New Insight into Fusarium Toxins and Aflatoxins

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Mycotoxins".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 25476

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Molecular Plant Biology, Department of Biochemistry, University of Turku, FI-20520 Turku, Finland
Interests: fungal species; Fusarium and Aspergillus species; fungi used in biological control; toxigenic fungi
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Special Issue Information

Dear Colleagues,

Besides the direct plant yield losses due to Fusarium infection, the concern of grain contamination by Fusarium toxins arises from their frequent occurrence at toxicologically relevant levels. The main toxins produced by Fusarium species are fumonisins and trichothecenes. The most important fumonisin producer is F. verticillioides. The most important trichothecenes are deoxynivalenol (DON) and T-2-toxin. F. graminearum is the most important DON producer, while F. langsethiae is the most importan T-2-toxin producer. In addition, zearalenone (ZON), moniliformin (MON) and enniatins (ENNs), including beauvericin (BEA), are produced by different Fusarium species.

The alimentary toxic aleukia (ATA) outbreaks in Russia were probably due to T-2 toxin-producing Fusarium species. Grains and processed grains, which are used as feed- and food-stuffs, might retain their original toxin levels as “harvested” from the field but might be altered in concentration and nature, giving rise to modified Fusarium toxins with changed toxicological properties. Interactions between Fusarium toxins should also be taken into consideration.

Aflatoxins, which are produced by Aspergillus species, are a group of polyketide-derived furanocoumarins and the most carcinogenic compounds among the known mycotoxins. At least 34 genes have been identified in the aflatoxin biosynthesis pathway. The pathway genes involved in aflatoxin production are clustered in fungi, which enables coordination of their transcriptional activation and regulation. The aflatoxin gene cluster presents at least one specific regulatory gene—aflR encoding a protein— an AflR that binds to the promoter of biosynthetic genes and assists in recruiting RNA polymerase II to initiate transcription.

The molecular study of biosynthetic pathways can help elucidate the mechanisms underlying fungal toxin production and enables the development of new effective approaches to control fungal toxicity.

Prof. Dr. Tapani Yli-Mattila
Guest Editor

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Keywords

  • genetics
  • pathways
  • transcriptomics
  • proteomis
  • fumonisins
  • triichothecenes
  • aflatoxins

Published Papers (6 papers)

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Research

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14 pages, 2116 KiB  
Article
Biocontrol of Fusarium graminearum, a Causal Agent of Fusarium Head Blight of Wheat, and Deoxynivalenol Accumulation: From In Vitro to In Planta
by Asmaa Abbas and Tapani Yli-Mattila
Toxins 2022, 14(5), 299; https://doi.org/10.3390/toxins14050299 - 22 Apr 2022
Cited by 12 | Viewed by 3874
Abstract
Crop diseases caused by Fusarium graminearum threaten crop production in both commercial and smallholder farming. F. graminearum produces deoxynivalenol mycotoxin, which is stable during food and feed processing. Therefore, the best way to prevent the sporulation of pathogens is to develop new [...] Read more.
Crop diseases caused by Fusarium graminearum threaten crop production in both commercial and smallholder farming. F. graminearum produces deoxynivalenol mycotoxin, which is stable during food and feed processing. Therefore, the best way to prevent the sporulation of pathogens is to develop new prevention strategies. Plant-based pesticides, i.e., natural fungicides, have recently gained interest in crop protection as alternatives to synthetic fungicides. Herein we show that treatment with the methanolic extract of medicinal plant Zanthoxylum bungeanum (M20 extract), decreased F. graminearum growth and abrogated DON production. The F. graminearum DNA levels were monitored by a quantitative TaqMan real-time PCR, while DON accumulation was assessed by HPLC quantification. This M20 extract was mainly composed of four flavonoids: quercetin, epicatechin, kaempferol-3-O-rhamnoside, and hyperoside. The in vitro bioassay, which measured the percent inhibition of fungal growth, showed that co-inoculation of four F. graminearum strains with the M20 extract inhibited the fungal growth up to 48.5%. After biocontrol treatments, F. graminearum DNA level was reduced up to 85.5% compared to that of wheat heads, which received F. graminearum mixture only. Moreover, DON production was decreased in wheat heads by 73% after biocontrol treatment; meanwhile in wheat heads inoculated with F. graminearum conidia, an average of 2.263 ± 0.8 mg/kg DON was detected. Overall, this study is a successful case from in vitro research to in planta, giving useful information for wheat protection against F. graminearum responsible for Fusarium Head Blight and DON accumulation in grains. Further studies are needed to study the mechanism by which M20 extract inhibited the DON production and what changes happened to the DON biosynthetic pathway genes. Full article
(This article belongs to the Special Issue New Insight into Fusarium Toxins and Aflatoxins)
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19 pages, 2769 KiB  
Article
Volatile Organic Compounds Emitted by Aspergillus flavus Strains Producing or Not Aflatoxin B1
by Laurie Josselin, Caroline De Clerck, Marthe De Boevre, Antonio Moretti, M. Haïssam Jijakli, Hélène Soyeurt and Marie-Laure Fauconnier
Toxins 2021, 13(10), 705; https://doi.org/10.3390/toxins13100705 - 06 Oct 2021
Cited by 14 | Viewed by 2689
Abstract
Aspergillus flavus is a phytopathogenic fungus able to produce aflatoxin B1 (AFB1), a carcinogenic mycotoxin that can contaminate several crops and food commodities. In A. flavus, two different kinds of strains can co-exist: toxigenic and non-toxigenic strains. Microbial-derived volatile organic compounds (mVOCs) [...] Read more.
Aspergillus flavus is a phytopathogenic fungus able to produce aflatoxin B1 (AFB1), a carcinogenic mycotoxin that can contaminate several crops and food commodities. In A. flavus, two different kinds of strains can co-exist: toxigenic and non-toxigenic strains. Microbial-derived volatile organic compounds (mVOCs) emitted by toxigenic and non-toxigenic strains of A. flavus were analyzed by solid phase microextraction (SPME) coupled with gas chromatography–mass spectrometry (GC-MS) in a time-lapse experiment after inoculation. Among the 84 mVOCs emitted, 44 were previously listed in the scientific literature as specific to A. flavus, namely alcohols (2-methylbutan-1-ol, 3-methylbutan-1-ol, 2-methylpropan-1-ol), aldehydes (2-methylbutanal, 3-methylbutanal), hydrocarbons (toluene, styrene), furans (2,5-dimethylfuran), esters (ethyl 2-methylpropanoate, ethyl 2-methylbutyrate), and terpenes (epizonaren, trans-caryophyllene, valencene, α-copaene, β-himachalene, γ-cadinene, γ-muurolene, δ-cadinene). For the first time, other identified volatile compounds such as α-cadinol, cis-muurola-3,5-diene, α-isocomene, and β-selinene were identified as new mVOCs specific to the toxigenic A. flavus strain. Partial Least Square Analysis (PLSDA) showed a distinct pattern between mVOCs emitted by toxigenic and non-toxigenic A. flavus strains, mostly linked to the diversity of terpenes emitted by the toxigenic strains. In addition, the comparison between mVOCs of the toxigenic strain and its non-AFB1-producing mutant, coupled with a semi-quantification of the mVOCs, revealed a relationship between emitted terpenes (β-chamigrene, α-corocalene) and AFB1 production. This study provides evidence for the first time of mVOCs being linked to the toxigenic character of A. flavus strains, as well as terpenes being able to be correlated to the production of AFB1 due to the study of the mutant. This study could lead to the development of new techniques for the early detection and identification of toxigenic fungi. Full article
(This article belongs to the Special Issue New Insight into Fusarium Toxins and Aflatoxins)
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18 pages, 1424 KiB  
Article
Fusarium verticillioides and Aspergillus flavus Co-Occurrence Influences Plant and Fungal Transcriptional Profiles in Maize Kernels and In Vitro
by Alessandra Lanubile, Paola Giorni, Terenzio Bertuzzi, Adriano Marocco and Paola Battilani
Toxins 2021, 13(10), 680; https://doi.org/10.3390/toxins13100680 - 24 Sep 2021
Cited by 10 | Viewed by 2457
Abstract
Climate change will increase the co-occurrence of Fusarium verticillioides and Aspergillus flavus, along with their mycotoxins, in European maize. In this study, the expression profiles of two pathogenesis-related (PR) genes and four mycotoxin biosynthetic genes, FUM1 and FUM13, fumonisin [...] Read more.
Climate change will increase the co-occurrence of Fusarium verticillioides and Aspergillus flavus, along with their mycotoxins, in European maize. In this study, the expression profiles of two pathogenesis-related (PR) genes and four mycotoxin biosynthetic genes, FUM1 and FUM13, fumonisin pathway, and aflR and aflD, aflatoxin pathway, as well as mycotoxin production, were examined in kernels and in artificial medium after a single inoculation with F. verticillioides or A. flavus or with the two fungi in combination. Different temperature regimes (20, 25 and 30 °C) over a time-course of 21 days were also considered. In maize kernels, PR genes showed the strongest induction at 25 °C in the earlier days post inoculation (dpi)with both fungi inoculated singularly. A similar behaviour was maintained with fungi co-occurrence, but with enhanced defence response at 9 dpi under 20 °C. Regarding FUM genes, in the kernels inoculated with F. verticillioides the maximal transcript levels occurred at 6 dpi at 25 °C. At this temperature regime, expression values decreased with the co-occurrence of A. flavus, where the highest gene induction was detected at 20 °C. Similar results were observed in fungi grown in vitro, whilst A. flavus presence determined lower levels of expression along the entire time-course. As concerns afl genes, considering both A. flavus alone and in combination, the most elevated transcript accumulation occurred at 30 °C during all time-course both in infected kernels and in fungi grown in vitro. Regarding mycotoxin production, no significant differences were found among temperatures for kernel contamination, whereas in vitro the highest production was registered at 25 °C for aflatoxin B1 and at 20 °C for fumonisins in the case of single inoculation. In fungal co-occurrence, both mycotoxins resulted reduced at all the temperatures considered compared to the amount produced with single inoculation. Full article
(This article belongs to the Special Issue New Insight into Fusarium Toxins and Aflatoxins)
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16 pages, 1897 KiB  
Article
Population Genetic Structure and Chemotype Diversity of Fusarium graminearum Populations from Wheat in Canada and North Eastern United States
by Abbot O. Oghenekaro, Maria A. Oviedo-Ludena, Mitra Serajazari, Xiben Wang, Maria A. Henriquez, Nancy G. Wenner, Gretchen A. Kuldau, Alireza Navabi, Hadley R. Kutcher and W. G. Dilantha Fernando
Toxins 2021, 13(3), 180; https://doi.org/10.3390/toxins13030180 - 01 Mar 2021
Cited by 11 | Viewed by 4296
Abstract
Fusarium head blight (FHB) is a major disease in wheat causing severe economic losses globally by reducing yield and contaminating grain with mycotoxins. In Canada, Fusarium graminearum is the principal etiological agent of FHB in wheat, producing mainly the trichothecene mycotoxin, deoxynivalenol (DON) [...] Read more.
Fusarium head blight (FHB) is a major disease in wheat causing severe economic losses globally by reducing yield and contaminating grain with mycotoxins. In Canada, Fusarium graminearum is the principal etiological agent of FHB in wheat, producing mainly the trichothecene mycotoxin, deoxynivalenol (DON) and its acetyl derivatives (15-acetyl deoxynivalenol (15ADON) and 3-acetyl deoxynivalenol (3ADON)). Understanding the population biology of F. graminearum such as the genetic variability, as well as mycotoxin chemotype diversity among isolates is important in developing sustainable disease management tools. In this study, 570 F. graminearum isolates collected from commercial wheat crops in five geographic regions in three provinces in Canada in 2018 and 2019 were analyzed for population diversity and structure using 10 variable number of tandem repeats (VNTR) markers. A subset of isolates collected from the north-eastern United States was also included for comparative analysis. About 75% of the isolates collected in the Canadian provinces of Saskatchewan and Manitoba were 3ADON indicating a 6-fold increase in Saskatchewan and a 2.5-fold increase in Manitoba within the past 15 years. All isolates from Ontario and those collected from the United States were 15ADON and isolates had a similar population structure. There was high gene diversity (H = 0.803–0.893) in the F. graminearum populations in all regions. Gene flow was high between Saskatchewan and Manitoba (Nm = 4.971–21.750), indicating no genetic differentiation between these regions. In contrast, less gene flow was observed among the western provinces and Ontario (Nm = 3.829–9.756) and USA isolates ((Nm = 2.803–6.150). However, Bayesian clustering model analyses of trichothecene chemotype subpopulations divided the populations into two clusters, which was correlated with trichothecene types. Additionally, population cluster analysis revealed there was more admixture of isolates among isolates of the 3ADON chemotypes than among the 15ADON chemotype, an observation that could play a role in the increased virulence of F. graminearum. Understanding the population genetic structure and mycotoxin chemotype variations of the pathogen will assist in developing FHB resistant wheat cultivars and in mycotoxin risk assessment in Canada. Full article
(This article belongs to the Special Issue New Insight into Fusarium Toxins and Aflatoxins)
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Review

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16 pages, 372 KiB  
Review
Fumonisins in African Countries
by Tapani Yli-Mattila and Leif Sundheim
Toxins 2022, 14(6), 419; https://doi.org/10.3390/toxins14060419 - 19 Jun 2022
Cited by 6 | Viewed by 3152
Abstract
Maize and other cereals are the commodities most contaminated with fumonisins. The maize acreage is increasing in Africa, and the maize harvest provides important foods for humans and feeds for domestic animals throughout the continent. In North Africa, high levels of fumonisins have [...] Read more.
Maize and other cereals are the commodities most contaminated with fumonisins. The maize acreage is increasing in Africa, and the maize harvest provides important foods for humans and feeds for domestic animals throughout the continent. In North Africa, high levels of fumonisins have been reported from Algeria and Morocco, while low levels have been detected in the rather few fumonisin analyses reported from Tunisia and Egypt. The West African countries Burkina Faso, Cameroon, Ghana, and Nigeria all report high levels of fumonisin contamination of maize, while the few maize samples analysed in Togo contain low levels. In Eastern Africa, high levels of fumonisin contamination have been reported from the Democratic Republic of Congo, Ethiopia, Kenya, Tanzania, and Uganda. The samples analysed from Rwanda contained low levels of fumonisins. Analysis of maize from the Southern African countries Malawi, Namibia, South Africa, Zambia, and Zimbabwe revealed high fumonisin levels, while low levels of fumonisins were detected in the few analyses of maize from Botswana and Mozambique. Full article
(This article belongs to the Special Issue New Insight into Fusarium Toxins and Aflatoxins)
24 pages, 1278 KiB  
Review
Aflatoxin Contamination, Its Impact and Management Strategies: An Updated Review
by Saba Shabeer, Shahzad Asad, Atif Jamal and Akhtar Ali
Toxins 2022, 14(5), 307; https://doi.org/10.3390/toxins14050307 - 27 Apr 2022
Cited by 57 | Viewed by 7632
Abstract
Aflatoxin, a type of mycotoxin, is mostly produced by Aspergillus flavus and Aspergillus parasiticus. It is responsible for the loss of billions of dollars to the world economy, by contaminating different crops such as cotton, groundnut, maize, and chilies, and causing immense effects [...] Read more.
Aflatoxin, a type of mycotoxin, is mostly produced by Aspergillus flavus and Aspergillus parasiticus. It is responsible for the loss of billions of dollars to the world economy, by contaminating different crops such as cotton, groundnut, maize, and chilies, and causing immense effects on the health of humans and animals. More than eighteen different types of aflatoxins have been reported to date, and among them, aflatoxins B1, B2, G1, and G2 are the most prevalent and lethal. Early detection of fungal infection plays a key role in the control of aflatoxin contamination. Therefore, different methods, including culture, chromatographic techniques, and molecular assays, are used to determine aflatoxin contamination in crops and food products. Many countries have set a maximum limit of aflatoxin contamination (2–20 ppb) in their food and agriculture commodities for human or animal consumption, and the use of different methods to combat this menace is essential. Fungal infection mostly takes place during the pre- and post-harvest stage of crops, and most of the methods to control aflatoxin are employed for the latter phase. Studies have shown that if correct measures are adopted during the crop development phase, aflatoxin contamination can be reduced by a significant level. Currently, the use of bio-pesticides is the intervention employed in many countries, whereby atoxigenic strains competitively reduce the burden of toxigenic strains in the field, thereby helping to mitigate this problem. This updated review on aflatoxins sheds light on the sources of contamination, and the on occurrence, impact, detection techniques, and management strategies, with a special emphasis on bio-pesticides to control aflatoxins. Full article
(This article belongs to the Special Issue New Insight into Fusarium Toxins and Aflatoxins)
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