Corn smut is a plant disease caused by the pathogenic fungus Mycosarcoma maydis, synonym Ustilago 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, often eaten as a filling in quesadillas and other tortilla-based dishes, as well as in soups.
Taxonomy Mycosarcoma maydis is the best known and studied fungus of the Ustilaginomycetes, a sub class of Basidiomycota, and is often used as the exemplar species when talking about its entire class. Formerly it was placed in genus Ustilago, but in 2016, it was placed in genus Mycosarcoma.
Description
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, wherein the 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. These dark-colored spores give the cob a burned, scorched appearance. When grown in the lab on very simple media, M. maydis 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 signaling is successful, they then send out conjugation tubes to find each other, after which they fuse and make a hypha to enter the corn 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 corn plant, and cannot be maintained in the laboratory. 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.
Ecology 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. 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 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. Moreover, M. maydis has a well-established recombinational DNA repair system. 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 proteins, and 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 M. maydis is known to produce four Gα proteins, and one each of Gβ and Gγ.
Habitat Although not all the conditions that favor growth of M. 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. 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. Finally, humans wounding the corn (with shears or other tools) present the opportunity for corn smut to easily enter the plant.
Management
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. 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.
Culinary use
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