Aspergillus flavus

Last updated

Aspergillus flavus
Aspergillus flavus.jpg
A conidiophore of A. flavus
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Eurotiomycetes
Order: Eurotiales
Family: Aspergillaceae
Genus: Aspergillus
Species:
A. flavus
Binomial name
Aspergillus flavus
Link (1809)
Aspergillus flavus in a petri dish Aspergillus flavus in petri dish.png
Aspergillus flavus in a petri dish

Aspergillus flavus is a saprotrophic and pathogenic [1] fungus with a cosmopolitan distribution. [2] It is best known for its colonization of cereal grains, legumes, and tree nuts. Postharvest rot typically develops during harvest, storage, and/or transit. Its specific name flavus derives from the Latin meaning yellow, a reference to the frequently observed colour of the spores. A. flavus infections can occur while hosts are still in the field (preharvest), but often show no symptoms (dormancy) until postharvest storage or transport. In addition to causing preharvest and postharvest infections, many strains produce significant quantities of toxic compounds known as mycotoxins, which, when consumed, are toxic to mammals. [3] A. flavus is also an opportunistic human and animal pathogen, causing aspergillosis in immunocompromised individuals. [4]

Contents

Hosts

Aspergillus flavus is found globally as a saprophyte in soils and causes disease on many important agriculture crops. Common hosts of the pathogen are cereal grains, legumes, and tree nuts. Specifically, A. flavus infection causes ear rot in corn and yellow mold in peanuts either before or after harvest. [4] Infection can be present in the field, preharvest, postharvest, during storage, and during transit. It is common for the pathogen to originate while host crops are still in the field; however, symptoms and signs of the pathogen are often unseen. A. flavus has the potential to infect seedlings by sporulation on injured seeds. In grains, the pathogen can invade seed embryos and cause infection, which decreases germination and can lead to infected seeds planted in the field. The pathogen can also discolor embryos, damage seedlings, and kill seedlings, which reduces grade and price of the grains. The incidence of A. flavus infection increases in the presence of insects and any type of stress on the host in the field as a result of damage. Stresses include stalk rot, drought, severe leaf damage, and/or less than ideal storage conditions. [3] Generally, excessive moisture conditions and high temperatures of storage grains and legumes increase the occurrence of A. flavus aflatoxin production. [4] In mammals, the pathogen can cause liver cancer through consumption of contaminated feed or aspergillosis through invasive growth. [4]

Morphology and pathology

Aspergillus flavus colonies are commonly powdery masses of yellowish-green spores on the upper surface and reddish-gold on the lower surface. In both grains and legumes, infection is minimized to small areas, and discoloration and dullness of affected areas is often seen. Growth is rapid and colonies appear powdery in texture. [5]

Hyphal growth usually occurs by thread-like branching and produces mycelia. Hyphae are septate and hyaline. Once established, the mycelium secretes degradative enzymes or proteins which can break down complex nutrients (food). Individual hyphae strands are not typically seen by the unaided eye; however, conidia producing thick mycelial mats are often seen. The conidiospores are asexual spores produced by A. flavus during reproduction. [5] [6] [7]

The conidiophores of A. flavus are rough and colorless. Phialides are both uniseriate (arranged in one row) and biseriate. [5]

Recently, Petromyces was identified as the sexual reproductive stage of A. flavus, where the ascospores develop within sclerotia. [4] The sexual state of this heterothallic fungus arises when strains of opposite mating type are cultured together. [8] Sexual reproduction occurs between sexually compatible strains belonging to different vegetative compatibility groups.

Aspergillus flavus is complex in its morphology and can be classified into two groups based on the size of sclerotia produced. Group I consists of L strains with sclerotia greater than 400 μm in diameter. Group II consists of S strains with sclerotia less than 400 μm in diameter. Both L and S strains can produce the two most common aflatoxins (B1 and B2). Unique to the S strains is the production of aflatoxin G1 and G2 which typically are not produced by A. flavus. [4] The L strain is more aggressive than the S strain, but produces less aflatoxin in culture. The L strain also has a more acidic homoeostatic point and produces less sclerotia than the S strain under more limiting conditions. [9]

Disease cycle

Aspergillus flavus overwinters in the soil and appears as propagules on decaying matter, either as mycelia or sclerotia. Sclerotia germinate to produce additional hyphae and asexual spores called conidia. These conidia are said to be the primary inoculum for A. flavus. The propagules in the soil, which are now conidia, are dispersed by wind and insects (such as stink bugs or lygus bugs). The conidia can land on and infect either grains or legumes. The spores enter the corn through the silks and thus infect the kernel. Conidiophores and conidia are produced in the spring from sclerotial surfaces. There is a secondary inoculum for A. flavus, which is conidia on leaf parts and leaves. A. flavus grows on leaves after damage by leaf-feeding insects. Insects are said to be a source of inoculum and promote inoculum production. [10] [11]

Environment

Aspergillus flavus is unique in that it is a thermotolerant fungus, so can survive at temperatures that other fungi cannot.[ citation needed ]A. flavus can contribute to the storage rots, especially when the plant material is stored at high moisture levels. A. flavus grows and thrives in hot and humid climates. [10]

Temperature: A. flavus has a minimum growth temperature of 12 °C (54 °F) and a maximum growth temperature of 48 °C (118 °F). Though the maximum growth temperature is around 48 °C (118 °F), the optimum growth temperature is 37 °C (99 °F). A. flavus had rapid growth at 30–55 °C (86–131 °F), slow growth at 12–15 °C (54–59 °F), and almost ceases growth at 5–8 °C (41–46 °F). [3] [12]

Moisture: A. flavus growth occurs at different moisture levels for different crops. For starchy cereals, growth occurs at 13.0–13.2%. For soybeans, growth occurs at 11.5–11.8%. For other crops, growth occurs at 14%. [3] A. flavus growth is prevalent in tropical countries. [4] Minimum aw (water activity) required for growth is inversely correlated with temperature – in other words higher temperatures permit lower aw. This is known to range from aw 0.78 at 33 °C (91 °F) to 0.84 at 25 °C (77 °F). Gibson et al 1994 provides a model relating expected growth rate to aw x temperature parameters. [13]

Management

To ensure grains and legumes remain free of A. flavus infection, certain conditions must be incorporated before, during, and after harvest. Moisture levels should be kept below 11.5%. Temperature in storage units should be kept as low as possible since the pathogen is unable to grow below 5 °C. The low temperature facilitates slower respiration and prevents moisture increase. Fumigants are used to decrease the occurrence and persistence of insects and mites, which aids the rapid growth of the pathogen. Sanitary practices including, removing old and unripe seeds, exclusion of damaged and broken seeds, and overall cleanliness assist in minimizing the colonization and spread of the pathogen. [3]

The most common management practice for grains and legumes is the use of aeration systems. Air is pushed through the storage bins at low flow rates, which removes excess moisture and heat. Regulation of air flow allows the moisture content in harvested products to remain at a constant level and decreases the temperature within the bins. Temperature levels can decrease enough so insects and mites are dormant, which reduces rapid growth of the pathogen. [3]

Some environmental control practice have been explored to aid in the reduction of A. flavus infection. Resistant crop lines have shown little to no protection against unfavorable environmental conditions. However, good irrigation practices aid in the reduction of stress brought upon by drought, which in turn, reduces the likelihood of pathogen infection. Some research has been done in identifying particular plant proteins, both pathogen-related and drought-resistant proteins, that defend against A. flavus entry. [4]

To protect tree nuts and corn plants affected by A. flavus, scientists of the Agricultural Research Service found that treating these plants with the yeast Pichia anomala reduced the growth of A. flavus. The study showed that treating pistachio trees with P. anomala inhibited the growth of A. flavus up to 97% when compared to untreated trees. [14] The yeast successfully competes with A. flavus for space and nutrients, ultimately limiting its growth. [15]

Essential oils of Glycyrrhiza glabra inhibit growth. [16]

Aspergillus flavus AF36

Aspergillus flavus strain AF36 is noncarcinogenic and aflatoxin-free and is used as an active ingredient in pesticides. AF36 is a fungal antagonist and is applied as a commercial biocontrol to cotton and corn to reduce aflatoxin exposure. AF36 was initially isolated in Arizona and has also occurred in Texas. It is grown on sterile seeds which serve as the carrier and a source of nutrients. Following application and colonization and in the presence of high moisture, AF36 growing seeds outcompete aflatoxin-producing strains of A. flavus. Nonaflatoxin spore dispersal is aided by wind and insects. [17] [18]

Importance

Aspergillus flavus infections will not always reduce crop yields alone; however, postharvest disease can reduce the total crop yield by 10 to 30%, and in developing countries that produce perishable crops, total loss can be greater than 30%. In grains and legumes, postharvest disease results in the production of mycotoxins. [3] The largest economic loss caused by this pathogen is a result of aflatoxin production. In the United States, annual economic loss estimations of peanuts, corn, cottonseed, walnuts, and almonds are less severe when compared to Asia and Africa. [4]

After Aspergillus fumigatus , A. flavus is the second-leading cause of aspergillosis. Primary infection is caused by the inhalation of spores; bigger spores have a better chance of settling in the upper respiratory tract. The deposition of certain spore sizes could be a leading factor for why A. flavus is a common etiological cause of fungal sinusitis and cutaneous infections and noninvasive fungal pneumonia. Countries with dry weather, such as Saudi Arabia and most of Africa, are more prone to aspergillosis. Two allergens have been characterized in A. flavus: Asp fl 13 and Asp fl 18. In tropical and warm climates, A. flavus has been shown to cause keratitis in about 80% of infections. A. flavus infection is typically treated with antifungal drugs such as amphotericin B, itraconazole, voriconazole, posaconazole, and caspofungin; however, some antifungal resistance has been shown in amphotericin B, itraconazole, and voriconazole. [10]

Aflatoxin

In 1960 on an English farm, about 100,000 turkeys died. Investigation into the cause of death showed the primary food source, peanut meal, was infected with A. flavus. The culture was isolated, grown in pure culture, and a subset of healthy turkeys was infected. The pure culture isolate caused death in the healthy turkeys. Chemical investigation into the cause of death showed the production of four toxic chemicals, named aflatoxins after being discovered in A. flavus. Turkey necropsies showed aflatoxins targeted the liver and either completely killed the tissue cells or induced tumor formation. The discovery of aflatoxins led to substantial changes in agricultural practices and regulations on how grains and legumes were grown, harvested, and stored. [19]

The amount of aflatoxins produced by A. flavus is affected by environmental factors. If other competitive fungal organisms are present on host plants, aflatoxin production is low. However, if noncompetitive fungal organisms are present on host plants, aflatoxin production can be quite high. The nature of the host is also an important factor in aflatoxin production. High A. flavus growth on soybean produces very little aflatoxin. High A. flavus growth aided by increased moisture content and warm temperatures on peanut, nutmeg, and peppers produces high concentrations of aflatoxins. A. flavus growth on spices produces low concentrations of aflatoxin as long as the spices remain dry. [19]

Species sensitivity is highly variable when exposed to aflatoxins. Rainbow trout are highly sensitive at 20 ppb, causing liver tumor development in half the population. White rats develop liver cancer when exposed to 15 ppb. [19] Young piglets, ducklings, and turkeys exposed to high doses of aflatoxin become sick and die. Pregnant cows, mature pigs, cattle, and sheep exposed to low doses of aflatoxin over long periods develop weakening, intestinal bleeding, debilitation, reduced growth, nausea, no appetite, and predisposition to other infections. [3]

The four major aflatoxins produced are B1, B2, G1, and G2. The production of the major toxins is a result of particular strains of A. flavus. Aflatoxin B1 is the most toxic and potent hepatocarcinogenic natural compound characterized. A. flavus also produces other toxic compounds including sterigmatocystin, cyclopiazonic acid, kojic acid, β-nitropropionic acid, aspertoxin, aflatrem, gliotoxin, and aspergillic acid. [10]

In humans, A. flavus aflatoxin production can lead to acute hepatitis, immunosuppression, hepatocellular carcinoma, and neutropenia. The absence of any regulation of screening for the fungus in countries that also have a high prevalence of viral hepatitis highly increases the risk of hepatocellular carcinoma. [20] The deaths of ten conservationists present at the opening of a 15th century tomb in Kraków, Poland in the 1970s has been attributed to aflatoxins originating from A. flavus present in the tomb. [21] [22]

After the premature death of several Polish scientists following the 1973 opening of the tomb of the 15th century Polish King (and Lithuanian Grand Duke) Casimir IV Jagiellon, microbiologist Bolesław Smyk identified the presence of the fungus Aspergillus flavus in samples taken from the tomb, and media reports have suggested that the likely cause of the deaths were the aflatoxins produced by this fungus. [23]

It has since been suggested that it may also have contributed to some of the deaths following the 1922 discovery and subsequent opening of the tomb of Egyptian Pharaoh Tutankhamun, particularly the deaths of Lord Carnarvon, George Jay Gould, and Arthur Mace, [23] [24] though the link has been disputed (at least in Carnarvon's case). [24]

Related Research Articles

<span class="mw-page-title-main">Aflatoxin</span> Group of poisons produced by moulds

Aflatoxins are various poisonous carcinogens and mutagens that are produced by certain molds, particularly Aspergillus species mainly by Aspergillus flavus and Aspergillus parasiticus. According to the USDA, "They are probably the best known and most intensively researched mycotoxins in the world." The fungi grow in soil, decaying vegetation and various staple foodstuffs and commodities such as hay, maize, peanuts, coffee, wheat, millet, sorghum, cassava, rice, chili peppers, cottonseed, tree nuts, sesame seeds, sunflower seeds, and various cereal grains and oil seeds. In short, the relevant fungi grow on almost any crop or food. When such contaminated food is processed or consumed, the aflatoxins enter the general food supply. They have been found in both pet and human foods, as well as in feedstocks for agricultural animals. Animals fed contaminated food can pass aflatoxin transformation products into milk, milk products, and meat. For example, contaminated poultry feed is the suspected source of aflatoxin-contaminated chicken meat and eggs in Pakistan.

<i>Botrytis cinerea</i> Species of fungus

Botrytis cinerea is a necrotrophic fungus that affects many plant species, although its most notable hosts may be wine grapes. In viticulture, it is commonly known as "botrytis bunch rot"; in horticulture, it is usually called "grey mould" or "gray mold".

<span class="mw-page-title-main">Texas root rot</span> Pathogenic fungus

Texas root rot is a disease that is fairly common in Mexico and the southwestern United States resulting in sudden wilt and death of affected plants, usually during the warmer months. It is caused by a soil-borne fungus named Phymatotrichopsis omnivora that attacks the roots of susceptible plants. It was first discovered in 1888 by Pammel and later named by Duggar in 1916.

<i>Aspergillus fumigatus</i> Species of fungus

Aspergillus fumigatus is a species of fungus in the genus Aspergillus, and is one of the most common Aspergillus species to cause disease in individuals with an immunodeficiency.

<i>Aspergillus</i> Genus of fungi

Aspergillus is a genus consisting of several hundred mold species found in various climates worldwide.

<i>Uncinula necator</i> Species of fungus

Uncinula necator is a fungus that causes powdery mildew of grape. It is a common pathogen of Vitis species, including the wine grape, Vitis vinifera. The fungus is believed to have originated in North America. European varieties of Vitis vinifera are more or less susceptible to this fungus. Uncinula necator infects all green tissue on the grapevine, including leaves and young berries. It can cause crop loss and poor wine quality if untreated. The sexual stage of this pathogen requires free moisture to release ascospores from its cleistothecia in the spring. However, free moisture is not needed for secondary spread via conidia; high atmospheric humidity is sufficient. Its anamorph is called Oidium tuckeri.

<span class="mw-page-title-main">Phomopsis cane and leaf spot</span> Fungal plant disease

Phomopsis cane and leaf spot occurs wherever grapes are grown. Phomopsis cane and leaf spot is more severe in grape-growing regions characterized by a humid temperate climate through the growing season. Crop losses up to 30% have been reported to be caused by Phomopsis cane and leaf spot.

<i>Aspergillus terreus</i> Species of fungus

Aspergillus terreus, also known as Aspergillus terrestris, is a fungus (mold) found worldwide in soil. Although thought to be strictly asexual until recently, A. terreus is now known to be capable of sexual reproduction. This saprotrophic fungus is prevalent in warmer climates such as tropical and subtropical regions. Aside from being located in soil, A. terreus has also been found in habitats such as decomposing vegetation and dust. A. terreus is commonly used in industry to produce important organic acids, such as itaconic acid and cis-aconitic acid, as well as enzymes, like xylanase. It was also the initial source for the drug mevinolin (lovastatin), a drug for lowering serum cholesterol.

<i>Alternaria solani</i> Species of fungus

Alternaria solani is a fungal pathogen that produces a disease in tomato and potato plants called early blight. The pathogen produces distinctive "bullseye" patterned leaf spots and can also cause stem lesions and fruit rot on tomato and tuber blight on potato. Despite the name "early," foliar symptoms usually occur on older leaves. If uncontrolled, early blight can cause significant yield reductions. Primary methods of controlling this disease include preventing long periods of wetness on leaf surfaces and applying fungicides. Early blight can also be caused by Alternaria tomatophila, which is more virulent on stems and leaves of tomato plants than Alternaria solani.

<i>Colletotrichum coccodes</i> Pathogenic fungus

Colletotrichum coccodes is a plant pathogen, which causes anthracnose on tomato and black dot disease of potato. Fungi survive on crop debris and disease emergence is favored by warm temperatures and wet weather.

<i>Botrytis fabae</i> Species of fungus

Botrytis fabae is a plant pathogen, a fungus that causes chocolate spot disease of broad or fava bean plants, Vicia faba. It was described scientifically by Mexican-born Galician microbiologist Juan Rodríguez Sardiña in 1929.

Pathogenic fungi are fungi that cause disease in humans or other organisms. Although fungi are eukaryotic, many pathogenic fungi are microorganisms. Approximately 300 fungi are known to be pathogenic to humans; their study is called "medical mycology". Fungal infections are estimated to kill more people than either tuberculosis or malaria—about two million people per year.

Aspergillus ochraceus is a mold species in the genus Aspergillus known to produce the toxin ochratoxin A, one of the most abundant food-contaminating mycotoxins, and citrinin. It also produces the dihydroisocoumarin mellein. It is a filamentous fungus in nature and has characteristic biseriate conidiophores. Traditionally a soil fungus, has now began to adapt to varied ecological niches, like agricultural commodities, farmed animal and marine species. In humans and animals the consumption of this fungus produces chronic neurotoxic, immunosuppressive, genotoxic, carcinogenic and teratogenic effects. Its airborne spores are one of the potential causes of asthma in children and lung diseases in humans. The pig and chicken populations in the farms are the most affected by this fungus and its mycotoxins. Certain fungicides like mancozeb, copper oxychloride, and sulfur have inhibitory effects on the growth of this fungus and its mycotoxin producing capacities.

<i>Aspergillus candidus</i> Species of fungus

Aspergillus candidus is a white-spored species of fungus in the genus Aspergillus. Despite its lack of pigmentation, it is closely related to the most darkly-pigmented aspergilli in the Aspergillus niger group. It is a common soil fungus worldwide and is known as a contaminant of a wide array of materials from the indoor environment to foods and products. It is an uncommon agent of onychomycosis and aspergillosis. The species epithet candidus (L.) refers to the white pigmentation of colonies of this fungus. It is from the Candidi section. The fungi in the Candidi section are known for their white spores. It has been isolated from wheat flour, djambee, and wheat grain.

Cladosporium fulvum is an Ascomycete called Passalora fulva, a non-obligate pathogen that causes the disease on tomatoes known as the tomato leaf mold. P. fulva only attacks tomato plants, especially the foliage, and it is a common disease in greenhouses, but can also occur in the field. The pathogen is likely to grow in humid and cool conditions. In greenhouses, this disease causes big problems during the fall, in the early winter and spring, due to the high relative humidity of air and the temperature, that are propitious for the leaf mold development. This disease was first described in the North Carolina, by Mordecai Cubitt Cooke (1883), on cultivated tomato, although it is originally from South and Central America. The causal fungus of tomato leaf mold may also be referred to as Cladosporium fulvum, a former name.

<i>Penicillium digitatum</i> Species of fungus

Penicillium digitatum is a mesophilic fungus found in the soil of citrus-producing areas. It is a major source of post-harvest decay in fruits and is responsible for the widespread post-harvest disease in Citrus fruit known as green rot or green mould. In nature, this necrotrophic wound pathogen grows in filaments and reproduces asexually through the production of conidiophores and conidia. However, P. digitatum can also be cultivated in the laboratory setting. Alongside its pathogenic life cycle, P. digitatum is also involved in other human, animal and plant interactions and is currently being used in the production of immunologically based mycological detection assays for the food industry.

<i>Botrytis squamosa</i> Species of fungus which can damage onion crops

Botrytis squamosa is a fungus that causes leaf blight on onion that is distinctly characterized by the two stages – leaf spotting followed by blighting. The pathogen is an ascomycete that belongs to the family Sclerotiniaceae in the order Helotiales. The lesions start out as whitish streaks and take on a yellow tinge as they mature. They cause yield losses up to 30%. This fungus is endemic to the USA and has also been reported in Europe, Asia, and Australia. Typical management of this disease includes chemical fungicides with significant efforts being made to establish a means of biological control.

<i>Aspergillus parasiticus</i> Species of fungus

Aspergillus parasiticus is a fungus belonging to the genus Aspergillus. This species is an unspecialized saprophytic mold, mostly found outdoors in areas of rich soil with decaying plant material as well as in dry grain storage facilities. Often confused with the closely related species, A. flavus, A. parasiticus has defined morphological and molecular differences. Aspergillus parasiticus is one of three fungi able to produce the mycotoxin, aflatoxin, one of the most carcinogenic naturally occurring substances. Environmental stress can upregulate aflatoxin production by the fungus, which can occur when the fungus is growing on plants that become damaged due to exposure to poor weather conditions, during drought, by insects, or by birds. In humans, exposure to A. parasiticus toxins can cause delayed development in children and produce serious liver diseases and/or hepatic carcinoma in adults. The fungus can also cause the infection known as aspergillosis in humans and other animals. A. parasiticus is of agricultural importance due to its ability to cause disease in corn, peanut, and cottonseed.

Cladosporium ear rot is a disease that affects maize. The disease is caused by the saprophytic fungus Cladosporium herbarum and is characterized by black or dark green fungal growths that cause black streaks on kernels.

Aspergillus wentii is an asexual, filamentous, endosymbiotic fungus belonging to the mold genus, Aspergillus. It is a common soil fungus with a cosmopolitan distribution, although it is primarily found in subtropical regions. Found on a variety of organic materials, A. wentii is known to colonize corn, cereals, moist grains, peanuts and other ground nut crops. It is also used in the manufacture of biodiesel from lipids and is known for its ability to produce enzymes used in the food industry.

References

  1. ↑ Masayuki Machida; Katsuyai Gomi (2010). Aspergillus: Molecular Biology and Genomics. Horizon Scientific Press. p. 157. ISBN   978-1-904455-53-0.
  2. ↑ Ramírez-Camejo, L. A.; Zuluaga-Montero, A.; Lázaro-Escudero, M. A.; Hernández-Kendall, V. N.; Bayman, P. (2012). "Phylogeography of the cosmopolitan fungus Aspergillus flavus: Is everything everywhere?". Fungal Biology. 116 (3): 452–463. doi:10.1016/j.funbio.2012.01.006. PMID   22385627.
  3. 1 2 3 4 5 6 7 8 Agrios, George N. (2005). Plant Pathology: Fifth Edition. Elsevier Academic Press. p. 922. ISBN   978-0-12-044565-3.
  4. 1 2 3 4 5 6 7 8 9 Amaike, Saori; Nancy P. Keller (2011). "Aspergillus flavus". Annual Review of Phytopathology. 49: 107–133. doi:10.1146/annurev-phyto-072910-095221. PMID   21513456.
  5. 1 2 3 "Aspergillus Species". The Fungi: Descriptions. doctorfungus. Archived from the original on 20 November 2010. Retrieved 23 October 2012.
  6. ↑ "Aspergillus". Microbe Wiki. Microbewiki. Retrieved 23 October 2012.
  7. ↑ Alexopoulos, C.J. (1996). Introductory Mycology. John Wiley & Sons, Inc. p. 869. ISBN   978-0-471-52229-4.
  8. ↑ Horn BW, Moore GG, Carbone I (2009). "Sexual reproduction in Aspergillus flavus". Mycologia. 101 (3): 423–9. doi:10.3852/09-011. PMID   19537215. S2CID   20648447.
  9. ↑ "Archived copy" (PDF). Archived from the original (PDF) on 2016-03-05. Retrieved 2014-06-25.{{cite web}}: CS1 maint: archived copy as title (link)
  10. 1 2 3 4 Hedayati, M.T.; A.C. Pasqualotto; P.A. Warn; P. Bowyer; D.W. Denning (2007). "Aspergillus flavus: human pathogen, allergen, and mycotoxin producer". Microbiology. 153 (6): 1677–1692. doi: 10.1099/mic.0.2007/007641-0 . PMID   17526826.
  11. ↑ Diener, U.L.; R.J. Cole; T.H. Sanders; G.A. Payne; L.S. Lee; M.A. Klich (1987). "Epidemiology of aflatoxin formation by Aspergillus flavus". Annual Review of Phytopathology. 25: 249–270. doi:10.1146/annurev.phyto.25.1.249.
  12. ↑ "Aspergillus flavus". Center for Integrated Fungal Research. Archived from the original on 2013-06-09. Retrieved 2012-12-05.
  13. ↑ Pitt, John (2009). Fungi and food spoilage. New York City: Springer-Verlag. ISBN   978-0-387-92206-5. OCLC   437346680. ISBN   978-1-4899-8409-8. ISBN   978-0-387-92207-2.
  14. ↑ "Helpful Yeast Battles Food-Contaminating Aflatoxin : USDA ARS". www.ars.usda.gov.
  15. ↑ "Helpful Yeast Battles Food-Contaminating Aflatoxin". USDA Agricultural Research Service. January 27, 2010.
  16. ↑ Mamedov, Nazim A.; Egamberdieva, Dilfuza (2019). "Phytochemical Constituents and Pharmacological Effects of Licorice: A Review". Plant and Human Health, Volume 3. Cham: Springer Publishing. pp. 1–21. doi:10.1007/978-3-030-04408-4_1. ISBN   978-3-030-04407-7. S2CID   104427400.
  17. ↑ "Aspergillus flavus strain AF36 (006456) Fact Sheet" (PDF). Environmental Protection Agency. Archived from the original (PDF) on 2014-07-15.
  18. ↑ "Aspergillus flavus AF36" (PDF). Arizona Experimental Pesticides. Ag.Arizona.edu. Archived from the original (PDF) on 2015-05-13.
  19. 1 2 3 Hudler, George W. (1998). Magical mushrooms, Mischievous Molds . Princeton, New Jersey: Princeton University Press. pp.  86–89. ISBN   978-0-691-02873-6.
  20. ↑ Crawford JM, Liver and Biliary Tract. Pathologic Basis of Disease, ed. Kumar V, et al. 2005, Philadelphia: Elsevier Saunders. p. 924
  21. ↑ Nungovitch, Petro Andreas (2018). Here All Is Poland: A Pantheonic History of Wawel, 1787–2010. Lexington Books. p. 214. ISBN   978-1-4985-6913-2.
  22. ↑ Jones, Barry (2018). Dictionary of World Biography. Australian National University Press. p. 154. ISBN   978-1-76046-218-5.
  23. 1 2 Al-Shamahi, Ella (2022). "Tutankhamun: Secrets of the Tomb". Channel 4 . Retrieved 1 June 2023.
  24. 1 2 Cox, Ann M. (7 June 2003). "The death of Lord Carnarvon". Correspondence. The Lancet. 361 (9373). Elsevier Ltd.: 1994. doi:10.1016/S0140-6736(03)13576-3. PMID   12801779. S2CID   45173628 . Retrieved 18 September 2021.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.