Mark Busman

National Center for Agricultural Utilization Research

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Robert H. Proctor

National Center for Agricultural Utilization Research

Susan P. McCormick

National Center for Agricultural Utilization Research

Kerry O’Donnell

Agricultural Research Service

Daren W. Brown

National Center for Agricultural Utilization Research

Hye-Seon Kim

National Center for Agricultural Utilization Research

Imane Laraba

National Center for Agricultural Utilization Research

Martha Vaughan

National Center for Agricultural Utilization Research

Chris M. Maragos

Agricultural Research Service

Silvio Uhlig

Norwegian Veterinary Institute

Todd J. Ward

Agricultural Research Service

Cooperative Institutions

Agricultural Research Service

United States Department of Agriculture

National Center for Agricultural Utilization Research

Medical University of South Carolina

Plant (United States)

National Oceanic and Atmospheric Administration

Michigan State University

University of California, Davis

Cornell University

University of Wisconsin–Madison

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Phylogenomic Analysis of a 55.1-kb 19-Gene Dataset Resolves a MonophyleticFusariumthat Includes theFusarium solaniSpecies Complex

Phytopathology (2020)

David M. Geiser Abdullah M. S. Al‐Hatmi Takayuki Aoki Tsutomu Arie Virgilio Balmas

Scientific communication is facilitated by a data-driven, scientifically sound taxonomy that considers the end-user's needs and established successful practice. In 2013, the Fusarium community voiced near unanimous support for a concept of Fusarium that represented a clade comprising all agriculturally and clinically important Fusarium species, including the F. solani species complex (FSSC). Subsequently, this concept was challenged in 2015 by one research group who proposed dividing the genus Fusarium into seven genera, including the FSSC described as members of the genus Neocosmospora, with subsequent justification in 2018 based on claims that the 2013 concept of Fusarium is polyphyletic. Here, we test this claim and provide a phylogeny based on exonic nucleotide sequences of 19 orthologous protein-coding genes that strongly support the monophyly of Fusarium including the FSSC. We reassert the practical and scientific argument in support of a genus Fusarium that includes the FSSC and several other basal lineages, consistent with the longstanding use of this name among plant pathologists, medical mycologists, quarantine officials, regulatory agencies, students, and researchers with a stake in its taxonomy. In recognition of this monophyly, 40 species described as genus Neocosmospora were recombined in genus Fusarium, and nine others were renamed Fusarium. Here the global Fusarium community voices strong support for the inclusion of the FSSC in Fusarium, as it remains the best scientific, nomenclatural, and practical taxonomic option available.

Monophyly

Polyphyly

Fusarium solani

10.1094/phyto-08-20-0330-le

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Citations (156)

Fusarium subtropicale, sp. nov., a novel nivalenol mycotoxin–producing species isolated from barley (Hordeum vulgare) in Brazil and sister to F. praegraminearum

Mycologia (2018)

Carolina Bertuzzi Pereira Todd J. Ward Dauri José Tessmann Emerson M. Del Ponte Imane Laraba

Surveys were conducted in commercial wheat and barley fields in the south central production regions of state of Paraná, Brazil, from 2011 to 2015. Spikes displaying visible Fusarium head blight symptoms were collected and the pathogen isolated from the tissues. The 754 Fusarium isolates recovered were identified by a high-throughput multilocus genotyping assay (MLGT) designed to identify trichothecene toxin–producing fusaria (i.e., formerly B-clade, but referred to here as F. sambucinum species complex lineage 1 [FSAMSC-1]) together with sequencing a portion of the translation elongation factor 1-α (TEF1) gene. One strain was discovered that appeared to be closely related to but phylogenetically distinct from F. praegraminearum based on the relatively low 97.7% TEF1 identity and positive genotype obtained with one of the two F. praegraminearum species–specific MLGT probes. Molecular phylogenetic analyses of a 10-gene data set resolved this novel FSAMSC-1 species and F. praegraminearum as sisters. Formally described herein as F. subtropicale, it is phenotypically distinct from the 22 other FSAMSC-1 species in that it produces mostly 1–3-septate macroconidia. Whole-genome sequence data were used to predict its potential to produce mycotoxins. Chemical analyses confirmed that F. subtropicale could produce the mycotoxins 4,15-diacetylnivalenol, butenolide, culmorin, and fusarin C in vitro, and the pathogenicity experiment revealed that F. subtropicale could infect but not spread in susceptible hard red spring wheat cultivar “Norm.”

Species complex

10.1080/00275514.2018.1512296

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Citations (11)

Fusarium verticillioides chitin synthases CHS5 and CHS7 are required for normal growth and pathogenicity

Current Genetics (2011)

Troy M. Larson David F. Kendra Mark Busman Daren W. Brown

Chitin synthase

10.1007/s00294-011-0334-6

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Citations (46)

Marasas et al. 1984 “Toxigenic Fusarium Species: Identity and Mycotoxicology” revisited

Figshare (2018)

Kerry O’Donnell Susan P. McCormick Mark Busman Robert H. Proctor Todd J. Ward

This study was conducted to determine the species identity and mycotoxin potential of 158 Fusarium strains originally archived in the South African Medical Research Council’s Mycotoxigenic Fungal Collection (MRC) that were reported to comprise 17 morphologically distinct species in the classic 1984 compilation by Marasas et al., Toxigenic Fusarium Species: Identity and Mycotoxicology. Maximum likelihood and maximum parsimony molecular phylogenetic analyses of single and multilocus DNA sequence data indicated that the strains represented 46 genealogically exclusive phylogenetically distinct species distributed among eight species complexes. Moreover, the phylogenetic data revealed that 80/158 strains were received under a name that is not accepted today (ex F. moniliforme) or classified under a different species name. In addition, gas chromatography–mass spectrometry (GC-MS) and/or high-performance liquid chromatography–mass spectrometry (HPLC-MS)-based mycotoxin analyses were conducted to determine which toxins the strains could produce in liquid and/or solid cultures. All of the trichothecene toxin–producing fusaria were nested within the F. sambucinum (FSAMSC) or F. incarnatum-equiseti (FIESC) species complexes. Consistent with this finding, GC-MS analyses detected trichothecenes in agmatine-containing broth or rice culture extracts of all 13 FSAMSC and 10/12 FIESC species tested. Species in six and seven of the eight species complexes were able to produce moniliformin and beauvericin, respectively, whereas B-type fumonisins were only detected in extracts of cracked maize kernel cultures of three species in the F. fujikuroi (FFSC) species complex.

10.6084/m9.figshare.7390385

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Production and characterization of a monoclonal antibody that cross-reacts with the mycotoxins nivalenol and 4-deoxynivalenol

Food Additives & Contaminants (2006)

Chris M. Maragos Mark Busman Yoshiko Sugita‐Konishi

Nivalenol is a mycotoxin produced by certain fungi that are pathogenic to important cereal crops, in particular maize, wheat, and barley. This toxin, 3alpha,4beta,7alpha,15-tetrahydroxy-12,13-epoxytrichothec-9-en-8-one, is found worldwide and is closely related to 4-deoxynivalenol (DON or vomitoxin), a mycotoxin associated with outbreaks of Fusarium head blight in North America. The literature on the toxicity of nivalenol suggests it is similar, if not more toxic, than DON. Despite the development of rapid immunologically based assays for detecting DON, such assays have not existed for detecting nivalenol without chemical modification of the analyte. This paper describes the development of a monoclonal antibody using a nivalenol-glycine protein conjugate. The monoclonal antibody was most specific for an acetylated form of DON (3-Ac-DON), but it exhibited sensitivity and cross-reactivity that were useful for detecting nivalenol and DON at relevant levels without the need to modify either toxin chemically. In an competitive indirect ELISA format, the concentrations of toxins able to inhibit colour development by 50% (IC50) were 1.7, 15.8, 27.5, 68.9, and 1740 ng ml(-1) for the mycotoxins 3-Ac-DON, DON, nivalenol, 15-Ac-DON, and fusarenon-X, respectively. The antibody was also used to develop a competitive direct ELISA for DON and nivalenol, with IC50's of 16.5 ng ml(-1) (DON) and 33.4 ng ml(-1) (nivalenol). These assays are capable of detecting both DON and nivalenol simultaneously, a property that may be useful in regions where these toxins co-occur or in formats, such as immunoaffinity columns, where co-isolation of both toxins is desirable.

10.1080/02652030600699072

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Citations (44)

Identification of Early Fumonisin Biosynthetic Intermediates by Inactivation of the FUM6 Gene in Fusarium verticillioides

Journal of Agricultural and Food Chemistry (2012)

Silvio Uhlig Mark Busman Deborah S. Shane Helene Thorsen Rønning Frode Rise

Fumonisins are polyketide mycotoxins produced by the maize pathogen Fusarium verticillioides and are associated with multiple human and animal diseases. A fumonisin biosynthetic pathway has been proposed, but structures of early pathway intermediates have not been demonstrated. The F. verticillioides FUM6 gene is required for an early pathway step. Here, metabolites produced by strains of the fungus with an inactivated FUM6 gene were purified and shown by mass spectrometry and NMR spectroscopy to have fumonisin-like structures but without substitutions at C-14 and C-15. The major metabolite was 2-amino-12,16-dimethylicosane-3,10-diol. Lesser amounts of 3-keto and triol analogues of the metabolite were also identified. In precursor feeding experiments, 2-amino-12,16-dimethylicosane-3,10-diol was transformed to fumonisins by a F. verticillioides strain with an inactive fumonisin polyketide synthase gene. The results support the hypothesis that the FUM6-encoded enzyme catalyzes fumonisin C-14 and C-15 hydroxylation and provide direct spectroscopic and biochemical evidence for structures of early intermediates in fumonisin biosynthesis.

Fumonisin

Hydroxylation

Polyketide synthase

Metabolic pathway

10.1021/jf302967b

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Citations (22)

Variation in sequence and location of the fumonisin mycotoxin niosynthetic gene cluster in Fusarium

Gewasbescherming (2010)

Robert H. Proctor François Van Hove Antonia Susca A. Stea Mark Busman

In Fusarium, the ability to produce fumonisins is governed by a 17-gene fumonisin biosynthetic gene (FUM) cluster. Here, we examined the cluster in F. oxysporum strain O-1890 and nine other species selected to represent a wide range of the genetic diversity within the GFSC.

Gene cluster

Fumonisin

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LC-MS/MS method for the determination of the fungal pigment bikaverin in maize kernels as an indicator of ear rot

Food Additives & Contaminants Part A (2012)

Mark Busman Robert A. E. Butchko Robert H. Proctor

Bikaverin is a polyketide-derived pigment produced by multiple species of the fungus Fusarium, some of which can cause ear and kernel rot of maize. A method was developed for the analysis of bikaverin by high-performance liquid chromatography (LC) coupled to electrospray ionisation tandem mass spectrometry (MS/MS). The quantitative nature of the LC-MS/MS method was demonstrated over a range of concentrations of bikaverin in maize. For spike-recovery experiments utilising maize spiked with bikaverin to a level 5 µg g⁻¹ of maize, the measured recovery (%) was 70.6 ± 10.4. Based on the utilised method, the limit of detection (based on a signal-to-noise ratio (S/N) > 3) was better than 0.5 µg g⁻¹ from bikaverin spiked into uncontaminated ground maize. Further, the limit of quantitation (LOQ) was 3 µg g⁻¹ (based on S/N > 10) from bikaverin spiked into ground maize. The method was applied to assess contamination of maize with bikaverin following inoculation of developing maize ears with Fusarium verticillioides under agricultural field conditions.

10.1080/19440049.2012.704528

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Citations (21)

Reducing production of fumonisin mycotoxins in Fusarium verticillioides by RNA interference

Mycotoxin Research (2017)

Eric T. Johnson Robert H. Proctor Christopher A. Dunlap Mark Busman

Fumonisin

Gene cluster

10.1007/s12550-017-0296-8

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Citations (27)

Low aflatoxin levels and flowering delay inAspergillus flavus-resistant maize lines are correlated with increased corn earworm damage and enhanced seed fumonisin content

bioRxiv (Cold Spring Harbor Laboratory) (2020)

Chalivendra C. Subbaiah Fangneng Huang Mark Busman W. Paul Williams Jong Hyun Ham

ABSTRACT Preharvest mycotoxin contamination of field-grown crops is influenced not only by the host genotype, but also inoculum load, insect pressure and their confounding interactions with seasonal weather. In two field trials, we observed a preferred natural infestation of specific maize ( Zea mays L.) genotypes by corn earworm ( Helicoverpa zea Boddie) and investigated this unexpected interaction. These studies involved four maize lines with contrasting levels of resistance to Aspergillus flavus . The resistant lines had 7 to 14-fold greater infested ears than the susceptible lines. However, seed aflatoxin B 1 levels, in mock- or A. flavus -inoculated ears were consistent with maize genotype resistance to A. flavus . Further, the corn earworm-infested ears had greater levels of fumonisin content in seeds than uninfested ears, indicating that the insect may have vectored native Fusarium verticillioides inoculum. The two maize lines with heavy infestation showed delayed flowering. The availability of young silk for egg-laying could have been a factor in the pervasive corn earworm damage of these lines. At the same time, H. zea larvae reared on AF-infused diet showed decreasing mass with increasing AF and >30% lethality at 250 ppb. In contrast, corn earworm was tolerant to fumonisin with no significant loss in mass even at 100 ppm, implicating the low seed aflatoxin content as a predominant factor for the prevalence of corn earworm infestation and the associated fumonisin contamination in A. flavus resistant lines. These results highlight the need for integrated strategies targeting mycotoxigenic fungi and their insect vectors to enhance the safety of crop commodities. IMPORTANCE Aspergillus and Fusarium spp. not only cause ear rots in maize leading to crop loss, they can also contaminate the grain with carcinogenic mycotoxins. Incorporation of genetic resistance into breeding lines is an ideal solution for mycotoxin mitigation. However, the goal is fraught by a major problem. Resistance for AF or FUM accumulation is quantitative and contributed by several loci with small effects. Our work reveals that host phenology (flowering time) and insect vector-mycotoxin interactions can further confound breeding efforts. A host genotype even with demonstrable resistance can become vulnerable due to seasonal variation in flowering time or an outbreak of chewing insects. Incorporation of resistance to a single mycotoxin accumulation and not pairing it with insect resistance may not adequately ensure food safety. Diverse strategies including host-induced silencing of genes essential for fungal and insect pest colonization and broad-spectrum biocontrol systems need to be considered for robust mycotoxin mitigation.

Helicoverpa zea

Fumonisin

Preharvest

10.1101/2020.02.03.933309

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Citations (2)