ Ferguson, DO; Holloman, HK (1996). "Recombinational repair of gaps in DNA is asymmetric in Ustilago maydis and can be explained by a migrating D-loop model". PNAS USA. 93 (11): 5419–5424. Bibcode:1996PNAS...93.5419F. doi:10.1073/pnas.93.11.5419. PMC 39261. PMID 8643590.
  34. ^ Kojic, M; Kostrub, CF; Buchman, AR; Holloman, WK (2002). "BRCA2 Homolog Required for Proficiency in DNA Repair, Recombination, and Genome Stability in Ustilago maydis". Molecular Cell. 10 (3): 683–691. doi:10.1016/S1097-2765(02)00632-9. PMID 12408834.
  35. ^ Geiser, Elena; Wiebach, Vincent; Wierckx, Nick; Blank, Lars M. (1 January 2014). "Prospecting the biodiversity of the fungal family Ustilaginaceae for the production of value-added chemicals". Fungal Biology and Biotechnology. 1: 2. doi:10.1186/s40694-014-0002-y. ISSN 2054-3085. PMC 5598272. PMID 28955444.
  • McGee, Harold (2004). On Food and Cooking (revised ed.). Scribner. p. 349 "Huitlacoche, or Corn Smut". ISBN 978-0-684-80001-1.
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