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Fusarium and Fusarium Toxins

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

Deadline for manuscript submissions: closed (28 February 2022) | Viewed by 35992

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Dr. Florence Richard-Forget

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INRAE, UR 1264 MycSA Mycologie et Sécurité des Aliments, Centre de recherche Nouvelle-Aquitaine-Bordeaux, Villenave D’Ornon, France
Interests: mycotoxins; toxigenic fungi; Fusarium mycotoxins; Fusarium species; production of mycotoxins; biosynthesis of mycotoxins
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Jens Laurids Sørensen

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Department of Chemistry and Bioscience, Aalborg University, Niels Bohrs Vej 8, 6700 Esbjerg, Denmark

Dr. Linda J. Harris

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Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, Ottawa, Canada

Special Issue Information

Dear Colleagues,

The genus Fusarium is one of the most economically important genera of fungi infecting agricultural crops worldwide, causing not only severe yield losses but also mycotoxin contaminated and health-threatening food and feed commodities. Mycotoxins produced by Fusarium spp., also referred to as Fusarium mycotoxins, encompass a wide range of chemical compounds, including three of the most important mycotoxins (trichothecenes, fumonisins, zearalenone) and so-called “emerging” mycotoxins (enniatins, moniliformin, beauvericin and fusaproliferin). This wide spectrum also encloses modified forms of mycotoxins which occurrence in food and feed matrices in addition to parent forms is increasingly documented.

Increased knowledge regarding the determinants and factors that govern the accumulation of Fusarium mycotoxins in agricultural commodities is still needed to improve the current and future management of the mycotoxin risk associated with crops and guarantee the safety of related feed and food products.

This special issue of Toxins looks forward to receiving contributions, either research papers or reviews, about the most recent significant insights covering (but not limited to) 1) genomic and epigenomic data related to Fusarium spp., 2) the biosynthetic pathways of Fusarium mycotoxins and the molecular mechanisms that regulate their expression, 3) the adaptation and evolution of toxigenic Fusarium spp. under abiotic constraints, 4) the tripartite interactions of host plant – toxigenic Fusarium – microbiota, 5) the chemistry of mycotoxins and the mechanisms of their modification (by the fungus itself, neighbouring microorganisms and the host plant). Papers with regards to new sustainable control and mitigation strategies and new knowledge that will help anticipating the evolution of the mycotoxin associated-risks in response to modifications in agronomic practices and to climate change are also welcome.

Dr. Florence Richard-Forget
Prof. Dr. Jens Laurids Sørensen
Dr. Linda J. Harris
Guest Editors

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Keywords

Fusarium
mycotoxins
trichothecenes
fumonisins
zearalenone
emerging mycotoxins
modified forms of mycotoxins
prevention
mitigation
sustainable agriculture
climate change

Published Papers (11 papers)

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26 pages, 1529 KiB

Open AccessArticle

Impact of a Natural Fusarial Multi-Mycotoxin Challenge on Broiler Chickens and Mitigation Properties Provided by a Yeast Cell Wall Extract and a Postbiotic Yeast Cell Wall-Based Blend

by Manoj B. Kudupoje, Venkataramaiah Malathi and Alexandros Yiannikouris

Toxins 2022, 14(5), 315; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins14050315 - 28 Apr 2022

Cited by 15 | Viewed by 2730

Abstract

Yeast cell wall-based preparations have shown efficacy against Aspergillus-based toxins but have lower impact against type-B trichothecenes. Presently, we investigated a combination of deoxynivalenol (DON), T-2 toxin (T2) and zearalenone (ZEA), and the effect of a yeast cell wall extract (YCWE) and a post-biotic yeast cell wall-based blend (PYCW) with the objectives of preventing mycotoxins’ negative effects in commercial broilers. A total of 720 one-day-old male Cobb broilers were randomly allocated to: (1) control diet, (aflatoxins 6 µg/kg; cyclopiazonic acid 15 µg/kg; fusaric acid 25 µg/kg; fumonisin B1 310 µg/kg); (2) Diet1 + 0.2% YCWE; (3) Diet1 + 0.2% PYCW; (4) Contaminated diet (3.0 mg/kg DON; 2.17 mg/kg 3-acetyldeoxynivalenol; 104 g/kg T2; 79 g/kg ZEA); (5) Diet4 + 0.2% YCWE; and (6) Diet4 + 0.2% PYCW. Naturally contaminated diets adversely affected performance, serum biochemistry, liver function, immune response, altered cecal SCFA goblet cell count and architecture of intestinal villi. These adverse effects were reduced in birds fed PYCW and to a lesser extent YCWE, indicating protection against toxic assault. PYCW yielded better production performance and stimulated liver function, with higher response to NDV and IBV vaccination. Furthermore, mycotoxins were found to affect production outputs when evaluated with the European poultry production efficiency factor compared to control or YCWE and PYCW supplemented treatments. Taken together, YCWE, when complemented with nutritional add-ons (PYCW), could potentiate the remediation of the negative effects from a multi mycotoxins dietary challenge in broiler birds. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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10 pages, 689 KiB

Open AccessCommunication

Trichothecene Genotype Profiling of Wheat Fusarium graminearum Species Complex in Paraguay

by Andrea Alejandra Arrua Alvarenga, Julio César Masaru Iehisa Ouchi, Cinthia Carolina Cazal Martínez, Juliana Moura Mendes, Adans Agustín Colmán, Danilo Fernández Ríos, Pablo David Arrua, Claudia Adriana Barboza Guerreño, Man Mohan Kohli, María Laura Ramírez, Ana Acuña Ruíz, María Magdalena Sarmiento, María Cecilia Ortíz, Adriana Nuñez and Horacio D. Lopez-Nicora

Toxins 2022, 14(4), 257; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins14040257 - 05 Apr 2022

Cited by 4 | Viewed by 3019

Abstract

Paraguay is a non-traditional wheat-producing country in one of the warmest regions in South America. Fusarium Head Blight (FHB) is a critical disease affecting this crop, caused by the Fusarium graminearum species complex (FGSC). A variety of these species produce trichothecenes, including deoxynivalenol (DON) and its acetylated forms (3-ADON and 15-ADON) or nivalenol (NIV). This study characterized the phylogenetic relationships, and chemotype diversity of 28 strains within FGSC collected from wheat fields across different country regions. Phylogenetic analysis based on the sequence of elongation factor-1α gene (EF-1α) from 28 strains revealed the presence of four species in the FGSC: F. graminearum sensu stricto, F. asiaticum, F. meridionale and F. cortaderiae. Ten strains selected for further analysis revealed that all F. graminearum strains were 15-ADON chemotype, while the two strains of F. meridionale and one strain of F. asiaticum were NIV chemotype. Thus, the 15-ADON chemotype of F. graminearum sensu stricto was predominant within the Fusarium strains isolated in the country. This work is the first report of phylogenetic relationships and chemotype diversity among Fusarium strains which will help understand the population diversity of this pathogen in Paraguay. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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13 pages, 7283 KiB

Open AccessArticle

Ecophysiology of Fusarium chaquense a Novel Type A Trichothecene Producer Species Isolated from Natural Grasses

by Maria J. Nichea, Eugenia Cendoya, Miriam Haidukowski, Adriana M. Torres and María L. Ramirez

Toxins 2021, 13(12), 895; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13120895 - 13 Dec 2021

Viewed by 2075

Abstract

Fusarium chaquense, a recently formally described novel species, has been identified as an T-2 toxin (T-2), HT-2 toxin (HT-2) and other toxins producer in natural grasses (Poaceae) from Argentina. The major objective of this study was to describe the effect of water activity (a_W, 0.995, 0.98, 0.95, 0.93 and 0.91), temperature (15, 25 and 30 °C) and incubation time (5, 15 and 25 days) on growth and to evaluate the production of T-2, HT-2 toxins and beauvericin (BEA) by two F. chaquense strains in a grass-based media. The results showed a wide range of conditions for F. chaquense growth and mycotoxin production. Both strains had a maximum growth rate at the highest a_W (0.995) and 25 °C. Regarding mycotoxin production, more T-2 than the other analysed mycotoxins were produced by the two strains. T-2 production was favoured at 0.995 a_W and 30 °C, while HT-2 production at 0.98–0.95 a_W and 15 °C. The maximum levels of BEA were produced at 0.995 a_W and 25–30 °C. Two-dimensional profiles of a_W by temperature interactions were obtained from these data in order to identify areas where conditions indicate a significant risk of mycotoxins accumulation on grass. For its versatility on growth and mycotoxin production in a wide range of a_W and temperatures, F. chaquense would have an adaptive advantage over other Fusarium species, and this would explain its high frequency of isolation in natural grasses grown up in the Chaco wetlands. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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23 pages, 17903 KiB

Open AccessArticle

Molecular Docking and Comparative Inhibitory Efficacy of Naturally Occurring Compounds on Vegetative Growth and Deoxynivalenol Biosynthesis in Fusarium culmorum

by Safa Oufensou, Alessandro Dessì, Roberto Dallocchio, Virgilio Balmas, Emanuela Azara, Paola Carta, Quirico Migheli and Giovanna Delogu

Toxins 2021, 13(11), 759; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13110759 - 26 Oct 2021

Cited by 6 | Viewed by 2573

Abstract

The fungal pathogen Fusarium culmorum causes Fusarium head blight in cereals, resulting in yield loss and contamination of the grain by type B trichothecene mycotoxins such as deoxynivalenol (DON), and its acetylated derivatives. Synthesis of trichothecenes is driven by a trichodiene synthase (TRI5) that converts farnesyl pyrophosphate (FPP) to trichodiene. In this work, 15 naturally occurring compounds that belong to the structural phenol and hydroxylated biphenyl classes were tested in vitro and in planta (durum wheat) to determine their inhibitory activity towards TRI5. In vitro analysis highlighted the fungicidal effect of these compounds when applied at 0.25 mM. Greenhouse assays showed a strong inhibitory activity of octyl gallate 5, honokiol 13 and the combination propyl gallate 4 + thymol 7 on trichothecene biosynthesis. Docking analyses were run on the 3D model of F. culmorum TRI5 containing the inorganic pyrophosphate (PPi) or FPP. Significant ligand affinities with TRI-PPi and TRI-FPP were observed for the same sites for almost all compounds, with 1 and 2 as privileged sites. Octyl gallate 5 and honokiol 13 interacted almost exclusively with sites 1 and 2, by concurrently activating strong H-bonds with common sets of amino acids. These results open new perspectives for the targeted search of naturally occurring compounds that may find practical application in the eco-friendly control of FHB in wheat. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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16 pages, 3174 KiB

Open AccessArticle

Biocontrol Agents Reduce Progression and Mycotoxin Production of Fusarium graminearum in Spikelets and Straws of Wheat

by Lucile Pellan, Cheikh Ahmeth Tidiane Dieye, Noël Durand, Angélique Fontana, Sabine Schorr-Galindo and Caroline Strub

Toxins 2021, 13(9), 597; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13090597 - 27 Aug 2021

Cited by 4 | Viewed by 3095

Abstract

The aim of this study was to evaluate the interactions between wheat plant (spikelets and straws), a strain of mycotoxigenic pathogen Fusarium graminearum and commercial biocontrol agents (BCAs). The ability of BCAs to colonize plant tissue and inhibit the pathogen or its toxin production was observed throughout two phases of the life cycle of pathogens in natural conditions (colonization and survival). All evaluated BCAs showed effective reduction capacities of pathogenic traits. During establishment and the expansion stage, BCAs provoked an external growth reduction of F. graminearum (77–93% over the whole kinetic studied) and mycotoxin production (98–100% over the whole kinetic studied). Internal growth of pathogen was assessed with digital droplet polymerase chain reaction (ddPCR) and showed a very strong reduction in the colonization of the internal tissues of the spikelet due to the presence of BCAs (98% on average). During the survival stage, BCAs prevented the formation of conservation perithecia of the pathogen on wheat straw (between 88 and 98% of perithecia number reduction) and showed contrasting actions on the ascospores they contain, or perithecia production (−95% on average) during survival form. The mechanisms involved in these different interactions between F. graminearum and BCAs on plant matrices at different stages of the pathogen’s life cycle were based on a reduction of toxins, nutritional and/or spatial competition, or production of anti-microbial compounds. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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19 pages, 2470 KiB

Open AccessArticle

Identification and Functional Characterization of the Gene Cluster Responsible for Fusaproliferin Biosynthesis in Fusarium proliferatum

by Asja Ćeranić, Thomas Svoboda, Franz Berthiller, Michael Sulyok, Jonathan Matthew Samson, Ulrich Güldener, Rainer Schuhmacher and Gerhard Adam

Toxins 2021, 13(7), 468; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13070468 - 06 Jul 2021

Cited by 7 | Viewed by 2844

Abstract

The emerging mycotoxin fusaproliferin is produced by Fusarium proliferatum and other related Fusarium species. Several fungi from other taxonomic groups were also reported to produce fusaproliferin or the deacetylated derivative, known as siccanol or terpestacin. Here, we describe the identification and functional characterization of the Fusarium proliferatum genes encoding the fusaproliferin biosynthetic enzymes: a terpenoid synthase, two cytochrome P450s, a FAD-oxidase and an acetyltransferase. With the exception of one gene encoding a CYP450 (FUP2, FPRN_05484), knock-out mutants of the candidate genes could be generated, and the production of fusaproliferin and intermediates was tested by LC-MS/MS. Inactivation of the FUP1 (FPRN_05485) terpenoid synthase gene led to complete loss of fusaproliferin production. Disruption of a putative FAD-oxidase (FUP4, FPRN_05486) did not only affect oxidation of preterpestacin III to terpestacin, but also of new side products (11-oxo-preterpstacin and terpestacin aldehyde). In the knock-out strains lacking the predicted acetyltransferase (FUP5, FPRN_05487) fusaproliferin was no longer formed, but terpestacin was found at elevated levels. A model for the biosynthesis of fusaproliferin and of novel derivatives found in mutants is presented. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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12 pages, 2223 KiB

Open AccessCommunication

Production and Selectivity of Key Fusarubins from Fusarium solani due to Media Composition

by Sebastian Birkedal Kristensen, Tobias Bruun Pedersen, Mikkel Rank Nielsen, Reinhard Wimmer, Jens Muff and Jens Laurids Sørensen

Toxins 2021, 13(6), 376; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13060376 - 25 May 2021

Cited by 5 | Viewed by 2336

Abstract

Natural products display a large structural variation and different uses within a broad spectrum of industries. In this study, we investigate the influence of carbohydrates and nitrogen sources on the production and selectivity of production of four different polyketides produced by Fusarium solani, fusarubin, javanicin, bostrycoidin and anhydrofusarubin. We introduce four different carbohydrates and two types of nitrogen sources. Hereafter, a full factorial design was applied using combinations of three levels of sucrose and three levels of the two types of nitrogen. Each combination displayed different selectivity and production yields for all the compounds of interest. Response surface design was utilized to investigate possible maximum yields for the surrounding combinations of media. It was also shown that the maximum yields were not always the ones illustrating high selectivity, which is an important factor for making purification steps easier. We visualized the production over time for one of the media types, illustrating high yields and selectivity. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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14 pages, 2030 KiB

Open AccessArticle

Detoxification and Excretion of Trichothecenes in Transgenic Arabidopsis thaliana Expressing Fusarium graminearum Trichothecene 3-O-acetyltransferase

by Guixia Hao, Susan McCormick, Helene Tiley and Thomas Usgaard

Toxins 2021, 13(5), 320; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13050320 - 29 Apr 2021

Cited by 7 | Viewed by 2822

Abstract

Fusarium graminearum, the causal agent of Fusarium head blight (FHB), produces trichothecenes including deoxynivalenol (DON), nivalenol (NIV), and 3,7,15-trihydroxy-12,13-epoxytrichothec-9-ene (NX-3). These toxins contaminate grains and cause profound health problems in humans and animals. To explore exploiting a fungal self-protection mechanism in plants, we examined the ability of F. graminearum trichothecene 3-O-acetyltransferase (FgTri101) to detoxify several key trichothecenes produced by F. graminearum: DON, 15-ADON, NX-3, and NIV. FgTri101 was cloned from F. graminearum and expressed in Arabidopsis plants. We compared the phytotoxic effects of purified DON, NIV, and NX-3 on the root growth of transgenic Arabidopsis expressing FgTri101. Compared to wild type and GUS controls, FgTri101 transgenic Arabidopsis plants displayed significantly longer root length on media containing DON and NX-3. Furthermore, we confirmed that the FgTri101 transgenic plants acetylated DON to 3-ADON, 15-ADON to 3,15-diADON, and NX-3 to NX-2, but did not acetylate NIV. Approximately 90% of the converted toxins were excreted into the media. Our study indicates that transgenic Arabidopsis expressing FgTri101 can provide plant protection by detoxifying trichothecenes and excreting the acetylated toxins out of plant cells. Characterization of plant transporters involved in trichothecene efflux will provide novel targets to reduce FHB and mycotoxin contamination in economically important plant crops. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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12 pages, 25768 KiB

Open AccessArticle

Characterization of the Exo-Metabolome of the Emergent Phytopathogen Fusarium kuroshium sp. nov., a Causal Agent of Fusarium Dieback

by Angélica Gutiérrez-Sánchez, Javier Plasencia, Juan L. Monribot-Villanueva, José B. Rodríguez-Haas, Jose Abel López-Buenfil, Clemente J. García-Ávila, Eliel Ruiz-May, Diana Sánchez-Rangel and José A. Guerrero-Analco

Toxins 2021, 13(4), 268; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13040268 - 09 Apr 2021

Cited by 7 | Viewed by 2660

Abstract

Fusarium kuroshium is the fungal symbiont associated with the ambrosia beetle Euwallacea kuroshio, a plague complex that attacks avocado, among other hosts, causing a disease named Fusarium dieback (FD). However, the contribution of F. kuroshium to the establishment of this disease remains unknown. To advance the understanding of F. kuroshium pathogenicity, we profiled its exo-metabolome through metabolomics tools based on accurate mass spectrometry. We found that F. kuroshium can produce several key metabolites with phytotoxicity properties and other compounds with unknown functions. Among the metabolites identified in the fungal exo-metabolome, fusaric acid (FA) was further studied due to its phytotoxicity and relevance as a virulence factor. We tested both FA and organic extracts from F. kuroshium at various dilutions in avocado foliar tissue and found that they caused necrosis and chlorosis, resembling symptoms similar to those observed in FD. This study reports for first-time insights regarding F. kuroshium associated with its virulence, which could lead to the potential development of diagnostic and management tools of FD disease and provides a basis for understanding the interaction of F. kuroshium with its host plants. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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22 pages, 6000 KiB

Open AccessArticle

Multi-Mycotoxin Contamination of Maize Silages in Flanders, Belgium: Monitoring Mycotoxin Levels from Seed to Feed

by Jonas Vandicke, Katrien De Visschere, Maarten Ameye, Siska Croubels, Sarah De Saeger, Kris Audenaert and Geert Haesaert

Toxins 2021, 13(3), 202; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins13030202 - 11 Mar 2021

Cited by 32 | Viewed by 4470

Abstract

Maize silage, which in Europe is the main feed for dairy cattle in winter, can be contaminated by mycotoxins. Mycotoxigenic Fusarium spp. originating from field infections may survive in badly sealed silages or re-infect at the cutting edge during feed-out. In this way, mycotoxins produced in the field may persist during the silage process. In addition, typical silage fungi such as Penicillium spp. and Aspergillus spp. survive in silage conditions and produce mycotoxins. In this research, 56 maize silages in Flanders were sampled over the course of three years (2016–2018). The concentration of 22 different mycotoxins was investigated using a multi-mycotoxin liquid chromatography-tandem mass spectrometry (LC-MS/MS) method, and the presence of DNA of three Fusarium spp. (F. graminearum, F. culmorum and F. verticillioides) was analyzed in a selection of these samples using quantitative polymerase chain reaction (qPCR). Every maize silage contained at least two different mycotoxins. Nivalenol (NIV) and deoxynivalenol (DON) were the most prevalent (both in 97.7% of maize silages), followed by ENN B (88.7%). Concentrations often exceeded the EU recommendations for DON and zearalenone (ZEN), especially in 2017 (21.3% and 27.7% of the maize silages, respectively). No correlations were found between fungal DNA and mycotoxin concentrations. Furthermore, by ensiling maize with a known mycotoxin load in a net bag, the mycotoxin contamination could be monitored from seed to feed. Analysis of these net bag samples revealed that the average concentration of all detected mycotoxins decreased after fermentation. We hypothesize that mycotoxins are eluted, degraded, or adsorbed during fermentation, but certain badly preserved silages are prone to additional mycotoxin production during the stable phase due to oxygen ingression, leading to extremely high toxin levels. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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29 pages, 2616 KiB

Open AccessEditor’s ChoiceReview

Bioprospecting Phenols as Inhibitors of Trichothecene-Producing Fusarium: Sustainable Approaches to the Management of Wheat Pathogens

by Wiem Chtioui, Virgilio Balmas, Giovanna Delogu, Quirico Migheli and Safa Oufensou

Toxins 2022, 14(2), 72; https://0-doi-org.brum.beds.ac.uk/10.3390/toxins14020072 - 20 Jan 2022

Cited by 21 | Viewed by 4980

Abstract

Fusarium spp. are ubiquitous fungi able to cause Fusarium head blight and Fusarium foot and root rot on wheat. Among relevant pathogenic species, Fusarium graminearum and Fusarium culmorum cause significant yield and quality loss and result in contamination of the grain with mycotoxins, mainly type B trichothecenes, which are a major health concern for humans and animals. Phenolic compounds of natural origin are being increasingly explored as fungicides on those pathogens. This review summarizes recent research activities related to the antifungal and anti-mycotoxigenic activity of natural phenolic compounds against Fusarium, including studies into the mechanisms of action of major exogenous phenolic inhibitors, their structure-activity interaction, and the combined effect of these compounds with other natural products or with conventional fungicides in mycotoxin modulation. The role of high-throughput analysis tools to decipher key signaling molecules able to modulate the production of mycotoxins and the development of sustainable formulations enhancing potential inhibitors’ efficacy are also discussed. Full article

(This article belongs to the Special Issue Fusarium and Fusarium Toxins)

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