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Villagrán, Z.; Martínez-Reyes, M.; Gómez-Rodríguez, H.; Ríos-García, U.; Montalvo-González, E.; Ortiz-Basurto, R.I.; Anaya-Esparza, L.M.; Pérez-Moreno, J. Technological Applications of Huitlacoche. Encyclopedia. Available online: https://encyclopedia.pub/entry/46295 (accessed on 18 June 2024).
Villagrán Z, Martínez-Reyes M, Gómez-Rodríguez H, Ríos-García U, Montalvo-González E, Ortiz-Basurto RI, et al. Technological Applications of Huitlacoche. Encyclopedia. Available at: https://encyclopedia.pub/entry/46295. Accessed June 18, 2024.
Villagrán, Zuamí, Magdalena Martínez-Reyes, Horacio Gómez-Rodríguez, Uzziel Ríos-García, Efigenia Montalvo-González, Rosa Isela Ortiz-Basurto, Luis Miguel Anaya-Esparza, Jesús Pérez-Moreno. "Technological Applications of Huitlacoche" Encyclopedia, https://encyclopedia.pub/entry/46295 (accessed June 18, 2024).
Villagrán, Z., Martínez-Reyes, M., Gómez-Rodríguez, H., Ríos-García, U., Montalvo-González, E., Ortiz-Basurto, R.I., Anaya-Esparza, L.M., & Pérez-Moreno, J. (2023, July 01). Technological Applications of Huitlacoche. In Encyclopedia. https://encyclopedia.pub/entry/46295
Villagrán, Zuamí, et al. "Technological Applications of Huitlacoche." Encyclopedia. Web. 01 July, 2023.
Technological Applications of Huitlacoche
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Worldwide, the fungus known as huitlacoche (Ustilago maydis (DC.) Corda) is a phytopathogen of maize plants that causes important economic losses in different countries. Conversely, it is an iconic edible fungus of Mexican culture and cuisine, and it has high commercial value in the domestic market, though recently there has been a growing interest in the international market. Huitlacoche is an excellent source of nutritional compounds such as protein, dietary fiber, fatty acids, minerals, and vitamins. It is also an important source of bioactive compounds with health-enhancing properties. Furthermore, scientific evidence shows that extracts or compounds isolated from huitlacoche have antioxidant, antimicrobial, anti-inflammatory, antimutagenic, antiplatelet, and dopaminergic properties.

huitlacoche antioxidant

1. Introduction

Around the world, huitlacoche (Ustilago maydis) is considered a phytopathogen that causes severe damage to maize crops, leading to serious economic losses[1]. By contrast, Huitlacoche plays an important role in Mexican gastronomic culture due to its traditional uses, sensory attributes, and nutritional value[2]. Also, U. maydis is characterized by synthesizing intra- and extracellular compounds with potential biotechnological uses, including glycolipids, mannosylerythritol lipids, itaconic acid, siderophores, amino acid tryptophan-derived compounds, and hydrolytic enzymes[3][4][5], in this context, it could be considered a perfect system with great potential for diverse biotechnological applications as antioxidants, the development of functional foods, the synthesis of inorganic nanoparticles, and some pharmaceutical and environmental applications (Figure 1).
 
Figure 1. Potential technological applications of huitlacoche.
Mexico is a biologically diverse country characterized by its culture and traditional knowledge of gastronomy and medicine[6]. According to Molina-Castillo et al.[7], the Mexican food system could be classified into three categories: central (consumed every day, such as maize, beans, and chilies), secondary (consumed frequently, such as meat, eggs, potatoes, and tomatoes), and peripheral (consumed only during seasonal periods). In this context, Mexican cuisine is distinguished by including wild foods such as edible fungi based on their traditional knowledge and practice, particularly huitlacoche, consumed predominantly in the rural population[8][9]. Nonetheless, U. maydis and maize exhibited a related co-evolution associated with maize domestication and cultivation throughout the Americas, mainly in Mexico, which is considered the center of origin of maize but also where the Mexican diet is highly centered on corn-based products[10][11].The consumption of huitlacoche is endemic to Mexico[12][13]; its Nahuatl name (the language of Aztec civilizations) is derived from cuitla (excrement) and cochi (pig), which means pig’s excrement[14][15]. Currently, it is consumed and has been given numerous autochthonous names by more than 20 ancient Mexican ethnic groups, distributed mainly in Central and Southeastern Mexico but also in the north of the country[16]. In the Mixtec group (the third-largest indigen group after Nahua and Maya), it is called tɨká maa (tɨka = grasshopper; maa = bad), which means bad grasshopper[17]; meanwhile, it is called ta chak by the Mayas [18]. In some communities in Zacatecas, huitlacoche is called coloche or pitacoche[19]. In the Michoacan state (Purepecha culture), it is called terékua (means mushroom in Purepecha language), while it is called kjú tha in Otomí (Mexico state) and sunó weko wiwara in Rarámuri culture in the Chihuahua state[20]. In the Yucatan state (Maya culture), U. maydis is highly appreciated as food [21]. Nonetheless, in some Mayan and mestizo communities, this edible fungus is recollected for consumption within the family unit and is not collected for sale[4]. Additionally, the Wixarika culture (located in the northern region of Jalisco state) consumes huitlacoche (named Ki’au) as a food or ceremonial drink (tsinari or atole negro)[2]. Furthermore, huitlacoche is one of the most important edible fungi with cultural significance, nutritional value, and health benefits in one community of San Mateo Huexoyucan in the Tlaxcala state[17]. In the Chiapas state, it is used to prepare smoloc, a cold beverage, while in the Oaxaca state it is used to make “Mole negro”[2]. Presently, in Mexico, the consumption of huitlacoche is widely distributed, mainly in the center and southeast of the country (Figure 2).
Figure 2. Ethnic groups that give a traditional name to huitlacoche fungus in Mexico, and consumption distribution.
The origin of the consumption of huitlacoche as food has long been a matter of debate[22], since the documentary evidence is scarce, so it is reasonable to affirm that the beginning of its consumption is lost in the mists of time. One of the reasons for this fact is the enormous destruction of the pre-Hispanic codices after the conquest of Mexico by the Spaniards and the lack of knowledge related to the ethnic groups that inhabit the north of the country. However, the first documented evidence of the knowledge of this fungus in Mexico is found in the Florentine Codex, which dates back to the mid-16th century. In this Codex, two important pieces of evidence can be appreciated: (i) the first is an illustration of the fungus infecting a corn cob (Figure 3a); and (ii) the second is a detailed description in Nahuatl, the language of the Aztecs, which literally says “… Ear of corn that is born deformed, Cujtlacochi, it is black, dark, like a tamal (a traditional mexican dish), it looks like mud, it appears like mud. On green ears, on ripe ears it becomes ash, forms ash, turns ash…” (Figure 3b).
Figure 3. The most ancient evidence of huitlacoche in Mexico recorded in the Florentine Codex, dating from the mid-XVI century. (a) A figure of huitlacoche drawn by Aztec people, which appeared in Book 11, folio 251 of the Florentine Codex; (b) Description of the huitlacoche, called cujtlacochi, in the Nahuatl language, which appears in Book 11, folio 251 of the Florentine Codex. “Figures A and B are of public domain by the World Digital Library at: https://www.loc.gov/resource/gdcwdl.wdl_10622/?sp=501&st=image and https://www.loc.gov/resource/gdcwdl.wdl_10622/?sp=495&st=image&r=0.094,0.881,0.831,0.374,0 , respectively”. 
Huitlacoche is popular in Mexican cuisine because of its exotic flavor, which is acidic, astringent, earthy, bitter, and umami[23]. It is considered a delicacy and is used in a wide variety of food dishes (Figure 4a–f), including “antojitos mexicanos” as “quesadillas, tacos, tlacoyos, huaraches, sopes, enchiladas”; moreover, huitlacoche has been incorporated into modern food products such as soups, pasta, pizza, and bakes, among other things[24][25][26]. However, the most common way to prepare huitlacoche is by cooking it in a stir-fry in oil with onion, garlic, chili pepper, and epazote. Huitlacoche recipes can be found online and in some Mexican cookbooks.
Figure 4. Mexican mycogastronomy of huitlacoche: (ac) Traditional dishes; (df) Gourmet dishes; (a) Course of gastronomy of huitlacoche by a Mexican chef, taught to peasants in Piedra Canteada, Tlaxcala, in Central Mexico; (b) One of the most common dishes in which huitlacoche is consumed is called “quesadillas” in Spanish; (c) Different dishes using huitlacoche as the main ingredient; (d) Huitlacoche cream; (e) Fettuccini pasta containing huitlacoche; (f) Fettuccini gourmet dish containing huitlacoche.
Furthermore, huitlacoche can be sold fresh, canned (with or without other vegetables), or as a lyophilized/dehydrated product on the market (Figure 5a–c)[27]. In this context, using huitlacoche in food products with potential functional properties may be a viable alternative to its valorization, changing the perception of this natural resource as a corn pest[28]. In this context, its consumption has drawn a recent increasing interest worldwide (e.g., in Latin America, the United States, Japan, and Turkey) as a gourmet food[29][8].
Figure 5. Examples of different huitlacoche products commercialized in Mexico: (a) refrigerated galls; (b) brine in bottle; (c) canned products.
On the other hand, its ancestral medicinal use presents a different scenario, compared to that of its use as food. It can be affirmed that in Mexico it has been widely used since pre-Hispanic times by a large number of native cultures as medicine. Of the 200 species of medicinal mushrooms known in Mexico, the huitlacoche is the mushroom used most in traditional Mexican medicine. It is used to heal 55 illnesses in various ethnic groups, including: heart disease, colic, blisters, pimples, skin burns, athlete’s foot, wounds, nosebleeds, baby rashes, stopping hemorrhages, healing animal bites, alleviating dehydration, and helping with anxiety, as well as to treat diarrhea, indigestion, intestinal pains, and inflammations[29][30][31][32][33]. These beneficial effects could be attributed to the presence of various secondary metabolites (organic acids, phenolic compounds, and carotenoids) and to the fiber content of huitlacoche, including β-glucans that exert prebiotic properties[13][34][35]. Additionally, it has been used by an Otomi group in the state of Tlaxcala in Central Mexico as a cosmetic to enhance female beauty because of its properties to soften and refresh the skin. This ethnic group mixes the spores of the fungus with lemon juice and applies it to the face as a mask[36].

2. Potential Technological Applications of Huitlacoche

Several technological uses of huitlacoche have been associated with different bioactive molecules. These are antioxidants, the development of functional foods, biocontrol agent for wine, antimicrobial activity, the synthesis of inorganic nanoparticles, and some pharmaceutical and environmental applications, as discussed below.

2.1. Antioxidant Capacity

Various reactive oxygen species (ROS), including hydroxyl radicals, hydroxyl ions, and superoxide anions, are created in nature, even in the human body. Therefore, to neutralize these reactive substances, the consumption of food rich in antioxidant compounds is recommended[29]. In this context, basic techniques for estimating the antioxidant capacity of food systems include ABTS, DPPH, FRAP, and ORAC[37]. In general, huitlacoche exhibited good antioxidant properties (Table 1). Nonetheless, multiple extraction methods (maceration, ultrasound-assisted, stirring, and shaking) and various solvents (ethanol and methanol either alone or combined with water) can be used to obtain antioxidant extracts from huitlacoche samples[38][39][40][41]
Table 1. Antioxidant capacity of huitlacoche extracts.
Ethanolic extracts from huitlacoche powder have shown to exhibit antioxidant activity by ABTS (200–312 mmol of trolox equivalents (TE)/mL), DPPH (30–165 mmol TE/mL) and FRAP (11–251 mmol TE/mL); nonetheless, it has been reported that the antioxidant activity of huitlacoche is increased after a cooking process, associated with the release of phenolic compounds from the food matrix[41]. Similar trends were reported in fettuccine pasta supplemented with huitlacoche powder[24]. It has been reported that the antioxidant activity of huitlacoche extracts (cultivated in maize creole genotypes) measured by DPPH correlates (r = 0.6461) with the phenolic content[13][40]. Moreover, glycolipids from huitlacoche also exert antioxidant activity in ABTS radical scavenging tests[43]. On the other hand, it must be considered that the antioxidant capacity of huitlacoche is affected by its stage of development[13][34], its geographic location of cultivation[42], its extraction procedure, and the solvent used[38].
The bioaccessibility of phenolic compounds from huitlacoche and their antioxidant capacity during gastrointestinal digestion (in vitro) has been previously evaluated; this parameter indicated the potential intestinal absorption of the bioactive compounds and their availability during oral, gastric, and intestinal digestion. In this context, undigested huitlacoche contains phenolic compounds with antioxidant properties, which was found using DPPH and ABTS tests [13.94 mg of gallic acid equivalents (GAE)/g, 12.51 mg TE/g, and 9.58 mg TE/g, respectively]. Moreover, these values were increased during oral (19.76 mg GAE/g, 61.33 mg TE/g, and 32.73 mg TE/g, respectively) and gastric phases (30.22 mg GAE/g, 31.29 mg TE/g, and 64.71 mg TE/g, respectively). On the other hand, at the end of the gastric phase, a decrease of phenolic compounds was observed (6.79 mg GAE/g), but antioxidant capacity showed increased values compared to undigested samples (DPPH = 25.51 mg TE/g and ABTS = 40.54 mg TE/g). These results demonstrate that the consumption of huitlacoche provide antioxidant compounds with beneficial effects to the human body[38].
Evidence suggests that huitlacoche is an excellent source of natural antioxidants important for dietary consideration since they can stop or prevent oxidative stress in human cells promoted by free radicals. In this context, these results support the folkloric use of huitlacoche in Mexican ethnic groups to treat some ailments and its potential use in developing functional foods and nutraceutical products.

2.2. Development of Potential Functional Foods

Huitlacoche is an edible but highly perishable fungus (<3 days under ambient temperature); however, some strategies have been applied aimed at enhancing its shelf life[9]. In this context, huitlacoche has been explored as a functional ingredient to elaborate foods with potential health benefits in recent years[24][44][45]. The effect of huitlacoche flour addition on the functional and physicochemical properties of blue corn tortilla chips has been evaluated. An increase in total dietary fiber (↑175%), phenolic compounds (↑114%), and antioxidant capacity (↑18%) compared to the tortilla chip without huitlacoche-added flour has been found. Moreover, the color of the tortilla chips was influenced by adding huitlacoche flour (black color) in a dose-dependent response. On the other hand, there was an increased breaking force as the huitlacoche content increased, and no significant increase in protein, lipids, and moisture content was observed by adding huitlacoche flour to tortilla chips[45]. Furthermore, it has been reported that adding huitlacoche powder can improve the physicochemical, rheological, and thermal properties of blue corn flour and “masa” and modify the color of blue corn flour and “masa”, changing it from a blue to a black color. However, in an industrial process, huitlacoche only makes up 9% of the total weight of the ingredients used in the formulation of blue corn flour and “masa” due to effect on the cohesiveness and adhesiveness of the resultant products.
Fettuccine pasta supplemented with huitlacoche powder (5 to 25% in weight) has shown a significant increase in dietary fiber (1.93 g/100 g), phenolic compounds (↑300%), and antioxidant activity (↑100%) content, in a huitlacoche concentration-dependent manner compared to the control paste (dietary fiber = 0.01 g/100 g); moreover, the addition of huitlacoche did not alter the technological properties (cooking time, cooking loss, water absorption, water solubility, swelling powder, ad density) of fettuccine pasta[24].
The use of the chlorogenic acid esterase (enzyme isolated from U. maydis) to make bakery products had positive softening effects. The addition of this enzyme improves the dough’s rheological parameters; moreover, the enzyme exhibited low thermostability, which is an advantage for baking. In this context, this enzyme could be a technological alternative to improve the taste and digestibility of diverse food products, mainly those rich in chlorogenic acid because their astringency characterizes this kind of product[46].
Functionalizing traditional and modern food products using huitlacoche flour is a technological alternative to promote the consumption of this fungal resource. It can be added to bakery and corn-based food products, increasing the dietary fiber and antioxidant molecules of foods that provide human health effects.

2.3. Biocontrol Agent for Wine Production

Although Brettanomyces bruxellenis, a spoilage yeast, has a considerable impact on wine production, few tools are available to control its proliferation. In this regard, U. maydis CTC 1410 can produce a killer toxin (KP6-related toxin) that is effective against B. bruxellenis at low concentrations (400–2000 UA/mL) and acidic conditions (pH values from 3 to 4.5). This toxin is a small protein (encoded by dsRNA mycoviruses) that can be employed as a biological control strategy for wine production at the beginning of fermentation and aging[47].

2.4. Antimicrobial Activity

A vast and mostly untapped source of bioactive compounds with potential biotechnological uses is found in fungus secondary metabolites[48]. The antimicrobial properties of U. maydis extracts or isolated compounds against bacteria, yeast, and molds have also been investigated. Glycolipids (by U. maydis FBD12) exhibited antimicrobial activity against Staphylococcus aureus and Salmonella enterica var. Typhimurium at low doses (MIC value of 0.01 to 0.04 mg/mL) after 24 h of exposure[43]. The antimicrobial effect of glycolipids is explained by an alteration of membrane permeability, promoting cell death. Furthermore, glycolipids (Ustilagic acid C and B) from U. maydis exhibited moderate antifungal activity (MIC values of 50 to 100 µg/mL) against Aspergillus terreus and Candida albicans[49]. Additionally, it has been reported that Mannosylerythritol lipids exhibited antimicrobial effects against Bacillus subtilis in a concentration-dependent response[50]. In this context, U. maydis could be a good source of antimicrobial compounds with potential pharmaceutical and food industry applications.

2.5. Miscellaneous Applications

U. maydis is widely used in traditional medicine to treat diverse ailments; these beneficial effects are attributed to compounds with biological activities. Therefore, U. maydis has been explored for potential pharmaceutical applications, as discussed below.
Ustilipids are compounds extracted from the mycelium of U. maydis that exhibit dopaminergic properties; they act as antagonists of dopamine D2 and D3 receptors, which may be associated with the fatty acid profile of these compounds that include oleic, linoleic, stearic, palmitic, myristic, capric, caprylic, and caproic acids, indicating the pharmacological potential of ustilipids in the treatment of some neuroleptic diseases[51].
Additionally, it has been reported that Ustilagol compounds isolated from U. maydis MZ496986 exert antiplatelet and anti-inflammatory properties. Ustilagol G exhibited strong antiplatelet aggregation (IC50 = 16.5 µM) in U46619-stimulated human platelets, similar to that observed with aspirin (IC50 = 62.8 µM). Moreover, Ustilagol C and Ustilagol E showed anti-inflammatory properties in an LPS-induced macrophage RAW 264.7 model, associated with the structural configuration of these compounds and the ubication of methoxy groups at C-1, reducing NF-κB; however, the effect was in a dose-dependent response. These compounds could be explored as an alternative for neurodegenerative diseases[18].
The antimutagenic activity of U. maydis methanolic extracts from raw and cooked samples using a Salmonella typhimurium histidine reversion (his to his+) has been evaluated. These extracts showed antimutagenic activity ranging from 41 to 76%; however, these effects depended on maize genotype, the stage of maturity, and the cooking method. The antimutagenic activity of U. maydis extracts appears to be acceptable[40].
The antitumoral properties of Ustilagomaydisin A–C on multi-drug-resistant tumors has also been explored. These compounds are purine-derived compounds isolated from ethanolic extracts of U. maydis. These compounds have been shown to be weakly active against K562/A02 human leukemia cells compared to the drug verapamil[52].
The potential use of U. maydis as a platform to produce oral vaccines for cholera toxins has also been studied[53]. For this, huitlacoche has undergone genetic engineering to examine the expression and immunogenicity of the cholera toxin’s B subunit (CTB, secreted by Vibrio cholerae). Then, 12-week-old female BALB/c mice previously immunized with the oral vaccine based on recombinant CTB protein were challenged with the cholera toxin. Mice given an oral dose of CTB produced from huitlacoche exhibited substantial humoral responses linked with protection from the cholera toxin challenge. Furthermore, the oral vaccine maintained its immunogenetic activity after one year of storage at room temperature without reduction in CTB at 50 °C for 2 h, indicating its stability and immunogen effectivity[54].
According to these data, various extracts of isolated compounds of U. maydis can exert dopaminergic, antiplatelet, anti-inflammatory, antimutagenic, and antitumoral effects, which warrant additional research regarding the specific mechanisms of action and possible applications. Moreover, U. maydis could be an effective, safe, and low-cost platform for developing oral vaccines.

2.6. Synthesis of Inorganic Nanoparticles

In recent years, the green synthesis of inorganic nanoparticles has exhibited a growing trend because it is an easy, rapid, eco-friendly, and low-cost alternative compared to the traditional chemical routes. In this context, natural resources able to act as reducing and stabilizing agents are needed during synthesis. Cortés-Camargo et al.[55] recently used huitlacoche aqueous extract as a reducing and stabilizing agent for synthetizing silver (Ag) nanoparticles. They found that the aqueous extract of huitlacoche is a good reducing agent (from AgNO3 to Ag) due to the high content of amino acids. Nonetheless, it acts as a stabilizing agent (zeta potential of −10.75 mV), avoiding the agglomeration and sedimentation of Ag nanoparticles, which exhibited quasi-spherical shapes within 100 to 5000 nm. Similarly, Bakur et al.[56] synthesized Au nanoparticles using mannosylerythritol lipid (MEL, obtained from U. maydis fermentation) as a reducing and capping agent under alkaline conditions. They found that MELs could reduce HAuCl4 to obtain Au nanoparticles with spherical shapes, associated with their biosurfactant properties. These materials exhibited in vitro antimicrobial, anticancer, and antioxidant activities. According to these data, U. maydis (extracts or compounds) could be a technological alternative as a reducing/stabilizing agent to the synthesis of inorganic nanoparticles with biological activities by green synthesis methods.

2.7. Bioremediation

Every day, increasinh numbers of pollutants are released into all kinds of open waters; therefore, water treatment has received a lot of attention. In this context, U. maydis has been investigated as a biological alternative for heavy metal removal. Serrano-Gómez et al.[57] reported that the modification of U. maydis with formaldehyde can facilitate Cr(VI) biosorption from aqueous solutions in a pH-dependent manner. According to the authors, the adsorption of Cr(VI) is achieved in acidic conditions by electrostatic binding between the negative charge of the anion Cr(VI) and the positive charge of NH3+ groups (after the protonation of the -NH2 group), which are associated with the amino acids of U. maydis. Additionally, it has been reported that the biosorption of heavy metals such as Cr(III), Cd(II), Cu(II), Zn(II), and Ni(II) was successfully assessed using chitosan microcapsules functionalized with immobilized microfungal spores of U. maydis. However, the initial metal ion concentration, temperature, time, pH, and amount of sorbent all affect how effective this hybrid material is[58]. According to these data, U. maydis could be used as a potential bioremediation agent to remove heavy metals from aqueous media.

2.8. Other Investigated Applications

Merkevičiūte-Venslovė et al.[59] evaluated the effect of U. maydis on the quality (nutritive value and aerobic deterioration) of maize silage. They prepared 50% and 100% silage infected with U. maydis. After 90 days, silage produced from maize that was 50% and 100% U. maydis-infected exhibited poor quality (↓protein and fiber content), with decreased dry matter loss (↓1.2% and 8%, respectively) and decreased starch (↓12.5% and 33%, respectively) content compared to U. maydis free silage. They concluded that U. maydis negatively affects the quality of maize silage, probably due to the influence of this fungal resource with aerobic bacteria that promotes the fermentative process. On the other hand, they also mentioned that the silage that was 50% and 100% U. maydis-infected did not promote any adverse effect on livestock health and production.

3. Conclusions

In summary huitlacoche is one of the most important edible fungi with biocultural significance in Mexico; currently, it is traditionally consumed by diverse ethnic groups, and it is also used in a wide variety of food dishes throughout the country. Moreover, this fungal resource is a crop with agro-alimentary importance and is a functional food with commercial value. Evidence shows that huitlacoche is a valuable food source with high nutritional value and bioactive compounds that can stabilizing and capping agents for inorganic nanoparticle synthesis, involved in the remotion of heavy metals from aqueous media, biocontrol agents for wine production, and also have industrial potential, e.g., by producing biosurfactant compounds and enzymes [60]

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